Abstract
Frequent marine oil spills have led to increasingly serious oil pollution along shorelines. Microbial remediation has become a research hotspot of intertidal oil pollution remediation because of its high efficiency, low cost, environmental friendliness, and simple operation. Many microorganisms are able to convert oil pollutants into non-toxic substances through their growth and metabolism. Microorganisms use enzymes’ catalytic activities to degrade oil pollutants. However, microbial remediation efficiency is affected by the properties of the oil pollutants, microbial community, and environmental conditions. Feasible field microbial remediation technologies for oil spill pollution in the shorelines mainly include the addition of high-efficiency oil degrading bacteria (immobilized bacteria), nutrients, biosurfactants, and enzymes. Limitations to the field application of microbial remediation technology mainly include slow start-up, rapid failure, long remediation time, and uncontrolled environmental impact. Improving the environmental adaptability of microbial remediation technology and developing sustainable microbial remediation technology will be the focus of future research. The feasibility of microbial remediation techniques should also be evaluated comprehensively.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
With the continuous expansion of the offshore oil drilling, resource exploration, transportation, and other industrial activities, the marine environment and ecosystems have suffered from serious oil pollution (Lee et al. 2015). According to statistics, from 1970 to 2016 there were more than 460 large-scale oil spills (spill amount > 700 tonnes) around the world (ITOPF 2016), with a total oil spill of more than 5.734 million tons, making oil spills the second largest marine disaster after red tides (Garcia-Olivares et al. 2017). Once an ocean oil spill occurs, a large amount of oil spreads making oil spills and invades the whole shorelines rapidly under the action of currents and wind. The oil continuously penetrates into the deep layer via adsorption by shoreline sediments (Bejarano and Michel 2016), resulting in large-scale and persistent oil pollution along the shorelines. For example, in 2010, the Deepwater Horizon (DWH) blowout released 3.19 million barrels (435,000 tons) of crude oil into the Gulf of Mexico, resulting in approximately 22,000 tons of leaked oil settling on the northeastern coastline of the Gulf (Geng et al. 2021). Shorelines are not only buffer regions for the exchange of materials and energy between the sea and land but also habitats for a large number of sea and land animals/microorganisms (Barbier et al. 2011; Wang et al. 2020a). After oil spill accidents, the biodiversity of metazoan small animals and vertebrates significantly decreases (Table 1). In addition, the shorelines undergo frequent dry and wet alternation, which makes it more difficult to remediate. Therefore, once oil spill pollution occurs, it seriously impacts the ecological environment of the shorelines for a long period of time (Lv et al. 2020; Zhang et al. 2019a). As such, there is an urgent need for efficient remediation technologies for heavy oil pollution along the shorelines.
Conventional treatments for oil pollution in the shorelines include physical, chemical, and biological remediation approaches (Agarwala and Liu 2015). Among them, chemical remediation is likely to cause secondary pollution, while physical remediation is very expensive and is mainly used in emergency situations (Daccò et al. 2020). In addition, physical and chemical remediation cannot completely degrade the contaminating crude oil (Agarwala and Liu 2015; Daccò et al. 2020; Lim et al. 2016). Therefore, bioremediation offers a more efficient oil pollution treatment approach, with the advantages of safety, high efficiency, economy, simple operation, and no secondary pollution (Daccò et al. 2020; Pi et al. 2015).
Microbial remediation is the process of using microorganisms to degrade, remove, or detoxify pollutants in the environment, in order to restore normal ecosystem function (Megharaj et al. 2011; Ron and Rosenberg 2014). Research on the migration, transformation, and behavior fate of oil pollutants in marine environments has shown that microbial degradation is the most important and fundamental mechanism to achieve the removal of oil pollutants (Fuentes et al. 2014; Lawniczak et al. 2020; Varjani 2017). There are a large number of oil-degrading microorganisms in the natural environment, including bacteria and fungi, as well as a small amount of algae (Prince 2005; Xue et al. 2015). However, although a large number of publications have reported the biodegradation of petroleum hydrocarbons (Fuentes et al. 2014; Ghosal et al. 2016; Kadri et al. 2017; Lawniczak et al. 2020; Prince et al. 2013; Varjani 2017), only a small number have considered the bioremediation of the shorelines.
The present paper review summarizes current knowledge on the ability of microorganisms to degrade petroleum hydrocarbons, taking into account the sources of oil pollutants, distribution of oil pollutants in the shoreline, impact of oil pollutants on the ecological environment of the shoreline, oil degrading microorganisms, microbial metabolism pathway, and key enzymes for biodegradation of petroleum hydrocarbons. Finally, this review discusses factors affecting biodegradation rate and types of microbial remediation technologies, current limitations, and future research directions.
Causes of oil spills
Both natural and anthropogenic factors can cause ocean oil spills. One of the most common natural causes is oil leakage from the ocean seabed or the discharge of oil yielding rocks from the seabed into the ocean ecosystem (Dhaka and Chattopadhyay 2021). Anthropogenic causes are usually accidental and intentional oil spills. Accidental spills may be due to the grounding and collision of ships carrying oil (Exxon Valdez spill, etc.), accidents at offshore oil rigs (Deepwater Horizon oil drilling platform explosion, etc.), and the storage of crude oil and its derivatives. Intentional oil spills are mainly caused by the discharge of untreated wastewater, the release of fuel from service centers, illegal discharge of sewage, and acts of war. Once an ocean oil spill occurs, large amounts of oil can rapidly spread and invade the whole shorelines under the action of tides and waves. This oil continuously penetrates into the deep layer via adsorption by shoreline sediments.
Distribution of shoreline oil pollutants
Oil types
Crude oil is an organic compound composed of saturated hydrocarbons, aromatic hydrocarbons, resins, and asphaltenes (Varjani 2017). Based on the relative contents of these four components, crude oil can be divided into light, medium, and heavy. According to analysis of the 10 largest oil leakage accidents in history, leaked crude oil mainly includes light crude oil and heavy crude oil (Lim et al. 2016). Generally, light crude oil is mainly composed of saturated hydrocarbons and aromatic hydrocarbons, with relatively less resins and asphaltenes, heavy crude oil has higher contents of resins and asphaltenes (Head et al. 2006).
The behavior and degradability of oil pollutants that ultimately reach the shoreline depend on the type and composition of the crude oil. Most of offshore oil platforms produce light crude oil, but the demand for heavy oil and its marine transportation is growing, increasing the risk of shoreline oil pollution with low degradation potential (Martínez-Palou et al. 2011). However, even leakage of light crude oil leads to the deposition of hydrocarbons with low degradability, because weathering occurs during transportation to the coast (Bacosa et al. 2015). In the first few days, light oil may lose nearly half of its mass due to the release of gases, dissolution of water-soluble hydrocarbons, and evaporation of volatile compounds (Liu et al. 2012). Biodegradation of dispersed crude oil in the ocean is relatively fast (with a half-life of several weeks); however, it is usually much slower along the shorelines (Abou Khalil et al. 2022). Therefore, dispersing oil at sea and preventing it from reaching the shorelines may be the most appropriate approach for managing oil spills. Using fine sediments to disperse crude oil may be a promising method (Ji et al. 2023).
Sediment properties
The properties of surface and subsurface shoreline sediments play a major role in the distribution of oil pollutants (Taylor and Reimer 2008). Compared with fine-grained sediments, coarse sediments typically facilitate deeper oil infiltration. Sediments with sharp edges and/or wide grain size distributions have lower porosity. Beaches can be found of clay (< 4 μm), silt (4 to 60 μm), and sand (60 μm to 2 mm), and/or different combinations of larger aggregates. Some beaches may consist of two or more types of sediments with different properties (Li et al. 2010).
Oil distribution in the shoreline
The shoreline consists of the supratidal zone, intertidal zone (upper, middle, and lower intertidal zone), and subtidal zone. Generally, the upper intertidal zone has the highest amount of oil deposition (based on oil quality per mass of sediment) owing to the significant decline in the groundwater level associated with this location (Boufadel et al. 2019). The mass of oil in the intertidal zone decreases toward the seaward direction (from upper to mid- to lower intertidal zones), because the groundwater level increases. Oil may also reach the supratidal zone (e.g., zone landward of the shoreline) under the action of storm waves (e.g., storm surges) (Abou Khalil et al. 2021a). Once deposited onto the supratidal zone, oil can penetrate sediments and/or be covered by the sediments of subsequent storm waves. However, the concentration of oil deposited into the supratidal zones tends to be lower than that deposited into the intertidal zones. Table 1 summarizes the impact of some marine oil spill accidents on the supratidal zone, the intertidal zone (upper, middle, and lower intertidal zone), and subtidal zone. Additionally, the spilled oil slicks are likely to break into droplets in the subtidal and intertidal zones of the shoreline owing to wave power. The dispersed oil droplets can interact with the sediments to form oil particle aggregates (OPAs) (Ji et al. 2023). Moreover, some sediments can penetrate oil droplets, causing OPAs to decompose into smaller aggregates, making them less likely to settle and greatly enhancing the microbial degradation of petroleum hydrocarbons. Therefore, these findings also highlight the possibility of mineral deposits being used for dispersion.
Impact of oil pollutants on the shoreline ecological environment
Shoreline oil pollutants can cause significant damage to habitats and pose a serious threat to all organisms living along and within the shoreline (Michel et al. 2017). The potential impact of oil pollution on biota varies by species (Bejarano and Michel 2016). Exposure to spilled oil can affect organisms from the outside through the skin or through direct inhalation and ingestion. The animals most affected by oil include seabirds, turtles, and marine mammal (such as sea otters and seals) (Yuewen and Adzigbli 2018).
Coral reefs, mangroves, and swamps are the most sensitive coastal habitats to oil pollutants. These ecosystems provide coastal protection and feeding/nursery resources for many invertebrate and fish. For example, when the intertidal zone experiences low tide, oil floating on the water surface can be directly deposited onto coral habitats (Guzman et al. 2020). Mangroves are trees and shrubs commonly found along the coasts and estuaries of tropical and subtropical regions (Duke 2016). They provide coastal protection for inland areas from strong storms and provide habitats for various mammals, birds, insects, plants, and algae attached to tree roots (Iturbe-Espinoza et al. 2022). When exposed to tidal currents, oil can adhere to the exposed surfaces and roots of mangroves. When suffocated by oil pollution, plants and animals cannot survive in the mangrove ecosystem. Swamps develop in the intertidal zone of muddy shorelines. They are exposed to high tide water and are susceptible to the influence of floating oil (Challenger et al. 2015). Finally, oil pollution disrupts the food web and leads to shoreline erosion, which will seriously affect swamp areas.
Oil degrading microorganisms
Oil-degrading microorganisms were first isolated almost a century ago. To date, 200 types of oil degrading microorganisms in the marine environment have been reported in the literature, including 90 types of bacteria,103 types of fungi, and 23 types of algae (Prince 2005). Table 2 lists the crude oil degradation characteristics of bacteria, most of which are Proteobacteria, Actinobacteria, and Firmicutes. A group of obligate hydrocarbon-degrading γ-Proteobacteria can only use hydrocarbons as their carbon sources for growth and metabolism. Among them, Alcanivorax sp., Oleiphilus sp., Oleispira sp., and Thalassolituus sp. obligately degrade saturated hydrocarbons, while Cycloclasticus sp. obligately degrade aromatic hydrocarbons. In addition, Planococcus sp. is an obligate degrading bacterium of saturated hydrocarbons (Head et al. 2006). For the remediation of oil-contaminated intertidal sediments, Acinetobacter sp., Pseudomonas sp., and Bacillus sp. play important roles in the bioremediation of oil pollutants owing their widespread presence in the environment and extensive ability to degrade hydrocarbons.
Microbial degradation mechanism of oil pollutants
Both aerobic degradation and anaerobic degradation are involved in the biodegradation process of oil pollutants. Between them, aerobic degradation is relatively more common and has rapid reaction speed and strong adaptability to the environment (McGenity 2014).
Aerobic degradation of oil pollutants
Aerobic degradation has a rapid pollutant conversion rate and relatively low requirements for environmental conditions. The process of molecular oxygen as the hydrogen acceptor plays a major role in the remediation of oil-contaminated shorelines.
Aerobic degradation of saturated hydrocarbons
Saturated hydrocarbons, which are mainly composed of n-alkanes, branched chain alkanes, and cycloalkanes, are the most easily degradable components in petroleum (Rojo 2009). The degradation of n-alkanes mainly includes pathways of terminal oxidation, sub-terminal oxidation, and double-terminal oxidation (Abbasian et al. 2015). For the terminal oxidation of n-alkanes, the methyl of n-alkanes is eventually oxidized to alcohols, aldehydes, and fatty acids with the aid of hydroxylase (oxygenase) and dehydrogenase; these fatty acids enter the tricarboxylic acid cycle through β-oxidation (Fig. 1). For double-terminal oxidation, one end of the fatty acid formed by terminal oxidation is oxidized to hydroxyl through ω-oxidation, and then further metabolized to dicarboxylic acid, before finally entering the tricarboxylic acid cycle through β-oxidation (Fig. 1). Sub-terminal oxidation is a series oxidation of n-alkanes to secondary alcohols, methyl ketones, acetyl esters and then acetyl esters, grade alcohol (acetate), and finally fatty acids catalyzed by hydroxylase (oxygenase) and dehydrogenase (Fig. 1). At the end, the fatty acids enter the tricarboxylic acid cycle through β-oxidation. The above hydroxylation processes are catalyzed by monooxygenase, while long-chain alkanes can be oxygenated by dioxygenase to form alkyl hydrogen peroxide, which can then be converted into fatty acids without passing through the Finnerty pathway of alcohol intermediates (Sakai et al. 1996).
The degradation pathway of branched alkanes is similar to that of normal alkanes. It starts at the end or sub-end of the long chain alkanes to form branched fatty acids and enters the TAC cycle through ω- or β-oxidation. However, the more branches and the longer chains, the greater the difficulty of degradation. Phytane and pristane with high branching degree and isoprenoid structure are the most difficult to oxidize and are often used as biomarkers (Abbasian et al. 2015).
Cycloalkanes, such as steranes and hopanes, with complex structures are usually the most persistent in the environment (Wang 2007). The degradation mechanism of the side chain of cycloalkanes is believed to be similar to that of the sub-terminal oxidation of n-alkanes. Cycloketones are first formed by the catalysis of oxygenase and dehydrogenase, and then by lactonization (Abbasian et al. 2015). One of the limiting factors for the degradation of cycloalkanes is that there are no individual microorganisms known to be able to oxidize these macromolecules to produce cyclic ketones for lactonization (Abbasian et al. 2015; Kostichka et al. 2001). Therefore, a synergistic effect of microbial communities is crucial for the successful degradation of cycloalkanes (Abbasian et al. 2015; Varjani 2017).
Aerobic degradation of aromatic hydrocarbons
Benzene, toluene, ethylbenzene, and xylene (BTEX) are the most widely studied monocyclic aromatic hydrocarbons (El-Naas et al. 2014). In the presence of dioxygenase, the benzene ring is hydroxylated to form cis-dihydrodiol, the cis-dihydrodiol ring is then broken to produce catechol, and catechol is further metabolized to form succinic acid and acetyl CoA (Fig. 2) and other intermediates of the TCA cycle (Juhasz and Naidu 2000). The metabolic intermediates generate formic acid, acetaldehyde, and pyruvic acid. Some studies have shown that higher pH favors the formation of succinic acid and acetyl CoA, while high C/N ratios tend to enhance benzene-ring opening pathways (El-Naas et al. 2014). Hydroxylation of the benzene ring catalyzed by dioxygenase is usually the rate limiting step of aromatic degradation, and oxygenase is the key enzyme to promote catalysis (Wang et al. 2018b).
The degradation of polycyclic aromatic hydrocarbons (PAHs) mainly depends on their structural properties and the adaptability of microbial degrading enzymes (Alegbeleye et al. 2017b). In terms of PAH degrading bacteria, Rhodococcus sp., Sphingomonas sp., Pseudomonas sp., and Mycobacterium sp. are the most widely studied (Brzeszcz and Kaszycki 2018; Nzila 2018). There are two main pathways for the microbial degradation of PAHs. Low molecular weight polycyclic aromatic hydrocarbons (LMWPAHs) with two or three benzene rings (Nzila 2018) by microorganisms as their carbon and energy sources to metabolize into CO2 and H2O for complete degradation (Mallick et al. 2011). High molecular weight polycyclic aromatic hydrocarbons (HMWPAHs) are generally highly resistant to biodegradation and can only be degraded by co-metabolism (Ghosal et al. 2016; Sivaram et al. 2019). However, the co-metabolites of HMWPAHs may be more biotoxic and have greater difficulty to achieving final mineralization (Maiti et al. 2012).
Degradation of LMWPAHs as single carbon and energy sources
Naphthalene and phenanthrene are the simplest PAHs, and their degradation mechanism has been thoroughly studied. Figure 3 shows a typical process of naphthalene degradation by bacteria (Habe and Omori 2003). Hydroxylation of the benzene ring is the initial step in the degradation of naphthalene, during which benzene combines with two oxygen atoms to form cis-naphthalene dihydrodiol by dioxygenase. Then cis-naphthalene dihydrodiol cleaves a benzene ring and converts it into salicylaldehyde and salicylic acid by a series of enzymes. Salicylic acid can be further converted into catechol or gentian acid by hydroxylase. Both intermediates can be metabolized into the TCA cycle, and finally be mineralized by the bacteria.
The “bay region” and “K region” are often considered the basic structural units of PAHs (Mallick et al. 2011). Phenanthrene is the smallest PAH with the above structure, and so it is often used as a model compound for study on the metabolism of PAHs. The most common degradation pathway of phenanthrene is shown in Fig. 3 (Mallick et al. 2011). Phenanthrene is hydroxylated at the 3,4 C position by dioxygenase, followed by a series of biochemical reactions, such as dehydrogenation, isomerization, and hydration, to cleave a benzene ring to produce 1-hydroxy-2-naphthoic acid. For some bacteria, such as Pseudomonas sp., 1-hydroxy-2-naphthalenecarboxylic acid may be converted into dihydroxynaphthalene, which is further degraded in a manner similar to naphthalene, using a salicylic acid pathway or naphthalene pathway. For microbes that cannot use naphthalene, 1-hydroxy-2-naphthoic acid is oxidized and cleaved by dioxygenase to form phthalic acid and protocatechuic acid, which then enter the TCA cycle. In addition, there are a few reports on the hydroxylation and ring cleavage of phenanthrene at the 1,2 C and 9,10 C sites, while some strains even have multiple degradation pathways (Mallick et al. 2011).
Co-metabolism of HMWPAHs
Co-metabolism is the phenomenon by which microorganisms have the sole carbon source as their co-substrate or primary substrate and also catabolize the secondary substrate; in contrast, these substrates cannot be used individually (Beam and Perry 1973). For example, Pseudomonas saccharophila p15 cannot use benzoanthracene and benzo[α]pyrene as carbon sources and energy sources for its growth, but when salicylic acid exists in the medium, it is able to oxidize and degrade both substrates (Chen and Aitken 1999). Similarly, when salicylic acid, phthalic acid, phenanthrene, or even light oil and glucose are used as co-substrates, Pseudomonas sp. and halophilic bacterial consortium have higher degradation rates of benzo[a]pyrene (Arulazhagan et al. 2014; Chen and Aitken 1999). Co-metabolism also exists in the degradation of refractory nitrogen-sulfur heterocycles and halogenated aromatic hydrocarbons in a soil/compost mixture (Meyer and Steinhart 2000).
Co-metabolic degradation has been widely reported, but its mechanism is yet to be fully explained (Zhang et al. 2019b). At present, the hypothesis of co-induction or “co-enzyme effect” by nonspecific degrading enzymes has been accepted (Luo et al. 2014). Khara et al. (2014) reported that dioxygenase gene from Sphingomonas was transferred into Escherichia coli to enable the constructs to degrade more types of PAHs. With the existence of some substrates, the constructs were induced to produce dioxygenases for the degradation of HMWPAHs. These growth substrates were mostly LMWPAHs with similar structure or their degradation products (such as salicylic acid, phthalic acid, etc.) (Horvath 1972). Some studies have shown that conventional carbon sources, such as glucose and starch, can be used as the primary substrates for co-metabolism of refractory organic compounds (Luo et al. 2008), and their catabolism provides the necessary co-factors for PAH degradation. Owing to the complexity of biochemical and molecular mechanisms of microbial co-metabolism, the mechanisms need to be further studied and verified.
Anaerobic degradation of oil pollutants
It was long believed that O2 was not only the final electron acceptor for microbial degradation of petroleum hydrocarbons but also an indispensable reactant. Lovley and Lonergan (1990) isolated the first Fe (III) reducing bacteria that could anaerobically degrade aromatic hydrocarbons as the sole carbon source. Since then, many anaerobic microbes for the degradation of petroleum hydrocarbon have been reported (Chakraborty and Coates 2004; Jaekel et al. 2015; Kniemeyer et al. 2007; Widdel and Rabus 2001b). These microbes use NO3−, SO42−, CO2, or Fe (III) as electron acceptors for anaerobic degradation. Their reaction rates are slow with strict environmental requirements; however, many refractory organic compounds and their toxic metabolites that are hardly treated under aerobic conditions can be completely degraded in anaerobic environments (Díaz 2004; Sherry et al. 2013).
For common NO3− and SO42− reductions, the main anaerobic metabolism of the oil pollutants involved is fumarate addition, hydroxylation, methylation, and carboxylation (Widdel and Rabus 2001a), as shown in Fig. 4. Fumarate reaction, the main path of anaerobic degradation of oil hydrocarbons, is a process in which hydrocarbon carbon atoms cleave the double bond of fumarate to produce alkyl or aromatic fatty acids, depending on the C–H bond activation energy of the substrate (Kniemeyer et al. 2007; Meckenstock and Mouttaki 2011). It is generally considered that the optimal value for the reaction is 355–430 kJ/mol (Widdel and Rabus 2001a). The secondary terminal carbon sites of alkanes and alkyl side chains are more active within the above energy range, while the C–H bond energy of the benzene ring is higher (> 460 kJ/mol); therefore, it is more appropriate for the other three reactions (hydroxylation, methylation, and carboxylation) (Meckenstock and Mouttaki 2011; Weelink et al. 2010). Many studies have shown that some bacteria can hydroxyl benzene (the hydroxyl from H2O or HO·) to phenol under the action of dioxygenase, and then undergo further carboxylation and β-oxidation to finally generate benzoyl-CoA (Weelink et al. 2010). In addition, under SO42− reducing conditions, naphthalene may be degraded with the methylation reaction, while other petroleum hydrocarbons can obtain a carbon atom from CO2\CO32− and generate alkyl or aryl carboxylates (Rabus et al. 2016).
Key enzymes involved in microbial degradation
Although the microbial degradation of oil pollutants in shorelines involves both aerobic and anaerobic degradations, aerobic degradation is preferable owing to its faster reaction rate and stronger environmental adaptability. In aerobic treatment, the initial reaction step for the degradation of petroleum hydrocarbons is to add one or two hydroxyl groups to the hydrocarbon skeleton (Figs. 1, 2, and 3). The reaction is usually completed by the biocatalysis of monooxygenase or dioxygenase. Enzymes used depend on the molecular size of the petroleum hydrocarbons.
Alkane-degrading enzymes
The initial hydroxylation of alkanes can be accomplished by varying categories of monooxygenases (Table 3). The alkane hydroxylase from short chain alkane–degrading microbes is similar to methane monooxygenase. There are two different forms of methane monooxygenases: all methanotrophs produce a membrane-bound particulate form of methane monooxygenase (pMMO) that oxidizes n-alkanes in the C1–C4 range, while some methanotrophs additionally produce a soluble form (sMMO) that is active against a wider range of substrates, oxidizing C1–C7 n-alkanes to the corresponding alcohols (Moreno and Rojo 2019). In general, Pseudomonas butanovora, Gordonia sp. TY -5, Mycobacterium sp. ty-6, and Pseudoocardia sp. ty-7 can all secrete monooxygenase to degrade short-chain alkanes (Moreno and Rojo 2019). Soluble cytochrome P450 and membrane oxygenase AlkB (integrated membrane non haem di-iron monooxygenase) are able to degrade C5–C17 (medium long chain) alkanes (Funhoff et al. 2006). P450s have been found in strains of Acinetobacter, Mycobacterium sp., Rhodococcus sp., and Dietzia sp., and in several Gram-negative bacteria including hydrocarbonoclastic bacteria such as Alcanivorax sp. (Nie et al. 2014; Scheps et al. 2011; Schneiker et al. 2006; Sekine et al. 2006; Wang et al. 2010). AlkB has been found in a variety of bacteria, such as Pseudomonas putida gpo1, Mycobacterium tuberculosis, Rhodococcus rubrum, Burkholderia cepacia, Pseudomonas aeruginosa, and Acinetobacter sp., among others (Singh et al. 2012). Long chain alkane–degrading enzymes include yellow binding monooxygenase (AlmA) and long-chain alkane monooxygenase (LadA) which are able to degrade alkanes with carbon chain length greater than C18. AlmA are able to oxidize C20 to > C32 n-alkanes (Throne-Holst et al. 2007). Genes homologous to almA have been identified in several other long-chain n-alkane–degrading strains, including Acinetobacter sp. M1 and several Alcanivorax species (Liu et al. 2011; Wang and Shao 2012).
LadA is expressed in Geobacillus thermodenitrificans NG80-2, which oxidizes C15–C36 n-alkanes, generating the corresponding primary alcohols (Feng et al. 2007). In general, an alkane-degrading bacterial strain can generate multiple alkane hydroxylases for the treatment of varying chain lengths of alkanes. Pseudomonas aeruginosa PAO1 can secrete two alkane hydroxylases, AlkB1 and AlkB2 (Rojo 2009). Alcanivorax borkumensis possesses two types of AlkB (AlkB1 and AlkB2), three cytochrome P450s (P450-1, P450-2, and P450-3), and one AlmA (Throne-Holst et al. 2007).
Polycyclic aromatic hydrocarbon degrading enzymes
The initial PAH is mainly completed by ring hydroxylating dioxygenase (RHD) (Zeng et al. 2017). RHD is a multi-component enzyme, usually composed of two or three components, including oxygenase and electron transport chain (Kweon et al. 2008). Oxygenase is composed of an α subunit (αn) or both α and β subunits (αnβn); αn is a catalytic component responsible for electron transfer, while the βn subunit maintains the structural stability of the α-subunit (Kweon et al. 2008). Compared with alkane-degrading bacteria, PAH-degrading microbes have lower substrate specificity. The genes encoding the PAH oxygenase αn subunit in Gram-positive bacteria are mainly distributed in three gene clusters: (1) nah-like, (2) phnAc-like, and (3) bphA1-like (Cebron et al. 2008). Most of these genes are located on the chromosome or plasmid DNA (Habe and Omori 2003) and are often detected in the bacteria Sphingomonas sp., Burkholderia sp., polaromonas sp., Ralstonia sp., Comamonas sp., Marinobacter sp., and Pseudomonas sp. (Cebron et al. 2008) Similarly, there are genes in Gram-negative bacteria that encode oxygenase like those described above. The gene-encoding PAH dioxygenases αn in Gram-negative bacteria are mainly distributed in the following four gene clusters: (1) narA-like gene of Rhodococcus sp.; (2) nidA/pdoA1-like gene of Mycobacterium sp., Nocardioides sp., and Mycobacterium sp.; (3) phdA/pdoA2-like gene; and (4) nidA3/fadA1 of Mycobacterium sp. and Terrabacter sp. (Cebron et al. 2008). In addition to cyclohydroxylation dioxygenase, catechol dioxygenase is another key enzyme in the degradation process of polycyclic aromatic hydrocarbons. It can catalyze the intermediate metabolite pyrocatechol to carry out the meta and ortho cleavage, and promote complete ring opening of aromatic ring to produce the intermediate products of tricarboxylic acid cycle (Habe and Omori 2003). At present, studies have shown that xylE gene can encode catechol-2,3-dioxygenase synthesis (Song et al. 2017).
Microbial remediation technologies for oil-contaminated shorelines
Although the above factors impact microbial remediation of oil pollutants in the shorelines, many environmental factors cannot be easily adjusted to enhance pollutant degradation. For example, it is impractical to change the salinity and climate of the shorelines. Therefore, the study of feasible bioremediation enhancement strategies has become a research hotspot, and some research progress has been made in the four main aspects, as described below.
Oil-degrading microorganism-assisted microbial remediation
Oil pollution inevitably enables natural evolution of the marine microbial community (Khan et al. 2018). The bacterial populations are better able to tolerate and degrade pollutants via gradual accumulation to realize the environmental resilience (Liu et al. 2017a). However, the start-up of this process may be long, and indigenous populations are often unable to degrade all the oil pollutants (Shigenaka 2014). Addition of highly efficient oil-degrading microorganisms may be able to effectively solve the problems of indigenous populations with insufficient cell density, inhibited activity, and limited degradation ability. The forms of microorganisms so far applied include (i) microorganisms indigenous to the polluted sites, (ii) exogenous microorganisms (either the pure culture of known microbial species/single strain or a collection of individual microorganisms to form a high-density cell mass (i.e., a microbial consortium), and (iii) genetically engineered microorganisms (recombinant microorganisms) (Nwankwegu et al. 2022). The type of microorganisms added often depends on the latest and historical knowledge of the contaminated site.
At present, a large number of efficient oil-degrading microorganisms have been applied, and many bioremediation agents have been commercialized. However, contrary to laboratory results, efficient degradation bacteria often fail in field tests or practical applications along the shorelines. For example, Venosa et al. (1992) tested 10 commercial bacterial agents during the Exxon Valdez oil spill, and only 2 showed a promotion effect on biodegradation when these products were disinfected, each group showed better degradation performance. This shows that indigenous microorganisms dominate the bioremediation process. In fact, exogenous strains can effectively exert their restoration process only when they have adapted to the physical and chemical conditions of the shoreline environment; only then can they compete with indigenous microorganisms for nutrients and avoid predation by protozoa (Mercer and Trevors 2011).
Immobilized microorganisms are used to resist the invasion of the unfavorable intertidal environment and competing indigenous microorganisms (Dai et al. 2022; Nhi-Cong et al. 2020; Partovinia and Rasekh 2018). The most common immobilization technique is formation of a biofilm or entrapment and encapsulation of microorganisms using polymeric gels (Partovinia and Rasekh 2018). The immobilization carrier provides a favorable micro-environment that helps microorganisms resist the invasion of the unfavorable intertidal environment and competing indigenous microorganisms (Hajieghrari and Hejazi 2020; Ruan et al. 2018). Furthermore, they enhance the activity, stability, and heavy oil biodegradation efficiency of inoculated microorganisms. The immobilization carrier can also loosen the shoreline sediments and increase oxygen flow (Tao et al. 2019), thereby accelerating microbial degradation of heavy oil. In our study (Dai et al. 2022), we used a modified zeolite immobilized bacterial consortium to remediate an intertidal zone polluted by heavy oil. After 100 days, the heavy oil degradation efficiency was 52.99%. Biochar, as an environmentally friendly material, offers great potential in the bioremediation of contaminated soils (Zahed et al. 2021) owing to its low cost, safety, and ability to maintain the activity of bacteria. Moreover, biochar also can improve the relative abundance and composition of indigenous oil-degrading microorganisms in sediments by serving as a high-quality carbon source, providing a microbial habitat, reducing nutrient loss, and adsorbing toxic hydrocarbons.
Nutrient-assisted microbial remediation
Nutrient addition is the most effective measure to maintain balanced microbial growth and is not toxic to the environment. Nutrients include carbon, nitrogen, phosphorus, and some other growth-limiting co-substrates (Gongora et al. 2022; Soleimani et al. 2013). Adding nutrient solution or solids is an effective way to improve the degradation efficiency of oil pollutants (Abou-Khalil et al. 2022). However, tides and waves along the shoreline environment are frequent, and nutrients are often washed out by seawater. Maintaining a high nutrient concentration in interstitial sediments is a problem that must be solved.
There are two main research directions with regard to this problem. The first is focused on beach hydraulics of nutrients and proposes an optimal nutrient addition strategy. The simplest dosing method is to spray the nutrient solution evenly on the beach surface at low tide. For example, a large number of spraying devices are arranged on the beach. However, this is costly and the high-salt seawater environment can easily cause devices to block. Other options are to dig ditches at the high tide water level and pipelines with holes to transport nutrient solution to the entire beach under groundwater activity during the tidal process (Venosa et al. 1996), or to slowly release lipophilic nutrients. The nutrients for slow release are usually in solid form, with hydrophobic materials such as kerosene, vegetable oil, or resin coated on the surface of inorganic nutrients to achieve controlled release of nutrients and overcome seawater scouring (Gallego et al. 2006). For instance, a slow-release nutrition capsule, Customblen, was used for the remediation of the Exxon Valdez oil spill. Vegetable oil was used as the coating material to contain calcium phosphate, amine phosphate, and ammonium nitrate (N: P: K = 28:8:0) (Swannell et al. 1996). The effect is most remarkable when it is combined with lipophilic nutrition agent Inipol EAP22, after which it can bind on the surface of oil pollutants and maintain an effective nutrient concentration of the oil–water interface for a prolonged time during biodegradation. Some studies have also suggested that this kind of lipophilic agent is more suitable for high-energy and coarse-grained sediment beaches compared with inorganic slow-release nutrients (Gallego et al. 2006). However, there still exist challenges for their application, including how to manipulate the release rate of slow-release nutrients and how to avoid competition by microorganisms to utilize lipophilic nutrients as carbon sources, which may inhibit degradation.
Biosurfactant-assisted microbial remediation
Biosurfactants have a good promoting effect on microbial degradation of oil pollutants. Biosurfactants help degradation by solubilizing or emulsifying oil pollutants (Liu et al. 2017b), increasing the interfacial uptake of oil pollutants by degrading bacteria (Zhong et al. 2014) or enhancing soil enzyme activity (Wang et al. 2018c). In addition, biosurfactants have the ability to weaken bacterial adsorption and enhance bacterial transport to or throughout the remediation sites (Zhong et al. 2017), which is of crucial importance for successful addition of efficient oil-degrading microorganisms for remediation.
Rhamnolipids are the most intensively studied biosurfactant. Owing to their advantageous physicochemical and biological properties, rhamnolipids are widely used in the field of oil pollution remediation (Karlapudi et al. 2018). The effects of rhamnolipids and Tween-80 on the degradation of phenanthrene by Sphingomonas gf2b have been studied (Pei et al. 2010). The phenanthrene biodegradation by Sphingomonas sp. GF2B was significantly inhibited (only 33.5% of phenanthrene degraded), while rhamnolipids significantly increased the degradation of phenanthrene (up to 99.5% of phenanthrene degraded). The authors proposed that rhamnolipids increase phenanthrene solubility, which is likely responsible for the high phenanthrene biodegradation efficiency in the presence of rhamnolipids. The effect of rhamnolipids on the biodegradation efficiency of diesel oil has also been (Kaczorek 2012). The results showed that presence of rhamnolipids significantly enhanced diesel oil degradation, giving rise to 88% loss after 14 days as compared with 44% loss with no surfactant presence. The authors found that rhamnolipids significantly increased the cell surface hydrophobicity of Pseudomonas stutzeri AG 22 as compared with two other surfactants. In another study, the field-scale bioremediation of PAH-contaminated farmland soil from the Shenyang North New Area of China was investigated using the bacteria Arthrobacter globiformis with addition of different concentrations of rhamnolipids (Wang et al. 2018c). The optimum rhamnolipid concentration of 5 mg/kg resulted in a PAH removal rate of 35.6% at 150 days. This was 29.3% higher than that of the control (no rhamnolipids and Arthrobacter globiformis), 19.8% higher than the rhamnolipid treatment alone (5 mg/kg), and 13.8% higher than the Arthrobacter globiformis treatment alone. The authors concluded that rhamnolipids enhanced soil catalase, invertase activities, and Arthrobacter globiformis reproduction during the PAH biodegradation processes. However, there still exist challenges for rhamnolipid application, such as how to avoid blocking effects and how to be degraded by microorganisms to provide a carbon sources.
Enzyme-assisted microbial remediation
Enzyme remediation has been considered an ideal remediation strategy for intertidal oil pollution since it requires neither nutrition from the environment nor the prevention of predators and toxic substances. Moreover, it overcomes the limitation of slow rate of degradation exhibited by microorganisms (Dai et al. 2020; Gaur et al. 2021). In addition, enzyme remediation also has the advantages of playing a role in different pollutant concentrations, low energy input, reducing sludge generation, and high specific rapid biodegradation (Mishra et al. 2020). Catalase, lipase, and oxidoreductase, which include monooxygenase, dioxygenase, alcohol dehydrogenase, and alkane hydroxylase, play important roles in the degradation of hydrocarbons (Suganthi et al. 2018). Lipase catalyzes the hydrolysis of crude oil components into simple compounds that can be used by microorganisms, while catalase decomposes hydrogen peroxide into oxygen and water, which reduces the oxidative stress caused by hydrocarbons (Achuba and Okoh 2014). Oxidoreductase can catalyze the oxidation and reduction of toxic hydrocarbons into simpler components (Suganthi et al. 2018).
The removal effects of catalase, lipase, and oxidoreductase on petroleum hydrocarbons in oil sludge have been studied. A bacterial consortium (composed of Shewanella chilikensis, Halomonas hamiltonii, and Bacillus firmus) was able to degrade 96% of total petroleum hydrocarbon by producing enzymes such as 46 U/mL catalase, 68 U/mL oxidoreductase, and 80 U/mL lipases (Suganthi et al. 2018). In our study, the immobilized laccase-bacteria consortium system was also used to remediate a shoreline polluted by heavy oil (Dai et al. 2020). The degradation efficiency of the immobilized laccase-bacteria consortium for heavy oil was 66.5% after 100 days of remediation, with a reaction rate constant of 0.018 day−1. Moreover, immobilized laccase was found to rapidly decompose polycyclic aromatic hydrocarbons with high petroleum toxicity (Kucharzyka et al. 2018) and promote the growth and reproduction of heavy oil–degrading bacteria. The use of enzymes to degrade oil pollutants can quickly reduce biological toxicity and initiate the biodegradation of oil pollutants.
Influencing factors of microbial remediation of oil-contaminated shorelines
Microbial degradation is the main method for removing oil pollutants from shorelines. Bioremediation of the shorelines is mainly affected by physical and chemical properties, biodegradability, bioavailability of oil pollutants, and microbial degradation capacity. In addition, environmental factors (sediment properties, temperature, nutrients, oxygen, electron acceptor, salinity) also impact microbial remediation in shorelines. Effective bioremediation strategies need to take into account all the above factors.
Properties of oil pollutants
The physical and chemical properties and bioavailability of oil pollutants play a vital role in the effectiveness of bioremediation (Ma et al. 2015). The biodegradability of oil components is ranked in the following order: straight chain alkanes > branched chain alkanes > low molecular weight alkyl aromatics > monocyclic aromatic hydrocarbons > cycloalkanes > PAHs > resins > asphaltenes (Varjani and Upasani 2017). Oil pollutants in high concentration often have strong biotoxicity, which can not only inhibit the growth and metabolism of microorganisms but also limits the mass transfer of nutrients and O2 (Al-Hawash et al. 2018). However, a low pollutant concentration can also affect bioremediation because the microbial population may struggle to survive without sufficient carbon sources (Varjani and Upasani 2017). Bioavailability is the amount of substances that microorganisms can obtain through physical and chemical mechanisms. Increasing bioavailability is an effective pathway to improve the efficiency of bioremediation (Varjani and Upasani 2016). A large number of studies have shown that the addition of surfactants can increase the bioavailability of oil pollutants and improve bioremediation efficiency (Karlapudi et al. 2018; Kleindienst et al. 2015; Xu et al. 2018). There is increasing interest in the application of microbial surfactants over chemical surfactants owing to (a) relative nontoxicity and high biodegradability (Varjani and Upasani 2016a), (b) unique structural properties for application in environmental clean-up (Zhao et al., 2016), and (c) high selectivity and specific activity at harsh environmental conditions (e.g., temperature, pH, and salinity) (Varjani and Upasani 2016b).
Microbial community
The composition of oil pollutants is extremely complex, and a single type of microorganism will often have limited ability to degrade specific components in crude oil (Acosta-Gonzalez and Marques 2016). For example, Alcanivorax sp. is a common obligate alkane-degrading bacteria, while Cycloclasticus sp. and Marinobacter sp. are often reported as PAH-degrading bacteria (Head et al. 2006). For a single oil pollutant, its biodegradation is usually carried out step by step with the participation of various enzymes or microorganisms (Figs. 1, 2, 3, and 4). Therefore, the degradation of crude oil requires the cooperation of a variety of petroleum-degrading microorganisms. The species, quantity, and community structure of microorganisms in the sedimentary environment have important impacts on the remediation effect.
Oil pollution is also a process of acclimation and selection of environmental microorganisms (Shaoping et al. 2021; Abou-Khalil et al. 2023). Microbial populations that can adapt to the polluted environment or have pollutant-degradation enzymes gradually enrich to perform selective succession with the changing composition of the oil pollutants, which will ultimately realize the gradual removal of various types of oil pollutants (Head et al. 2006; Vila et al. 2010). It is of great significance to elucidate the complex synergistic mechanism of oil-degrading bacteria, and dynamic relationships between changes of oil components and changes of microbial community structure and metabolic function in the process of degradation.
Environmental conditions in the shorelines
Temperature
The ambient temperature along the shorelines affects the viscosity, toxicity, solubility, and volatility of the spilled oil, and composition/bio-availability of the pollutants, and the growth and reproduction, metabolic activity, the oil pollution degradation rate of microorganisms (Megharaj et al., 2011). Increasing temperature increases the solubility of hydrophobic pollutants, decreases viscosity, and enhances diffusion and transfer of long chain n-alkanes from solid phase to water phase. At low temperatures, the viscosity of oil increases, volatilization of toxic short-chain alkanes is reduced, and their water solubility is decreased, which delays the onset of biodegradation (Aislabie et al. 2006). The optimal oil degradation temperature in an aerobic environment is 15–40 °C, and in the marine environment is ~ 20–30 °C (Al-Hawash et al. 2018). In open environments, the temperature fluctuation range, frequency, and duration vary with place and season, resulting in different restoration effects.
Nutrients
Availability of nutrients is important for successful oil biodegradation, including nitrogen, iron, and phosphorus in some cases. After an oil spill, the carbon source (petroleum hydrocarbons) in seawater and sediments increases greatly, and nutrients (e.g., N and P) become the limiting factor for biodegradation. Therefore, supply of nutrients for environmental microorganisms is an effective pathway to improve the efficiency of bioremediation, while the type, concentration, and ratio of nutrients should also be effectively controlled (Varjani et al. 2014). Excessive amounts of nitrogen in soil cause microbial inhibition. Maintaining nitrogen levels below 1800 mg nitrogen/kg H2O leads to optimal biodegradation of hydrocarbon pollutants (Walworth et al. 2007). Excessive nutrient concentrations, especially NPK, inhibit the biodegradation activity of hydrocarbon pollutants (Varjani 2017).
Oxygen
Alkanes and most aromatics generally require an oxygen supply for aerobic bioremediation. For example, in the bioremediation of the Exxon Valdez oil spill in the USA, many failed field study and practice cases could be attributed to the lack of oxygen in the sediment (Ramsay et al. 2000). On the surface of seawater, in the upper sediment layer, and in other areas exposed to waves and tidal currents, O2 is not a limiting factor. However, in fine sand beaches, muddy tidal flats, wetlands, swamps, and lower sediments conditions of most shorelines, the mass transfer of O2 is often insufficient for the consumption of microorganisms, which is thus considered the limiting step of bioremediation (Mercer and Trevors 2011). The O2 availability of sediments can be improved by applying oxygen generators (H2O2, CaO2) or mechanical means (e.g., compressed air supply) (Ramsay et al. 2000). Although some refractory oil pollutants can be completely degraded under anoxic and anaerobic conditions with NO3−, SO42−, CO2, or Fe (III) as electron acceptors (Meckenstock et al. 2016), the anaerobic degradation rate is much lower than that of the aerobic process. As such, it is only applicable in the low energy, fine, and its underlying sedimentary environment with insufficient O2 mass transfer.
pH
Seawater is usually slightly alkaline, but sediment pH can vary significantly. Organic matter increases acidity; the pH of swamp sediments can reach as low as 5.0, while mineral soil and sediment are neutral or slightly alkaline (Venosa and Zhu 2003). The acid-base environment of sediments has a significant influence on microbial activity and the availability of pollutants and nutrients (Obahiagbon et al. 2014). Most bacteria are suitable for degradation of oil pollutants in near neutral or slightly alkaline environments. This is also why bioremediation is difficult for oil pollution in marsh, mangrove, and other wetland systems (Mercer and Trevors 2011).
Salinity
High salinity is an important factor limiting the biodegradation of oil pollutants in the shoreline (especially in the supratidal zone and upper intertidal zone). Salinities can increase up to 160 g/L or even
higher in the supratidal zone and upper intertidal zone owing to the evaporation of seawater (Geng and Boufadel 2017). (Abou Khalil et al. 2021b) have shown that as salinity increases, the biodegradation of petroleum hydrocarbons by indigenous marine oil–degrading microorganisms decreases, with a decrease of two times at a salinity of 90 g/L and a decrease of four times at a salinity of 160 g/L. Furthermore, further research has shown that salinity has a significant impact on the biodegradation of aromatic hydrocarbons, while it has no significant impact on the biodegradation of alkanes (Abou Khalil et al. 2023). Various salt-tolerant and halophilic microorganisms with petroleum degradation ability have been screened to solve the above problems (Gibtan et al. 2017). In addition, salinity is also an important parameter affecting the cycle and migration of nitrogen and phosphorus in coastal sediments (Wang et al. 2018a).
Sediment properties
The migration and transformation of oil spill pollutants in sediments and pores, which are controlled by sediment, waves, and tidal conditions along the shoreline, determine the growth conditions of microorganisms (Wang et al. 2020b). Compared with fine beaches, oil pollutants are more likely to the penetrate deep sediments of coarse beaches and remain long term as they cannot be washed by waves (Boufadel et al. 2019); therefore, the larger the sediments grain sizes, the more sensitive they are to oil spill pollution (Southam et al. 2001). The O2 concentration of deep sediments is limited, and the biodegradation rate is relatively slow. In addition, waves, tidal currents, and oil exposure can significantly affect the removal of oil pollutants. For example, rocky coastlines exposed to waves and tidal currents are the least sensitive environments to oil spill pollution and human activities, and can be naturally restored after several months (Boufadel et al. 2019). Moreover, mechanical and chemical measures can accelerate the recovery speed. However, since both material flow and biological flow are controlled by physical scouring process, bioremediation is challenging. In contrast, loose and sheltered shoreline sediments (e.g., swamp, mangrove) with no waves or weak waves are very sensitive to oil spill pollution (Wang et al. 2020b). The pollutants usually stay for several years and mechanical and chemical treatments are likely to aggravate ecological damage. In these shoreline environments, bioremediation is often the most cost-effective method.
Limitations and future research directions
Although microbial remediation agents for shorelines have been repeatedly demonstrated in laboratory, they often fail in the field environment. In the shoreline environment, oil-degrading microorganisms (endogenous and exogenous) that were highly efficient in the laboratory may not be able to adapt to physical and chemical conditions to compete with the indigenous ecology. Moreover, they often need to go through a long start-up period. Under the unique hydrodynamic conditions of the shorelines, powder or solid based agents are easily diluted by seawater erosion, resulting in high failure rates. In addition, microorganisms preferentially degrade certain oil components, resulting in the accumulation of long-chain alkanes, polycyclic aromatic hydrocarbons, and other refractory components in the environment. This eventually increases the toxicity of the microenvironment, inhibiting the microbial growth and metabolic activity, leading to excessively long microbial remediation time. In addition, microbial remediation may also fail owing to uncontrolled environmental parameters (e.g., temperature, pH, and salinity) which are essential for optimum activity of microorganisms. Further research is needed to enhance the environmental adaptability of microbial remediation technologies.
Another perspective to consider in the future is sustainable microbial remediation technology of oil contaminated sediments. This will require effective multidisciplinary collaboration between researchers working in microbiology, environmental geochemistry, materials science, and engineering. New and sustainable microbial remediation technologies and low-carbon remediation materials should be further developed to meet the growing demand for sediment remediation. In addition, advanced characterization methods should be used to deepen understanding of the microbial degradation mechanism and promote the development of new microbial remediation technologies. The combined application of life cycle assessment, environmental impact assessment, cost-benefit analysis, and other methods to evaluate the feasibility of sustainable microbial remediation technology should also be carried out.
Conclusions
Oil pollutants have serious adverse impacts on the ecology of shoreline environments. Oil-degrading microorganisms can be used to degrade oil pollutants. Catabolic pathways involved in biodegradation reveal efficient strategies for oil pollution microbial remediation. Understanding key enzymes of oil microbial degradation is of great research interest to accelerate biodegradation. Optimizing the influencing factors will improve the efficiency of microbial remediation. Sustainable microbial remediation technology is the key to microbial remediation of shoreline oil pollutants. Addressing the limitations of microbial remediation technologies for shoreline oil pollution should be the focus of future research.
Data availability
Not applicable.
References
Agarwal A, Liu Y (2015) Remediation technologies for oil-contaminated sediments. Mar. Pollut. Bull 101(2):483–490
Abou Khalil C, Fortin N, Prince RC, Greer CW, Lee K, Boufadel MC (2021a) Crude oil biodegradation in upper and supratidal seashores. J Hazard Mater 416:125919. https://doi.org/10.1016/j.jhazmat.2021.125919
Abou Khalil C, Prince RC, Greer CW, Lee K, Boufadel MC (2022) Bioremediation of petroleum hydrocarbons in the upper parts of sandy beaches. Environ Sci Technol 56(12):8124–8131. https://doi.org/10.1021/acs.est.2c01338
Abou Khalil C, Fortin N, Wasserscheid J, Prince RC, Greer CW, Lee K, Boufadel MC (2023) Microbial responses to increased salinity in oiled upper tidal shorelines. Int Biodeter Biodegr 181:105603. https://doi.org/10.1016/j.ibiod.2023.105603
Abbasian F, Lockington R, Mallavarapu M, Naidu R (2015) A comprehensive review of aliphatic hydrocarbon biodegradation by bacteria. Appl Biochem Biotechnol 176(3):670–699. https://doi.org/10.1007/s12010-015-1603-5
Abou Khalil C, Prince VL, Prince RC, Greer CW, Lee K, Zhang B, Boufadel MC (2021b) Occurrence and biodegradation of hydrocarbons at high salinities. Sci Total Environ 762:143165. https://doi.org/10.1016/j.scitotenv.2020.143165
Achuba FI, Okoh PN (2014) Effect of petroleum products on soil catalase and dehydrogenase activities. Open J Soil Sci 04(12):399–406. https://doi.org/10.4236/ojss.2014.412040
Acosta-Gonzalez A, Marques S (2016) Bacterial diversity in oil-polluted marine coastal sediments. Curr Opin Biotechnol 38:24–32. https://doi.org/10.1016/j.copbio.2015.12.010
Aislabie J, Saul DJ, Foght JM (2006) Bioremediation of hydrocarbon-contaminated polar soils. Extremophiles 10(3):171–179. https://doi.org/10.1007/s00792-005-0498-4
Al-Awadhi H, Sulaiman RH, Mahmoud HM, Radwan SS (2007) Alkaliphilic and halophilic hydrocarbon-utilizing bacteria from Kuwaiti coasts of the Arabian Gulf. Appl Microbiol Biotechnol 77(1):183–186. https://doi.org/10.1007/s00253-007-1127-1
Al-Hawash AB, Dragh MA, Li S, Alhujaily A, Abbood HA, Zhang XY, Ma FY (2018) Principles of microbial degradation of petroleum hydrocarbons in the environment. Egypt J Aquat Res 44(2):71–76. https://doi.org/10.1016/j.ejar.2018.06.001
Alegbeleye OO, Opeolu BO, Jackson V (2017a) Bioremediation of polycyclic aromatic hydrocarbon (PAH) compounds: (acenaphthene and fluorene) in water using indigenous bacterial species isolated from the Diep and Plankenburg rivers, Western Cape, South Africa. Braz J Microbiol 48(2):314–325. https://doi.org/10.1016/j.bjm.2016.07.027
Alegbeleye OO, Opeolu BO, Jackson VA (2017b) Polycyclic aromatic hydrocarbons: a critical review of environmental occurrence and bioremediation. Environ Manage 60(4):758–783. https://doi.org/10.1007/s00267-017-0896-2
Arulazhagan P, Al-Shekri K, Huda Q, Godon JJ, Basahi JM, Jeyakumar D (2017) Biodegradation of polycyclic aromatic hydrocarbons by an acidophilic Stenotrophomonas maltophilia strain AJH1 isolated from a mineral mining site in Saudi Arabia. Extremophiles 21(1):163–174. https://doi.org/10.1007/s00792-016-0892-0
Arulazhagan P, Sivaraman C, Kumar SA, Aslam M, Banu JR (2014) Co-metabolic degradation of benzo (e) pyrene by halophilic bacterial consortium at different saline conditions. J Environ Biol 35(3):445
Austin B, Calomiris JJ, Walker JD, Colwell RR (1977) Numerical taxonomy and ecology of petroleum-degrading bacteria. Appl Environ Microbiol 34(1):60–68. https://doi.org/10.1128/aem.34.1.60-68.1977
Ayotamuno MJ, Kogbara RB, Ogaji SOT, Probert SD (2006) Bioremediation of a crude-oil polluted agricultural-soil at Port Harcourt, Nigeria. Appl Energy 83(11):1249–1257. https://doi.org/10.1016/j.apenergy.2006.01.003
Azizan NH, Abdul Rahim MS, Abidin ZAZ, Sharif MF, Chowdhury AJK (2020) Screening of biodegradation potential for n-alkanes and polycyclic aromatic hydrocarbon among isolates from the north-western tip of Pahang. Desalin Water Treat 191:207–212. https://doi.org/10.5004/dwt.2020.25304
Bacosa HP, Thyng KM, Plunkett S, Erdner DL, Liu Z (2016) The tarballs on Texas beaches following the 2014 Texas City “Y” Spill: modeling, chemical, and microbiological studies. Mar Pollut Bull 109(1):236–244. https://doi.org/10.1016/j.marpolbul.2016.05.076
Bacosa HP, Erdner DL, Liu Z (2015) Differentiating the roles of photooxidation and biodegradation in the weathering of Light Louisiana Sweet crude oil in surface water from the Deepwater Horizon site. Mar. Pollut. Bull 95(1):265–272
Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR (2011) The value of estuarine and coastal ecosystem services. Ecol Monogr 81:169–193. https://doi.org/10.1890/10-1510.1
Beam H, Perry J (1973) Co-metabolism as a factor in microbial degradation of cycloparaffinic hydrocarbons. Arch Microbiol 91(1):87–90. https://doi.org/10.1007/BF00409542
Bejarano AC, Michel J (2016) Oil spills and their impacts on sand beach invertebrate communities: a literature review. Environ Pollut 218:709–722. https://doi.org/10.1016/j.envpol.2016.07.065
Ben SO, Goni-Urriza MS, El Bour M, Dellali M, Aissa P, Duran R (2008) Characterization of aerobic polycyclic aromatic hydrocarbon-degrading bacteria from Bizerte lagoon sediments, Tunisia. J Appl Microbiol 104(4):987–997. https://doi.org/10.1111/j.1365-2672.2007.03621.x
Binazadeh M, Karimi IA, Li Z (2009) Fast biodegradation of long chain n-alkanes and crude oil at high concentrations with Rhodococcus sp. Moj-3449. Enzyme Microb Technol 45(3):195–202. https://doi.org/10.1016/j.enzmictec.2009.06.001
Boufadel M, Geng XL, An CJ, Owens E, Chen Z, Lee K, Taylor E, Prince RC (2019) A review on the factors affecting the deposition, retention, and biodegradation of oil stranded on beaches and guidelines for designing laboratory experiments. Curr Pollut Rep 5(4):407–423. https://doi.org/10.1007/s40726-019-00129-0
Brown LM, Gunasekera TS, Ruiz ON (2017) Draft genome sequence of Nocardioides Iuteus strain BAFB, an alkane-degrading bacterium isolated from JP-7-polluted soil. Genome Announc 5(4):1–2. https://doi.org/10.1128/genomeA.01529-16
Brown LM, Gunasekera TS, Striebich RC, Ruiz ON (2016) Draft genome sequence of Gordonia sihwensis strain 9, a branched alkane-degrading bacterium. Genome Announc 4(3). https://doi.org/10.1128/genomeA.00622-16
Brzeszcz J, Kaszycki P (2018) Aerobic bacteria degrading both n-alkanes and aromatic hydrocarbons: an undervalued strategy for metabolic diversity and flexibility. Biodegradation 29(4):359–407. https://doi.org/10.1007/s10532-018-9837-x
Bragg JR, Prince RC, Harner EJ, Atlas RM (1994) Effectiveness of bioremediation for the Exxon Valdez oil spill. Nature 368:413–418. https://doi.org/10.1038/368413a0
Conan G (1982) The long-term effects of the Amoco Cadiz oil spill. Phil. Trans. R. Soc. Lond. B 297(1087):323–333. https://doi.org/10.1098/rstb.1982.0045
Curl, H., Barton, K., Harris, L. (1992). Oil spill case histories, 1967-1991: Summaries of significant US and international spills. Final report (No. PB-93-144517/XAB; HMRAD-92-11). National Ocean Service, Seattle, WA (United States). Hazardous Materials Response and Assessment Div.
Callaghan AV (2013) Enzymes involved in the anaerobic oxidation of n-alkanes: from methane to long-chain paraffins. Front Microbiol 4(89):1–9. https://doi.org/10.3389/fmicb.2013.00089
Cebron A, Norini MP, Beguiristain T, Leyval C (2008) Real-time PCR quantification of PAH-ring hydroxylating dioxygenase (PAH-RHDalpha) genes from Gram positive and Gram negative bacteria in soil and sediment samples. J Microbiol Methods 73(2):148–159. https://doi.org/10.1016/j.mimet.2008.01.009
Chaıneaua CH, Morelb UJ, Duponta J, Bury E, Oudot J (1999) Comparison of the fuel oil biodegradation potential of hydrocarbon-assimilating microorganisms isolated from a temperate agricultural soil. Sci Total Environ 227:237–247. https://doi.org/10.1016/S0048-9697(99)00033-9
Chakraborty R, Coates JD (2004) Anaerobic degradation of monoaromatic hydrocarbons. Appl Microbiol Biotechnol 64(4):437–446. https://doi.org/10.1007/s00253-003-1526-x
Chakraborty R, O'Connor SM, Chan E, Coates JD (2005) Anaerobic degradation of benzene, toluene, ethylbenzene, and xylene compounds by Dechloromonas strain RCB. Appl Environ Microbiol 71(12):8649–8655. https://doi.org/10.1128/AEM.71.12.8649-8655.2005
Chaudhary P, Sharma R, Singh SB, Nain L (2011) Bioremediation of PAH by Streptomyces sp. Bull Environ Contam Toxicol 86(3):268–271. https://doi.org/10.1007/s00128-011-0211-5
Chen SH, Aitken MD (1999) Salicylate Stimulates the degradation of high-molecular weight polycyclic aromatic hydrocarbons by Pseudomonas saccharophila P15. Environ Sci Technol 33(3):435–439. https://doi.org/10.1021/es9805730
Chung WK, King GM (2001) Isolation, characterization, and polyaromatic hydrocarbon degradation potential of aerobic bacteria from marine macrofaunal burrow sediments and description of Lutibacterium anuloederans gen. nov., sp. nov., and Cycloclasticus spirillensus sp. nov. Appl Environ Microbiol 67(12):5585–5592. https://doi.org/10.1128/AEM.67.12.5585-5592.2001
Challenger GE, Gmur S, Taylor E (2015) A review of Gulf of Mexico coastal marsh erosion studies following the 2010 Deepwater Horizon oil spill and comparison to over 4 years of shoreline loss data from Fall 2010 to Summer 2015. Mar Pollut Bull 164:111983. https://doi.org/10.1016/j.marpolbul.2021.111983
Cong Dang PD, Ayako S, Hisanori T, Hoang Nguyen DP, Xo Hoa D, Yoshie T (2016) Identification and biodegradation characteristics of oil-degrading bacteria from subtropical Iriomote Island, Japan, and tropical Con Dao Island, Vietnam. Tropics 25(4):147–159. https://doi.org/10.3759/tropics.MS16-01
Cravo-Laureau C, Matheron R, Joulian C, Cayol JL, Hirschler-Rea A (2004) Desulfatibacillum alkenivorans sp. nov., a novel n-alkene-degrading, sulfate-reducing bacterium, and emended description of the genus Desulfatibacillum. Int J Syst Evol Microbiol 54(Pt 5):1639–1642. https://doi.org/10.1099/ijs.0.63104-0
Daane LL, Harjono I, Barns SM, Launen LA, Palleron NJ, Haggblom MM (2002) PAH-degradation by Paenibacillus spp. and description of Paenibacillus naphthalenovorans sp. nov., a naphthalene-degrading bacterium from the rhizosphere of salt marsh plants. Int J Syst Evol Microbiol 52(Pt 1):131–139. https://doi.org/10.1099/00207713-52-1-131
Dhaka A, Chattopadhyay P (2021) A review on physical remediation techniques for treatment of marine oil spills. J Environ Manage 288:112428. https://doi.org/10.1016/j.jenvman.2021.112428
Daccò C, Girometta C, Asemoloye MD, Carpani G, Picco AM, Tosi S (2020) Key fungal degradation patterns, enzymes and their applications for the removal of aliphatic hydrocarbons in polluted soils: A review. Int. Biodeter. Biodegr 147:104866. https://doi.org/10.1016/j.ibiod.2019.104866
Dai X, Lv J, Yan G, Chen C, Guo S, Fu P (2020) Bioremediation of intertidal zones polluted by heavy oil spilling using immobilized laccase-bacteria consortium. Bioresour. Technol 309:123305. https://doi.org/10.1016/j.biortech.2020.123305
Dai X, Lv J, Wei W, Guo S (2022) Bioremediation of heavy oil contaminated intertidal zones by immobilized bacterial consortium. Process Safety and Environmental Protection 158:70–78
Dai X, Yan G, Guo S (2017) Characterization of Dietzia cercidiphylli C-1 isolated from extra-heavy oil contaminated soil. Rsc Advances 7(32):19486–19491
Duke NC (2016) Oil spill impacts on mangroves: recommendations for operational planning and action based on a global review. Mar Pollut Bull 109:700–715. https://doi.org/10.1016/j.marpolbul.2016.06.082
Deng MC, Li J, Liang FR, Yi M, Xu XM, Yuan JP, Peng J, Wu CF, Wang JH (2014) Isolation and characterization of a novel hydrocarbon-degrading bacterium Achromobacter sp. HZ01 from the crude oil-contaminated seawater at the Daya Bay, southern China. Mar Pollut Bull 83(1):79–86. https://doi.org/10.1016/j.marpolbul.2014.04.018
Díaz, E. (2004). Bacterial degradation of aromatic pollutants: a paradigm of metabolic versatility.
Dore SY, Clancy QE, Rylee SM, Kulpa CFJ (2003) Naphthalene-utilizing and mercury-resistant bacteria isolated from an acidic environment. Appl Microbiol Biotechnol 63(2):194–199. https://doi.org/10.1007/s00253-003-1378-4
Dubbels BL, Sayavedra-Soto LA, Bottomley PJ, Arp DJ (2009) Thauera butanivorans sp. nov., a C2-C9 alkane-oxidizing bacterium previously referred to as ‘Pseudomonas butanovora’. Int J Syst Evol Microbiol 59(Pt 7):1576–1578. https://doi.org/10.1099/ijs.0.000638-0
Dyksterhouse SE, Gray JP, Herwig RP, Lara JC, Staley JT (1995) Cycloclasticus pugetii gen. nov., sp. nov., an aromatic hydrocarbon-degrading bacterium from marine sediments. Int J Syst Bacteriol 45(1):116–123. https://doi.org/10.1099/00207713-45-1-116
Dave DAEG, Ghaly AE (2011) Remediation technologies for marine oil spills: A critical review and comparative analysis. Am. J. Environ. Sci 7(5):423
El-Gend NS (2006) Biodegradation potentials of dibenzothiophene by new bacteria isolated from hydrocarbon polluted soil in Egypt. Biosci Biotechnol Res Asia 3:95–106
El-Naas MH, Acio JA, El Telib AE (2014) Aerobic biodegradation of BTEX: progresses and prospects. J Environ Chem Eng 2(2):1104–1122. https://doi.org/10.1016/j.jece.2014.04.009
Engelhardt MA, Daly K, Swannell RPJ, Head IM (2001) Isolation and characterization of a novel hydrocarbon-degrading, Gram-positive bacterium, isolated from intertidal beach sediment, and description of Planococcus alkanoclasticus sp. nov. J Appl Microbiol 90:237–247. https://doi.org/10.1046/j.1365-2672.2001.01241.x
Feitkenhauer H, Müller R, Märkl H (2003) Degradation of polycyclic aromatic hydrocarbons and long chain alkanes at 6070 C by Thermus and Bacillus spp. Biodegradation 14:367–372. https://doi.org/10.1023/A:1027357615649
Feng L, Wang W, Cheng J, Ren Y, Zhao G, Gao C, Tang Y, Liu X, Han W, Peng X, Liu R, Wang L (2007) Genome and proteome of long-chain alkane degrading Geobacillus thermodenitrificans NG80-2 isolated from a deep-subsurface oil reservoir. Proc Natl Acad Sci USA 104(13):5602–5607. https://doi.org/10.1073/pnas.0609650104
Fuentes S, Mendez V, Aguila P, Seeger M (2014) Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 98(11):4781–4794. https://doi.org/10.1007/s00253-014-5684-9
Funhoff EG, Bauer U, Garcia-Rubio I, Witholt B, van Beilen JB (2006) CYP153A6, a soluble P450 oxygenase catalyzing terminal-alkane hydroxylation. J Bacteriol 188(14):5220–5227. https://doi.org/10.1128/JB.00286-06
Gallego JR, Menndez-Vega D, Gonzlez-Rojas E, Snchez J, Garcia-Martnez MJ, Llamas JF (2006) Oleophilic fertilizers and bioremediation: a new perspective. In: Modern multidisciplinary applied microbiology. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany, pp 551–555. https://doi.org/10.1002/9783527611904.ch97
Gallo G, Piccolo LL, Renzone G, Rosa RL, Scaloni A, Quatrini P, Puglia AM (2012) Differential proteomic analysis of an engineered Streptomyces coelicolor strain reveals metabolic pathways supporting growth on n-hexadecane. Appl Microbiol Biotechnol 94:1289–1301. https://doi.org/10.1007/s00253-012-4046-8
Gao Y, Yu XZ, Wu SC, Cheung KC, Tam NF, Qian PY, Wong MH (2006) Interactions of rice (Oryza sativa L.) and PAH-degrading bacteria (Acinetobacter sp.) on enhanced dissipation of spiked phenanthrene and pyrene in waterlogged soil. Sci Total Environ 372(1):1–11. https://doi.org/10.1016/j.scitotenv.2006.09.029
Garcia-Olivares A, Aguero A, Haupt BJ, Marcos MJ, Villar MV, de Pablos JL (2017) A system of containment to prevent oil spills from sunken tankers. Sci Total Environ 593–594:242–252. https://doi.org/10.1016/j.scitotenv.2017.03.152
Guzman HM, Kaiser S, Weil E (2020) Assessing the long-term effects of a catastrophic oil spill on subtidal coral reef communities off the Caribbean coast of Panama (1985–2017). Mar. Biodivers 50:28
Geng XL, Boufadel MC, Jackson L (2016) Evidence of salt accumulation in beach intertidal zone due to evaporation. Sci Rep 6:31486. https://doi.org/10.1038/srep31486
Geng XL, Khalil CA, Prince RC, Lee K, An CJ, Boufadel MC (2021) Hypersaline pore water in Gulf of Mexico beaches prevented efficient biodegradation of Deepwater Horizon beached oil. Environ Sci Technol 55(20):13792–13801. https://doi.org/10.1021/acs.est.1c02760
Gaur VK, Gupta S, Pandey A (2021) Evolution in mitigation approaches for petroleum oil-polluted environment: recent advances and future directions. Environ Sci Pollut Res Int 29:61821–61837
Ghosal D, Dutta A, Chakraborty J, Basu S, Dutta TK (2013) Characterization of the metabolic pathway involved in assimilation of acenaphthene in Acinetobacter sp. strain AGAT-W. Res Microbiol 164(2):155–163. https://doi.org/10.1007/s11356-021-16047-y
Ghosal D, Ghosh S, Dutta TK, Ahn Y (2016) Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review. Front Microbiol 7:1369. https://doi.org/10.3389/fmicb.2016.01369
Ghosh S, Chakraborty S (2020) Production of polyhydroxyalkanoates (PHA) from aerobic granules of refinery sludge and Micrococcus aloeverae strain SG002 cultivated in oily wastewater. Int Biodeterior Biodegr 155:105091. https://doi.org/10.1016/j.ibiod.2020.105091
Gibtan A, Park K, Woo M, Shin JK, Lee DW, Sohn JH, Song M, Roh SW, Lee SJ, Lee HS (2017) Diversity of extremely halophilic archaeal and bacterial communities from commercial salts. Front Microbiol 8:799. https://doi.org/10.3389/fmicb.2017.00799
Golyshin PN (2002) Oleiphilaceae fam. nov., to include Oleiphilus messinensis gen. nov., sp. nov., a novel marine bacterium that obligately utilizes hydrocarbons. Int J Syst Evol Micr 52(3):901–911. https://doi.org/10.1099/00207713-52-3-901
Gongora E, Chen YJ, Ellis M, Okshevsky M, Whyte L (2022) Hydrocarbon bioremediation on Arctic shorelines: historic perspective and roadway to the future. Environ. Pollut 305:119247. https://doi.org/10.1016/j.envpol.2022.119247
Guo CL, Dang Z, Wong Y, Tam NF (2010) Biodegradation ability and dioxgenase genes of PAH-degrading Sphingomonas and Mycobacterium strains isolated from mangrove sediments. Int Biodeter Biodegr 64(6):419–426. https://doi.org/10.1016/j.ibiod.2010.04.008
Gurav R, Lyu HH, Ma JL, Tang JC, Liu QL, Zhang HR (2017) Degradation of n-alkanes and PAHs from the heavy crude oil using salt-tolerant bacterial consortia and analysis of their catabolic genes. Environ Sci Pollut Res 24(12):11392–11403. https://doi.org/10.1007/s11356-017-8446-2
Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotech Bioch 67(2):225–243. https://doi.org/10.1271/bbb.67.225
Hoff RZ (1993) Bioremediation: an overview of its development and use for oil spill cleanup. Mar Pollut Bull 26(9):476–481. https://doi.org/10.1016/0025-326X(93)90463-T
Hoff RZ (1992) A summary of bioremediation applications observed at marine oil spill. Report HMRB 91-2. Hazardous Materials Response and Assessment Division Seattle, National Oceanic and Atmospheric Administration, Washington.
Hajieghrari M, Hejazi P (2020) Enhanced biodegradation of n-Hexadecane in solid-phase of soil by employing immobilized Pseudomonas Aeruginosa on size-optimized coconut fibers. J Hazard Mater 389:122134. https://doi.org/10.1016/j.jhazmat.2020.122134
Hamann C, Hegemann J, Hildebrandt A (1999) Detection of polycyclic aromatic hydrocarbon degradation genes in different soil bacteria by polymerase chain reaction and DNA hybridization. FEMS Microbiol Lett 173:255–263. https://doi.org/10.1111/j.1574-6968.1999.tb13510.x
Hassanshahian M, Ahmadinejad M, Tebyanian H, Kariminik A (2013) Isolation and characterization of alkane degrading bacteria from petroleum reservoir waste water in Iran (Kerman and Tehran provenances). Mar Pollut Bull 73(1):300–305. https://doi.org/10.1016/j.marpolbul.2013.05.002
Head IM, Jones DM, Roling WF (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4(3):173–182. https://doi.org/10.1038/nrmicro1348
Hedlund BP, Geiselbrecht AD, Bair TJ, Staley JT (1999) Polycyclic aromatic hydrocarbon degradation by a new marine bacterium, Neptunomonas naphthovorans gen. nov., sp. nov. Appl Environ Microbiol 65:251–259. https://doi.org/10.1128/AEM.65.1.251-259.1999
Hirano S, Kitauchi F, Haruki M, Imanaka T, Morikawa M, Kanaya S (2004) Isolation and characterization of Xanthobacter polyaromaticivorans sp. nov. 127W that degrades polycyclic and heterocyclic aromatic compounds under extremely low oxygen conditions. Biosci Biotechnol Biochem 68(3):557–564. https://doi.org/10.1271/bbb.68.557
Horvath RS (1972) Microbial co-metabolism and the degradation of organic compounds in nature. Bacteriol Rev 36(2):146. https://doi.org/10.1128/br.36.2.146-155.1972
Hua X, Wu Z, Zhang H, Lu D, Wang M, Liu Y, Liu Z (2010) Degradation of hexadecane by Enterobacter cloacae strain TU that secretes an exopolysaccharide as a bioemulsifier. Chemosphere 80(8):951–956. https://doi.org/10.1016/j.chemosphere.2010.05.002
Ilori MO, Amobi CJ, Odocha AC (2005) Factors affecting biosurfactant production by oil degrading Aeromonas spp. isolated from a tropical environment. Chemosphere 61(7):985–992. https://doi.org/10.1016/j.chemosphere.2005.03.066
ITOPF (2016) The international tanker owners pollution federation limited oil tanker spill statistics 2015. Retrieved March 16:2016 https://www.itopf.org/knowledge-resources/documents-guides/
Iturbe-Espinoza P, Bonte M, Gundlach E, Brandt BW, Braster M, van Spanning RJM (2022) Adaptive changes of sediment microbial communities associated with cleanup of oil spills in Nigerian mangrove forests. Mar Pollut Bull 2022(176):113406. https://doi.org/10.1016/j.marpolbul.2022.113406
Ji W, Abou-Khalil C, Jayalakshmamma MP, Boufadel MC, Lee K (2023) Post-formation of oil particle aggregates: breakup and biodegradation. Environ Sci Technol 57(6):2341–2350. https://doi.org/10.1021/acs.est.2c05866
Jaekel U, Zedelius J, Wilkes H, Musat F (2015) Anaerobic degradation of cyclohexane by sulfate-reducing bacteria from hydrocarbon-contaminated marine sediments. Front Microbiol 6:116
Jeon CO, Park W, Ghiorse WC, Madsen EL (2004) Polaromonas naphthalenivorans sp. nov., a naphthalene-degrading bacterium from naphthalene-contaminated sediment. Int J Syst Evol Microbiol 54(Pt 1):93–97. https://doi.org/10.3389/fmicb.2015.00116
Jin HM, Kim JM, Lee HJ, Madsen EL, Jeon CO (2012) Alteromonas as a key agent of polycyclic aromatic hydrocarbon biodegradation in crude oil-contaminated coastal sediment. Environ Sci Technol 46(14):7731–7740. https://doi.org/10.1021/es3018545
Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a ]pyrene. Int Biodeterior Biodegr 45:57–88. https://doi.org/10.1016/S0964-8305(00)00052-4
Kaczorek E (2012) Effect of external addition of rhamnolipids biosurfactant on the modification of gram positive and gram negative bacteria cell surfaces during biodegradation of hydrocarbon fuel contamination. Pol J of Environ Stud 21(4):901–909
Kadri T, Rouissi T, Kaur Brar S, Cledon M, Sarma S, Verma M (2017) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by fungal enzymes: a review. J Environ Sci (China) 51:52–74. https://doi.org/10.1016/j.jes.2016.08.023
Kaplan CW, Kitts CL (2004) Bacterial succession in a petroleum land treatment unit. Appl Environ Microbiol 70(3):1777–1786. https://doi.org/10.1128/AEM.70.3.1777-1786.2004
Karlapudi AP, Venkateswarulu TC, Tammineedi J, Kanumuri L, Ravuru BK, Dirisala VR, Kodali VP (2018) Role of biosurfactants in bioremediation of oil pollution-a review. Petroleum 4(3):241–249. https://doi.org/10.1016/j.petlm.2018.03.007
Kato C, lnoue A, Horikoshi K (1996) Isolating and characterizing deep-sea marine microorganisms. Trends Biotechnol 14: 6–12. https://doi.org/10.1016/0167-7799(96)80907-3
Khan MAI, Biswas B, Smith E, Mahmud SA, Hasan NA, Khan MAW, Naidu R, Megharaj M (2018) Microbial diversity changes with rhizosphere and hydrocarbons in contrasting soils. Ecotoxicol Environ Saf 156:434–442. https://doi.org/10.1016/j.ecoenv.2018.03.006
Khara P, Roy M, Chakraborty J, Ghosal D, Dutta TK (2014) Functional characterization of diverse ring-hydroxylating oxygenases and induction of complex aromatic catabolic gene clusters in Sphingobium sp. PNB. FEBS Open Bio 4:290–300. https://doi.org/10.1016/j.fob.2014.03.001
Kim JG, Kim SH, Yoon JH, Lee PC (2013) Carotenoid production from n-alkanes with a broad range of chain lengths by the novel species Gordonia ajoucoccus A2T. Appl Microbiol Biotechnol 98:3759–3768. https://doi.org/10.1007/s00253-014-5516-y
Kim SJ, Park SJ, Jung M, Kim JG, Min UG, Hong HJ, Rhee SK (2014) Draft genome sequence of an aromatic compound-degrading bacterium, Desulfobacula sp. TS, belonging to the Deltaproteobacteria. FEMS Microbiol Lett 360(1):9–12. https://doi.org/10.1111/1574-6968.12591
Kleindienst S, Herbst FA, Stagars M, von Netzer F, von Bergen M, Seifert J, Peplies J, Amann R, Musat F, Lueders T, Knittel K (2014) Diverse sulfate-reducing bacteria of the Desulfosarcina/Desulfococcus clade are the key alkane degraders at marine seeps. ISME J 8(10):2029–2044. https://doi.org/10.1038/ismej.2014.51
Kleindienst S, Paul JH, Joye SB (2015) Using dispersants after oil spills: impacts on the composition and activity of microbial communities. Nat Rev Microbiol 13(6):388–396. https://doi.org/10.1038/nrmicro3452
Kniemeyer O, Musat F, Sievert SM, Knittel K, Wilkes H, Blumenberg M, Michaelis W, Classen A, Bolm C, Joye SB, Widdel F (2007) Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449(7164):898–901. https://doi.org/10.1038/nature06200
Kostichka K, Thomas SM, Gibson KJ, Nagarajan V, Cheng Q (2001) Cloning and characterization of a gene cluster for cyclododecanone oxidation in Rhodococcus ruber SC1. J Bacteriol 183(21):6478–6486. https://doi.org/10.1128/JB.183.21.6478-6486.2001
Kotani T, Kawashima Y, Yurimoto H, Kato N, Sakai Y (2006) Gene structure and regulation of alkane monooxygenases in propane-utilizing Mycobacterium sp. TY-6 and Pseudonocardia sp. TY-7. J. Biosci. Bioeng. 102(3):184–192. https://doi.org/10.1263/jbb.102.184
Kweon O, Kim SJ, Baek S, Chae JC, Adjei MD, Baek DH, Kim YC, Cerniglia CE (2008) A new classification system for bacterial Rieske non-heme iron aromatic ring-hydroxylating oxygenases. BMC Biochem 9:11. https://doi.org/10.1186/1471-2091-9-11
Lal B, Khanna S (1996) Degradation of crude oil by Acinetobacter calcoaceticus and Alcaligenes odorans. J. Appl. Microbiol 81(4):355–362
Lawniczak L, Wozniak-Karczewska M, Loibner AP, Heipieper HJ, Chrzanowski L (2020) Microbial degradation of hydrocarbons-basic principles for bioremediation: a review. Molecules 25(4). https://doi.org/10.3390/molecules25040856
Le TN, Mikolasch A, Awe S, Sheikhany H, Klenk HP, Schauer F (2010) Oxidation of aliphatic, branched chain, and aromatic hydrocarbons by Nocardia cyriacigeorgica isolated from oil-polluted sand samples collected in the Saudi Arabian Desert. J Basic Microbiol 50(3):241–253. https://doi.org/10.1002/jobm.200900358
Lee K, Boufadel M, Chen B, Foght J, Hodson P, Swanson S, Venosa A (2015) Expert panel report on the behaviour and environmental impacts of crude oil released into aqueous environments. Royal Society of Canada, Ottawa, 488.
Li X, Zhao L, Adam M (2016) Biodegradation of marine crude oil pollution using a salt-tolerant bacterial consortium isolated from Bohai Bay, China. Mar Pollut Bull 105(1):43–50. https://doi.org/10.1016/j.marpolbul.2016.02.073
Lim MW, Lau EV, Poh PE (2016) A comprehensive guide of remediation technologies for oil contaminated soil - present works and future directions. Mar Pollut Bull 109(1):14–45. https://doi.org/10.1016/j.marpolbul.2016.04.023
Liu A, Garcia-Dominguez E, Rhine ED, Young LY (2004) A novel arsenate respiring isolate that can utilize aromatic substrates. FEMS Microbiol Ecol 48(3):323–332. https://doi.org/10.1016/j.femsec.2004.02.008
Liu C, Shao Z (2005) Alcanivorax dieselolei sp. nov., a novel alkane-degrading bacterium isolated from sea water and deep-sea sediment. Int. J. Syst. Evol. Microbiol. 55(Pt 3):1181–1186. https://doi.org/10.1099/ijs.0.63443-0
Li H, Boufadel MC (2010) Long-term persistence of oil from the Exxon Valdez spill in two-layer beaches. Nat Geosci 3(2):96–99. https://doi.org/10.1038/ngeo749
Liu C, Wang W, Wu Y, Zhou Z, Lai Q, Shao Z (2011) Multiple alkane hydroxylase systems in a marine alkane degrader, Alcanivorax dieselolei B-5. Environ. Microbiol 13(5):1168–1178. https://doi.org/10.1111/j.1462-2920.2010.02416.x
Liu ZF, Liu JQ, Zhu QZ, Wu W (2012) The weathering of oil after the Deepwater Horizon oil spill: insights from the chemical composition of the oil from the sea surface, salt marshes and sediments. Environ Res Lett 7:035302. https://doi.org/10.1088/1748-9326/7/3/035302
Liu Q, Tang J, Gao K, Gurav R, Giesy JP (2017a) Aerobic degradation of crude oil by microorganisms in soils from four geographic regions of China. Sci Rep 7(1):14856. https://doi.org/10.1038/s41598-017-14032-5
Liu Y, Zeng G, Zhong H, Wang Z, Liu Z, Cheng M, Liu G, Yang X, Liu S (2017b) Effect of rhamnolipid solubilization on hexadecane bioavailability: enhancement or reduction? J Hazard Mater 322(Pt B): 394–401. https://doi.org/10.1016/j.jhazmat.2016.10.025
Lovley DR, Lonergan DJ (1990) Anaerobic oxidation of toluene, phenol, and p-cresol by the dissimilatory iron-reducing organism, GS-15. Appl Environ Microbiol 56(6):1858–1864. https://doi.org/10.1128/aem.56.6.1858-1864.1990
Luo W, Zhao Y, Ding H, Lin X, Zheng H (2008) Co-metabolic degradation of bensulfuron-methyl in laboratory conditions. J Hazard Mater 158(1):208–214. https://doi.org/10.1016/j.jhazmat.2008.02.115
Luo W, Zhu X, Chen W, Duan Z, Wang L, Zhou Y (2014) Mechanisms and strategies of microbial cometabolism in the degradation of organic compounds - chlorinated ethylenes as the model. Water Sci Technol 69(10):1971–1983. https://doi.org/10.2166/wst.2014.108
Lv M, Luan X, Liao C, Wang D, Liu D, Zhang G, Jiang G, Chen L (2020) Human impacts on polycyclic aromatic hydrocarbon distribution in Chinese intertidal zones. Nat Sustain 3(10):878–884. https://doi.org/10.1038/s41893-020-0565-y
Michel J, Fegley SR, Dahlin JA, Wood C (2017) Oil spill response-related injuries on sand beaches: When shoreline treatment extends the impacts beyond the oil. Mar Ecol Prog Ser 576:203–218. https://doi.org/10.3354/meps11917
Ma YL, Lu W, Wan LL, Luo N (2015) Elucidation of fluoranthene degradative characteristics in a newly isolated Achromobacter xylosoxidans DN002. Appl Biochem Biotechnol 175(3):1294–1305. https://doi.org/10.1007/s12010-014-1347-7
Mahmoud GA, Bagy MMK (2018) Microbial degradation of petroleum hydrocarbons. Microbial Action on Hydrocarbons:299–320. https://doi.org/10.1007/978-981-13-1840-5_12
Martínez-Palou R, de Lourdes MM, Zapata-Rendón B, Mar-Juárez E, Bernal-Huicochea C, de la Cruz C-LJ, Aburto J (2011) Transportation of heavy and extra-heavy crude oil by pipeline: a review. J Pet Sci Eng 75(3-4):274–282. https://doi.org/10.1016/j.petrol.2010.11.020
Maiti A, Das S, Bhattacharyya N (2012) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons by Bacillus thuringiensis strain NA2. J Sci 1:72–75
Mallick S, Chakraborty J, Dutta TK (2011) Role of oxygenases in guiding diverse metabolic pathways in the bacterial degradation of low-molecular-weight polycyclic aromatic hydrocarbons: a review. Crit Rev Microbiol 37(1):64–90. https://doi.org/10.3109/1040841X.2010.512268
Mallick S, Chatterjee S, Dutta TK (2007) A novel degradation pathway in the assimilation of phenanthrene by Staphylococcus sp. strain PN/Y via meta-cleavage of 2-hydroxy-1-naphthoic acid: formation of trans-2,3-dioxo-5-(2'-hydroxyphenyl)-pent-4-enoic acid. Microbiology (Reading) 153(Pt 7):2104–2115. https://doi.org/10.1099/mic.0.2006/004218-0
McGenity TJ (2014) Hydrocarbon biodegradation in intertidal wetland sediments. Curr Opin Biotechnol 27:46–54. https://doi.org/10.1016/j.copbio.2013.10.010
McGenity TJ (2019) Taxonomy, genomics and ecophysiology of hydrocarbon-degrading microbes. Hydrocarbon-Degrading Microbes 12
Meckenstock RU, Boll M, Mouttaki H, Koelschbach JS, Cunha Tarouco P, Weyrauch P, Dong X, Himmelberg AM (2016) Anaerobic degradation of benzene and polycyclic aromatic hydrocarbons. J Mol Microbiol Biotechnol 26(1–3):92–118. https://doi.org/10.1159/000441358
Meckenstock RU, Mouttaki H (2011) Anaerobic degradation of non-substituted aromatic hydrocarbons. Curr Opin Biotechnol 22(3):406–414. https://doi.org/10.1016/j.copbio.2011.02.009
Megharaj M, Ramakrishnan B, Venkateswarlu K, Sethunathan N, Naidu R (2011) Bioremediation approaches for organic pollutants: a critical perspective. Environ. Int 37(8):1362–1375. https://doi.org/10.1016/j.envint.2011.06.003
Mercer K, Trevors JT (2011) Remediation of oil spills in temperate and tropical coastal marine environments. The Environmentalist 31(3):338–347. https://doi.org/10.1007/s10669-011-9335-8
Meyer S, Moser R, Neef A, Stahl U, Kampfer P (1999) Differential detection of key enzymes of polyaromatic-hydrocarbon-degrading bacteria using PCR and gene probes. Microbiology 145(Pt 7):1731–1741. https://doi.org/10.1099/13500872-145-7-1731
Meyer S, Steinhart H (2000) Effects of heterocyclic PAHs (N S O) on the biodegradation of typical tar oil PAHs in a soil compost mixture. Chemosphere 40(4):359–367. https://doi.org/10.1016/S0045-6535(99)00237-4
Minerdi D, Sadeghi SJ, Di Nardo G, Rua F, Castrignanò S, Allegra P, Gilardi G (2015) CYP116B5: a new class VII catalytically self-sufficient cytochrome P450 from Acinetobacter radioresistens that enables growth on alkanes. Mol. Microbio 95(3):539–554. https://doi.org/10.1111/mmi.12883
Miralles G, Grossi V, Acquaviva M, Duran R, Claude Bertrand J, Cuny P (2007) Alkane biodegradation and dynamics of phylogenetic subgroups of sulfate-reducing bacteria in an anoxic coastal marine sediment artificially contaminated with oil. Chemosphere 68(7):1327–1334. https://doi.org/10.1016/j.chemosphere.2007.01.033
Mishra B, Varjani S, Agrawal DC, Mandal SK, Ngo HH, Taherzadeh MJ, Chang JS, You S, Guo W (2020) Engineering biocatalytic material for the remediation of pollutants: a comprehensive review. Environ. Technol. Innov 20:101063. https://doi.org/10.1016/j.eti.2020.101063
Mishra S, Singh SN (2012) Microbial degradation of n-hexadecane in mineral salt medium as mediated by degradative enzymes. Bioresour Technol 111:148–154. https://doi.org/10.1016/j.biortech.2012.02.049
Mohamad Shahimin MF, Foght JM, Siddique T (2016) Preferential methanogenic biodegradation of short-chain n-alkanes by microbial communities from two different oil sands tailings ponds. Sci Total Environ 553:250–257. https://doi.org/10.1016/j.scitotenv.2016.02.061
Moreno R, Rojo F (2019) Enzymes for aerobic degradation of alkanes in bacteria. Aerobic utilization of hydrocarbons, oils, and lipids, handbook of hydrocarbon and lipid microbiology:117–142
Muangchinda C, Pansri R, Wongwongsee W, Pinyakong O (2013) Assessment of polycyclic aromatic hydrocarbon biodegradation potential in mangrove sediment from Don Hoi Lot, Samut Songkram Province, Thailand. J Appl Microbiol 114(5):1311–1324. https://doi.org/10.1111/jam.12128
Muratova AY, Turkovskaya OV, Antonyuk LP, Makarov OE, Pozdnyakova LI, Ignatov VV (2005) Oil-oxidizing potential of associative Rhizobacteria of the genus Azospirillum. Microbiology 74(2):210–215. https://doi.org/10.1007/s11021-005-0053-4
Nhi-Cong LT, Lien DT, Gupta BS, Mai CTN, Ha HP, Nguyet NTM, Duan TH, Van Quyen D, Zaid HFM, Sankaran R, Show PL (2020) Enhanced degradation of diesel oil by using biofilms formed by indigenous purple photosynthetic bacteria from oil-contaminated coasts of vietnam on different carriers. Appl Biochem Biotechnol 191(1):313–330. https://doi.org/10.1007/s12010-019-03203-x
Nhi-Cong LT, Mikolasch A, Klenk HP, Schauer F (2009) Degradation of the multiple branched alkane 2,6,10,14-tetramethyl-pentadecane (pristane) in Rhodococcus ruber and Mycobacterium neoaurum. Int Biodeter Biodegr 63(2):201–207. https://doi.org/10.1016/j.ibiod.2008.09.002
Nie Y, Liang JL, Fang H, Tang YQ, Wu XL (2014) Characterization of a CYP153 alkane hydroxylase gene in a Gram-positive Dietzia sp. DQ12-45-1b and its “team role” with alkW1 in alkane degradation. Appl Microbiol Biotechnol 98(1):163–173. https://doi.org/10.1007/s00253-013-4821-1
Nopcharoenkul W, Netsakulnee P, Pinyakong O (2013) Diesel oil removal by immobilized Pseudoxanthomonas sp.RN402. Biodegradation 24:387–397. https://doi.org/10.1007/s10532-012-9596-z
Nwankwegu AS, Zhang L, Xie D, Onwosi CO, Muhammad WI, Odoh CK, Sam K, Idenyi JN (2022) Bioaugmentation as a green technology for hydrocarbon pollution remediation. Problems and prospects. J Environ Manage 304:114313. https://doi.org/10.1016/j.jenvman.2021.114313
Nzila A (2018) Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons under anaerobic conditions: overview of studies, proposed pathways and future perspectives. Environ Pollut 239:788–802
Obahiagbon KO, Amenaghawon AN, Agbonghae EO (2014) The effect of initial pH on the bioremediation of crude oil polluted water using a consortium of microbes. Pacific J Sci Technol 15(1). https://doi.org/10.1016/j.envpol.2018.04.074
Parales RE, Ditty JL, Harwood CS (2000) Toluene-degrading bacteria are chemotactic towards the environmental pollutants benzene, toluene, and trichloroethylene. Appl Environ Microbiol 66(9):4098–4104. https://doi.org/10.1128/AEM.66.9.4098-4104.2000
Partovinia A, Rasekh B (2018) Review of the immobilized microbial cell systems for bioremediation of petroleum hydrocarbons polluted environments. Crit Rev Environ Sci Technol 48(1):1–38. https://doi.org/10.1080/10643389.2018.1439652
Patel V, Cheturvedula S, Madamwar D (2012) Phenanthrene degradation by Pseudoxanthomonas sp. DMVP2 isolated from hydrocarbon contaminated sediment of Amlakhadi canal, Gujarat, India. J Hazard Mater 201–202:43–51. https://doi.org/10.1016/j.jhazmat.2011.11.002
Pei XH, Zhan XH, Wang SM, Lin YS, Zhou LX (2010) Effects of a biosurfactant and a synthetic surfactant on phenanthrene degradation by a sphingomonas strain. Pedosphere 20(6):771–779. https://doi.org/10.1016/S1002-0160(10)60067-7
Perry JJ (2015) Thermoleophilum. BMSAB:1–6
Pi Y, Xu N, Bao M, Li Y, Lv D, Sun P (2015) Bioremediation of the oil spill polluted marine intertidal zone and its toxicity effect on microalgae. Environ Sci-Proc Imp 17:877–885. https://doi.org/10.1016/S1002-0160(10)60067-7
Pilloni G, von Netzer F, Engel M, Lueders T (2011) Electron acceptor-dependent identification of key anaerobic toluene degraders at a tar-oil-contaminated aquifer by Pyro-SIP. FEMS Microbiol Ecol 78(1):165–175. https://doi.org/10.1111/j.1574-6941.2011.01083.x
Pleshakova YV, Belyakov AY, Deev DV (2019) Characteristics of hydrocarbon degradation by bacteria isolated from drill cuttings. Biology Bulletin 45(10):1174–1181. https://doi.org/10.1134/S1062359018100229
Prince RC (2005) The microbiology of marine oil spill bioremediation. Petroleum Microbiology:318–335. https://doi.org/10.1128/9781555817589.ch16
Prince RC, McFarlin KM, Butler JD, Febbo EJ, Wang FC, Nedwed TJ (2013) The primary biodegradation of dispersed crude oil in the sea. Chemosphere 90(2):521–526. https://doi.org/10.1016/j.chemosphere.2012.08.020
Prince RC, Bragg JR (1997) Shoreline bioremediation following the Exxon Valdez oil spill in Alaska. Bioremediat J 1(2):97–104 https://doi.org/10.1080/10889869709351324
Price ARG (1998) Impact of the 1991 Gulf War on the coastal environment and ecosystems: Current status and future prospects. Environ Int 24(1–2):91–96. https://doi.org/10.1016/S0160-4120(97)00124-4
Qi YB, Wang CY, Lv CY, Lun ZM, Zheng CG (2017) Removal capacities of polycyclic aromatic hydrocarbons (PAHs) by a newly isolated strain from oilfield produced water. Int J Environ Res Public Health 14(2). https://doi.org/10.3390/ijerph14020215
Rabus R, Boll M, Heider J, Meckenstock RU, Buckel W, Einsle O, Ermler U, Golding BT, Gunsalus RP, Kroneck PM, Kruger M, Lueders T, Martins BM, Musat F, Richnow HH, Schink B, Seifert J, Szaleniec M, Treude T et al (2016) Anaerobic microbial degradation of hydrocarbons: from enzymatic reactions to the environment. J Mol Microbiol Biotechnol 26(1–3):5–28. https://doi.org/10.1159/000443997
Rabalais S, Flint R (1983) Ixtoc-I effects on intertidal and subtidal infauna of south Texas Gulf beaches. Contrib Mar Sci 26:23–35 http://hdl.handle.net/1969.3/27416
Rabus R, Widdel F (1995) Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microbiot 163:96–103. https://doi.org/10.1007/BF00381782
Radwan SS, Al-Hasan RH, Mahmoud HM, Eliyas M (2007) Oil-utilizing bacteria associated with fish from the Arabian Gulf. J Appl Microbiol 103(6):2160–2167. https://doi.org/10.1111/j.1365-2672.2007.03454.x
Ramsay MA, Swannell RPJ, Shipton W, Duke NC (2000) Effect of bioremediation on the microbial community in oiled mangrove sediments. Mar Pollut Bull 41(7–12):413–419. https://doi.org/10.1016/S0025-326X(00)00137-5
Rojo F (2009) Degradation of alkanes by bacteria. Environ Microbiol 11(10):2477–2490. https://doi.org/10.1111/j.1462-2920.2009.01948.x
Ron EZ, Rosenberg E (2014) Enhanced bioremediation of oil spills in the sea. Curr Opin Biotechnol 27:191–194. https://doi.org/10.1016/j.copbio.2014.02.004
Ruan B, Wu P, Chen M, Lai X, Chen L, Yu L, Gong B, Kang C, Dang Z, Shi Z, Liu Z (2018) Immobilization of Sphingomonas sp. GY2B in polyvinyl alcohol-alginate-kaolin beads for efficient degradation of phenol against unfavorable environmental factors. Ecotoxicol Environ Saf 162:103–111. https://doi.org/10.1016/j.ecoenv.2018.06.058
Saito A, Iwabuchi T, Harayama S (2000) A novel phenanthrene dioxygenase from Nocardioides sp. strain KP7: expression in Escherichia coli. J Bacteriol 182:2134–2144. https://doi.org/10.1128/JB.182.8.2134-2141.2000
Sakai Y, Maeng JH, Kubota S, Tani A, Tani Y, Kato N (1996) A non-conventional dissimilation pathway for long chain n-alkanes in Acinetobacter sp. M-1 that starts with a dioxygenase reaction. J Ferment Bioeng 8(4):286–291. https://doi.org/10.1016/0922-338X(96)80578-2
Santiago MB, Moraes TDS, Massuco JE, Silva LO, Lucarini R, da Silva DF, Vieira TM, Crotti AEM, Martins CHG (2018) In vitro evaluation of essential oils for potential antibacterial effects against Xylella fastidiosa. J Phytopathol 166(11–12):790–798. https://doi.org/10.1111/jph.12762
Sarma PM, Duraja P, Deshpande S, Lal B (2010) Degradation of pyrene by an enteric bacterium, Leclercia adecarboxylata PS4040. Biodegradation 21(1):59–69. https://doi.org/10.1007/s10532-009-9281-z
Scheps D, Malca SH, Hoffmann H, Nestl BM, Hauer B (2011) Regioselective omega-hydroxylation of medium-chain n-alkanes and primary alcohols by CYP153 enzymes from Mycobacterium marinum and Polaromonas sp. strain JS666. Org Biomol Chem 9(19):6727–6733. https://doi.org/10.1039/C1OB05565H
Schneiker S, Martins dos Santos VA, Bartels D, Bekel T, Brecht M, Buhrmester J, Chernikova TN, Denaro R, Ferrer M, Gertler C, Goesmann A, Golyshina OV, Kaminski F, Khachane AN, Lang S, Linke B, McHardy AC, Meyer F, Nechitaylo T et al (2006) Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nat Biotechnol 24(8):997–1004. https://doi.org/10.1038/nbt1232
Sekine M, Tanikawa S, Omata S, Saito M, Fujisawa T, Tsukatani N, Tajima T, Sekigawa T, Kosugi H, Matsuo Y, Nishiko R, Imamura K, Ito M, Narita H, Tago S, Fujita N, Harayama S (2006) Sequence analysis of three plasmids harboured in Rhodococcus erythropolis strain PR4. Environ Microbiol 8(2):334–346. https://doi.org/10.1111/j.1462-2920.2005.00899.x
Šepič E, Bricelj M, Leskovsˇek H (1997) Biodegradation studies of polyaromatic hydrocarbons in aqueous media. J Appl Microbiol 83:561–568. https://doi.org/10.1046/j.1365-2672.1997.00261.x
Shaoping K, Zhiwei D, Bingchen W, Huihui W, Jialiang L, Hongbo S (2021) Changes of sensitive microbial community in oil polluted soil in the coastal area in Shandong, China for ecorestoration. Ecotoxicol Environ Saf 207:111551. https://doi.org/10.1016/j.ecoenv.2020.111551
Sherry A, Gray ND, Ditchfield AK, Aitken CM, Jones DM, Röling WFM, Hallmann C, Larter SR, Bowler BFJ, Head IM (2013) Anaerobic biodegradation of crude oil under sulphate-reducing conditions leads to only modest enrichment of recognized sulphate-reducing taxa. Int Biodeter Biodegr 81:105–113. https://doi.org/10.1016/j.ibiod.2012.04.009
Shigenaka G (2014) Twenty-five years after the Exxon Valdez oil spill-NOAA’s scientific support, monitoring, and research. NOAA Office of Response and Restoration, Seattle, 78 pp
Shinoda Y, Sakai Y, Ué M, Hiraishi A, Kato N (2000) Isolation and characterization of a new denitrifying Spirillum. Appl Environ Microbiol 66(4):1286–1291. https://doi.org/10.1128/AEM.66.4.1286-1291.2000
Shinoda Y, Sakai Y, Uenishi H, Uchihashi Y, Hiraishi A, Yukawa H, Yurimoto H, Kato N (2004) Aerobic and anaerobic toluene degradation by a newly isolated denitrifying bacterium, Thauera sp. strain DNT-1. Appl Environ Microbiol 70(3):1385–1392. https://doi.org/10.1128/AEM.70.3.1385-1392.2004
Singh SN, Kumari B, Mishra S (2012) Microbial degradation of alkanes. Microbial Degradation of Xenobiotics, Environmental Science and Engineering, pp 439–469. https://doi.org/10.1007/978-3-642-23789-8_17
Singleton DR, Ramirez LG, Aitken MD (2009) Characterization of a polycyclic aromatic hydrocarbon degradation gene cluster in a phenanthrene-degrading Acidovorax strain. Appl Environ Microbiol 75(9):2613–2620. https://doi.org/10.1128/AEM.01955-08
Sivaram AK, Logeshwaran P, Lockington R, Naidu R, Megharaj M (2019) Low molecular weight organic acids enhance the high molecular weight polycyclic aromatic hydrocarbons degradation by bacteria. Chemosphere 222:132–140. https://doi.org/10.1016/j.chemosphere.2019.01.110
Soleimani M, Farhoudi M, Christensen JH (2013) Chemometric assessment of enhanced bioremediation of oil contaminated soils. J Hazard Mater 254–255:372–381. https://doi.org/10.1016/j.jhazmat.2013.03.004
Song M, Yang Y, Jiang L, Hong Q, Zhang D, Shen Z, Yin H, Luo C (2017) Characterisation of the phenanthrene degradation-related genes and degrading ability of a newly isolated copper-tolerant bacterium. Environ Pollut 220(Pt B): 1059–1067. https://doi.org/10.1016/j.envpol.2016.11.037
Song XH, Xu Y, Li GM, Zhang Y, Huang TW, Hu Z (2011) Isolation, characterization of Rhodococcus sp. P14 capable of degrading high-molecular-weight polycyclic aromatic hydrocarbons and aliphatic hydrocarbons. Mar Pollut Bull 62(10):2122–2128. https://doi.org/10.1016/j.marpolbul.2011.07.013
Southam G, Whitney M, Knickerbocker C (2001) Structural characterization of the hydrocarbon degrading bacteria oil-interface: implications for bioremediation. Int Biodeter Biodegr 47:197–201. https://doi.org/10.1016/S0964-8305(01)00051-8
Stucki G, Alexander M (1987) Role of dissolution rate and solubility in biodegradation of aromatic compounds. Appl Environ Microbiol 53:292–297. https://doi.org/10.1128/aem.53.2.292-297.1987
Suganthi SH, Murshid S, Sriram S, Ramani K (2018) Enhanced biodegradation of hydrocarbons in petroleum tank bottom oil sludge and characterization of biocatalysts and biosurfactants. J Environ Manage 220:87–95. https://doi.org/10.1016/j.jenvman.2018.04.120
Sun W, Dong Y, Gao P, Fu M, Ta K, Li J (2015a) Microbial communities inhabiting oil-contaminated soils from two major oilfields in Northern China: implications for active petroleum-degrading capacity. J Microbiol 53(6):371–378. https://doi.org/10.1007/s12275-015-5023-6
Sun YM, Ning ZG, Yang F, Li XZ (2015b) Characteristics of newly isolated Geobacillus sp. ZY-10 degrading hydrocarbons in crude oil. Pol J Microbiol 64(3):253–263
Swannell RPJ, Lee K, Mcdonagh M (1996) Field evaluations of marine oil spill bioremediation. Microbiol Rev 60(2):342–365. https://doi.org/10.1128/mr.60.2.342-365.1996
Tao K, Zhang X, Chen X, Liu X, Hu X, Yuan X (2019) Response of soil bacterial community to bioaugmentation with a plant residue-immobilized bacterial consortium for crude oil removal. Chemosphere 222:831–838. https://doi.org/10.1016/j.chemosphere.2019.01.133
Tapilatu Y, Acquaviva M, Guigue C, Miralles G, Bertrand JC, Cuny P (2010) Isolation of alkane-degrading bacteria from deep-sea Mediterranean sediments. Lett Appl Microbiol 50(2):234–236. https://doi.org/10.1111/j.1472-765X.2009.02766.x
Teng Y, Luo Y, Sun M, Liu Z, Li Z, Christie P (2010) Effect of bioaugmentation by Paracoccus sp. strain HPD-2 on the soil microbial community and removal of polycyclic aromatic hydrocarbons from an aged contaminated soil. Bioresour. Technol 101(10):3437–3443. https://doi.org/10.1016/j.biortech.2009.12.088
Thangaraj K, Kapley A, Purohit HJ (2008) Characterization of diverse Acinetobacter isolates for utilization of multiple aromatic compounds. Bioresour Technol 99(7):2488–2494. https://doi.org/10.1016/j.biortech.2007.04.053
Taylor E, Reimer D (2008) Oil persistence on beaches in Prince William Sound—a review of SCAT surveys conducted from 1989 to 2002. Mar Pollut Bull 56(3):458–474. https://doi.org/10.1016/j.marpolbul.2007.11.008
Thavasi R, Jayalakshmi S, Balasubramanian T, Banat IM (2006) Biodegradation of crude oil by nitrogen fixing marine bacteria Azotobacter chroococcum. Res J Microbiol 1(5):401–408. https://doi.org/10.3923/jm.2006.401.408
Throne-Holst M, Markussen S, Winnberg A, Ellingsen TE, Kotlar HK, Zotchev SB (2006) Utilization of n-alkanes by a newly isolated strain of Acinetobacter venetianus: the role of two AlkB-type alkane hydroxylases. Appl Microbiol Biotechnol 72(2):353–360. https://doi.org/10.1007/s00253-005-0262-9
Throne-Holst M, Wentzel A, Ellingsen TE, Kotlar HK, Zotchev SB (2007) Identification of novel genes involved in long-chain n-alkane degradation by Acinetobacter sp. strain DSM 17874. Appl Environ Microbiol 73(10):3327–3332. https://doi.org/10.1128/AEM.00064-07
Turner DA, Pichtel J, Rodenas Y, McKillip J, Goodpaster JV (2015) Microbial degradation of gasoline in soil: effect of season of sampling. Forensic Sci Int 251:69–76. https://doi.org/10.1016/j.forsciint.2015.03.013
Uad I, Silva-Castro GA, Pozo C, González-López J, Calvo C (2010) Biodegradative potential and characterization of bioemulsifiers of marine bacteria isolated from samples of seawater, sediment and fuel extracted at 4000 m of depth (Prestige wreck). Int Biodeterior Biodegr 64(6):511–518. https://doi.org/10.1016/j.ibiod.2010.06.005
Varjani SJ (2017) Microbial degradation of petroleum hydrocarbons. Bioresour Technol 223:277–286. https://doi.org/10.1016/j.biortech.2016.10.037
Varjani SJ, Thaker MB, Upasani VN (2014) Optimization of growth conditions of native hydrocarbon utilizing bacterial consortium “HUBC” obtained from petroleum pollutant contaminated sites. Indian J App Res 4(10):474–476
Varjani SJ, Upasani VN (2016) Biodegradation of petroleum hydrocarbons by oleophilic strain of Pseudomonas aeruginosa NCIM 5514. Bioresour Technol 222:195–201. https://doi.org/10.1016/j.biortech.2016.10.006
Varjani SJ, Upasani VN (2016b) Carbon spectrum utilization by an indigenous strain of Pseudomonas aeruginosa NCIM 5514: production, characterization and surface active properties of biosurfactant. Bioresour Technol 221:510–516. https://doi.org/10.1016/j.biortech.2016.09.080
Varjani SJ, Upasani VN (2016a) Core flood study for enhanced oil recovery through ex-situ bioaugmentation with thermo- and halo-tolerant rhamnolipid produced by Pseudomonas aeruginosa NCIM 5514. Bioresour. Technol. 220:175–182. https://doi.org/10.1016/j.biortech.2016.08.060
Varjani SJ, Upasani VN (2017) A new look on factors affecting microbial degradation of petroleum hydrocarbon pollutants. Int Biodeter Biodegr 120:71–83. https://doi.org/10.1016/j.ibiod.2017.02.006
Venosa AD, Haines JR, Allen DM (1992) Efficacy of commercial inocula in enhancing biodegradation of weathered crude oil contaminating a Prince William Sound beach. J Ind Microbiol 10:1–11. https://doi.org/10.1007/BF01583628
Venosa AD, Suidan MT, Wrenn BA, Strohmeier KL, Haines JR, Eberhart BL, King D, Holder E (1996) Bioremediation of an exprimental oil spill on the shoreline of Delaware Bay. Environ Sci Technol 30(5):1764–1775. https://doi.org/10.1021/es950754r
Venosa AD, Zhu XQ (2003) Biodegradation of crude oil contaminating marine shorelines and freshwater wetlands. Spill Sci Technol B 8(2):163–178. https://doi.org/10.1016/S1353-2561(03)00019-7
Vila J, Maria Nieto J, Mertens J, Springael D, Grifoll M (2010) Microbial community structure of a heavy fuel oil-degrading marine consortium: linking microbial dynamics with polycyclic aromatic hydrocarbon utilization. FEMS Microbiol Ecol 73(2):349–362. https://doi.org/10.1111/j.1574-6941.2010.00902.x
Walworth J, Pond A, Snape I, Rayner J, Ferguson S, Harvey P (2007) Nitrogen requirements for maximizing petroleum bioremediation in a sub-Antarctic soil. Cold Reg Sci Technol 48(2):84–91. https://doi.org/10.1016/j.coldregions.2006.07.001
Wang H, Gilbert JA, Zhu Y, Yang X (2018a) Salinity is a key factor driving the nitrogen cycling in the mangrove sediment. Sci Total Environ 631–632:1342–1349. https://doi.org/10.1016/j.scitotenv.2018.03.102
Wang L, Wang W, Lai Q, Shao Z (2010) Gene diversity of CYP153A and AlkB alkane hydroxylases in oil-degrading bacteria isolated from the Atlantic Ocean. Environ Microbiol 12(5):1230–1242. https://doi.org/10.1111/j.1462-2920.2010.02165.x
Wang W, Wang L, Shao Z (2018b) Polycyclic aromatic hydrocarbon (PAH) degradation pathways of the obligate marine PAH degrader Cycloclasticus sp. strain P1. Appl Environ Microbiol 84(21). https://doi.org/10.1128/AEM.01261-18
Wang WP, Shao ZZ (2012) Diversity of flavin-binding monooxygenase genes (almA) in marine bacteria capable of degradation long-chain alkanes. FEMS Microbiol Ecol 80(3):523–533. https://doi.org/10.1111/j.1574-6941.2012.01322.x
Wang X, Liu Y, Song C, Yuan X, Zhang Q, Miao Y (2020a) Application analysis of immobilized bioremediation preparation in oil spill contaminated shore. IOP Conference Series: Earth and Environmental Science 558:042029. https://doi.org/10.1088/1755-1315/558/4/042029
Wang X, Sun L, Wang H, Wu H, Chen S, Zheng X (2018c) Surfactant-enhanced bioremediation of DDTs and PAHs in contaminated farmland soil. Environ Technol 39(13):1733–1744. https://doi.org/10.1080/09593330.2017.1337235
Wang Z, An CJ, Lee K, Owens E, Chen Z, Boufadel M, Taylor E, Feng Q (2020b) Factors influencing the fate of oil spilled on shorelines: a review. Environ Chem Lett 19(2):1611–1628. https://doi.org/10.1007/s10311-020-01097-4
Wang ZD (2007) Oil spill environmental forensics: fingerprinting and source identification.
Weelink SAB, van Eekert MHA, Stams AJM (2010) Degradation of BTEX by anaerobic bacteria: physiology and application. Rev Environ Sci Bio 9(4):359–385. https://doi.org/10.1007/s11157-010-9219-2
Wentzel A, Ellingsen TE, Kotlar HK, Zotchev SB, Throne-Holst M (2007) Bacterial metabolism of long-chain n-alkanes. Appl Microbiol Biotechnol 76(6):1209–1221. https://doi.org/10.1007/s00253-007-1119-1
Widdel F, Rabus R (2001a) Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotech:12. https://doi.org/10.1016/S0958-1669(00)00209-3
Widdel F, Rabus R (2001b) Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotechnol 12(3):259–276. https://doi.org/10.1016/S0958-1669(00)00209-3
Wu RR, Dang Z, Yi XY, Yang C, Lu GN, Guo CL, Liu CQ (2011) The effects of nutrient amendment on biodegradation and cytochrome P450 activity of an n-alkane degrading strain of Burkholderia sp. GS3C. J Hazard Mater 186(2-3):978–983. https://doi.org/10.1016/j.jhazmat.2010.11.095
Xia MQ, Liu Y, Taylor AA, Fu DF, Khan AR, Terry N (2017) Crude oil depletion by bacterial strains isolated from a petroleum hydrocarbon impacted solid waste management site in California. Int Biodeterior Biodegr 123:70–77. https://doi.org/10.1016/j.ibiod.2017.06.003
Xia W, Du Z, Cui Q, Dong H, Wang F, He P, Tang Y (2014) Biosurfactant produced by novel Pseudomonas sp. WJ6 with biodegradation of n-alkanes and polycyclic aromatic hydrocarbons. J Hazard Mater 276:489–498. https://doi.org/10.1016/j.jhazmat.2014.05.062
Xu X, Chen X, Su P, Fang F, Hu B (2016) Biodegradation potential of polycyclic aromatic hydrocarbons by bacteria strains enriched from Yangtze River sediments. Environ Technol 37(5):513–520. https://doi.org/10.1080/09593330.2015.1074289
Xu X, Liu W, Tian S, Wang W, Qi Q, Jiang P, Gao X, Li F, Li H, Yu H (2018) Petroleum hydrocarbon-degrading bacteria for the remediation of oil pollution under aerobic conditions: a perspective analysis. Front Microbiol 9:2885. https://doi.org/10.3389/fmicb.2018.02885
Xue J, Yu Y, Bai Y, Wang L, Wu Y (2015) Marine oil-degrading microorganisms and biodegradation process of petroleum hydrocarbon in marine environments: a review. Curr Microbiol 71(2):220–228. https://doi.org/10.1007/s00284-015-0825-7
Yakimov MM, Giuliano L, Denaro R, Crisafi E, Chernikova TN, Abraham WR, Luensdorf H, Timmis KN, Golyshin PN (2004) Thalassolituus oleivorans gen. nov., sp. nov., a novel marine bacterium that obligately utilizes hydrocarbons. Int J Syst Evol Microbiol 54(Pt 1):141–148. https://doi.org/10.1099/ijs.0.02424-0
Yakimov MM, Giuliano L, Gentile G, Crisafi E, Chernikova TN, Abraham WR, Lunsdorf H, Timmis KN, Golyshin PN (2003) Oleispira antarctica gen. nov., sp. nov., a novel hydrocarbonoclastic marine bacterium isolated from Antarctic coastal sea water. Int J Syst Evol Microbiol 53(Pt 3):779–785. https://doi.org/10.1099/ijs.0.02366-0
Yuste L, Corbella ME, Turiégano MJ, Karlson U, Puyet A, Rojo F (2000) Characterization of bacterial strains able to grow on high molecular mass residues from crude oil processing. FEMS Microbiol Ecol 32:69–75. https://doi.org/10.1111/j.1574-6941.2000.tb00700.x
Yuewen D, Adzigbli L (2018) Assessing the impact of oil spills on marine organisms. J Oceanogr Mar Res 6:472–479
Zahed MA, Salehi S, Madadi R, Hejabi F (2021) Biochar as a sustainable product for remediation of petroleum contaminated soil. Curr Res Green Sust Chem 4:100055. https://doi.org/10.1016/j.crgsc.2021.100055
Zeng J, Zhu Q, Wu Y, Chen H, Lin X (2017) Characterization of a polycyclic aromatic ring-hydroxylation dioxygenase from Mycobacterium sp. NJS-P. Chemosphere 185:67–74. https://doi.org/10.1016/j.chemosphere.2017.07.001
Zengler K, Heider J, Rosselló-Mora R, Widdel F (1999) Phototrophic utilization of toluene under anoxic conditions by a new strain of Blastochloris sulfoviridis. Arch Microbiol 172:204–212. https://doi.org/10.1007/s002030050761
Zhang B, Matchinski EJ, Chen B, Ye X, Jing L, Lee K (2019a) Marine oil spills—oil pollution, sources and effects. 391–406. https://doi.org/10.1016/B978-0-12-805052-1.00024-3
Zhang J, Lin XG, Liu WW, Wang YM, Zeng J, Chen H (2012) Effect of organic wastes on the plant-microbe remediation for removal of aged PAHs in soils. J Environ Sci (China) 24(8):1476–1482. https://doi.org/10.1016/S1001-0742(11)60951-0
Zhang S, Hu Z, Wang H (2019b) Metagenomic analysis exhibited the co-metabolism of polycyclic aromatic hydrocarbons by bacterial community from estuarine sediment. Environ Int 129:308–319 https://doi.org/10.1016/j.envint.2019.05.028
Zhao F, Zhou JD, Ma F, Shi RJ, Han SQ, Zhang J, Zhang Y (2016) Simultaneous inhibition of sulfate-reducing bacteria, removal of H2S and production of rhamnolipid by recombinant Pseudomonas stutzeri Rhl: applications for microbial enhanced oil recovery. Bioresour Technol 207:24–30. https://doi.org/10.1016/j.biortech.2016.01.126
Zheng C, He J, Wang Y, Wang M, Huang Z (2011) Hydrocarbon degradation and bioemulsifier production by thermophilic Geobacillus pallidus strains. Bioresour Technol 102(19):9155–9161. https://doi.org/10.1016/j.biortech.2011.06.074
Zhong H, Liu G, Jiang Y, Yang J, Liu Y, Yang X, Liu Z, Zeng G (2017) Transport of bacteria in porous media and its enhancement by surfactants for bioaugmentation: a review. Biotechnol Adv 35(4):490–504. https://doi.org/10.1016/j.biotechadv.2017.03.009
Zhong H, Liu Y, Liu ZF, Jiang YB, Tan F, Zeng GM, Yuan XZ, Yan M, Niu QY, Liang YS (2014) Degradation of pseudo-solubilized and mass hexadecane by a Pseudomonas aeruginosa with treatment of rhamnolipid biosurfactant. Int Biodeter Biodegra 94:152–159. https://doi.org/10.1016/j.ibiod.2014.07.012
Zhou L, Li H, Zhang Y, Han S, Xu H (2016) Sphingomonas from petroleum-contaminated soils in Shenfu, China and their PAHs degradation abilities. Braz J Microbiol 47(2):271–278. https://doi.org/10.1016/j.bjm.2016.01.001
Zhu X, Jin L, Sun K, Li S, Ling W, Li X (2016) Potential of endophytic bacterium Paenibacillus sp. PHE-3 isolated from Plantago asiatica L. for reduction of PAH contamination in Plant Tissues. Int J Environ Res Public Health 13(7). https://doi.org/10.3390/ijerph13070633
Zhuang WQ, Tay JH, Maszenan A, Tay S (2002) Bacillus naphthovorans sp. nov. from oil-contaminated tropical marine sediments and its role in naphthalene biodegradation. Appl. Microbiol. Biotechnol 58:547–554
Funding
The work is financially supported by the National Key Research and Development Program of China (No. 2022YFC3203001) and the Sprout Project of Beijing Academy of Science and Technology (No. 2022A-0006).
Author information
Authors and Affiliations
Contributions
XLD: writing—original draft, conceptualization, and resources; JL: writing—review and editing and resources; SHG: writing—review and editing; PCF: writing—review and editing, conceptualization, methodology, and supervision.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Robert Duran
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Dai, ., Lv, J., Fu, P. et al. Microbial remediation of oil-contaminated shorelines: a review. Environ Sci Pollut Res 30, 93491–93518 (2023). https://doi.org/10.1007/s11356-023-29151-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-29151-y