Introduction

Oceans and seas cover approximately 70% of the Earth’s surface, play a crucial role in the regulation of the global climate, and provide half of the atmospheric oxygen (Bollmann et al. 2010). The estimated total volume of the five oceans (the Pacific, Atlantic, Indian, Arctic, and Antarctic oceans) is 1.332 × 109 km3; these oceans are considered the largest continuous ecosystem (Charette and Smith 2010) and contain a large number of diverse habitats, allowing the life of a plethora of (micro)organisms.

Bacteria and archaea occupy virtually all marine ecosystems, and their quantity in oceans (including water and upper and deep oceanic sediments) is calculated to be 5.5 × 1029 cells, representing up to 90% of the total marine biomass (Flemming and Wuertz 2019). In addition, bacteria and archaea play pivotal roles in the ocean biogeochemical cycles of carbon, oxygen, nitrogen, phosphorous, sulfur, and iron (Azam and Malfatti 2007).

In addition to their ecological role, marine bacteria represent an important source for the biotechnology industry. These microorganisms have developed diverse molecular mechanisms to overcome fluctuating conditions in marine environments (such as changes in salinity, pH, nutrient and oxygen availability, light, pressure, and temperature), rendering them and the bioactive compounds they produce suitable for different applications in the bioremediation, pharmaceutical, cosmetic, and food industries (de la Calle 2017). Bioprospecting of marine bacteria involves a systematic search for useful and valuable products, such as genes, proteins, and secondary metabolites, from these microorganisms that can benefit society (Pardo-López 2019). Both culture methods and culture-independent techniques have been implemented for the exploration of marine bacteria and their biotechnological potential. Using culture techniques, many bacterial species and consortia have been isolated from different marine habitats that exhibit a high capacity to degrade hazardous compounds (Muriel-Millán et al. 2019; Syranidou et al. 2017), produce biopolymers (Higuchi-Takeuchi et al. 2016; Vásquez-Ponce et al. 2017), and express enzymes with unique properties used in industrial (Rodríguez-Salazar et al. 2020; Seghal Kiran et al. 2014) and pharmaceutical processes (Zhang et al. 2016). Furthermore, the isolation of metagenomic DNA from marine habitats coupled with functional screenings has allowed the identification of bioactive compounds, such as enzymes and antimicrobials, from marine bacteria that cannot be cultured (Mahapatra et al. 2020; Park et al. 2007). Recently, we discussed the use of a sequence-based analysis and functional metagenomics to investigate the biotechnology applications of marine bacteria (Rodríguez-Salazar et al. 2021); therefore, here, we focus on biotechnology applications of cultured bacterial species.

Although there is an abundance of information and many reports regarding the diversity of marine bacteria and their biotechnology applications, many marine environments and bacterial communities remain poorly explored and characterized. Indeed, innovative and multidisciplinary approaches have recently been implemented to characterize rare marine bacteria to identify new bioproducts (Smith et al. 2019). Therefore, marine bacteria continue to be a potential source of undiscovered biotechnological tools that could be used to address current global concerns, such as oil and plastic pollution. In this review, we first summarize recent studies that explored marine bacterial diversity at both the global and local levels, and then, we analyze and discuss new experimental information regarding the isolation and characterization of marine bacteria able to degrade hydrocarbons and synthetic plastics, and to produce biosurfactants, which are ecofriendly alternatives to synthetic surfactants (Fig. 1). This review provides an updated landscape of the biotechnological potentials in bioremediation using marine bacteria, which may be implemented as part of the strategies to address environmental pollution by hydrocarbons and plastics.

Fig. 1
figure 1

Biotechnology applications of marine bacteria. Marine environments contain a great diversity of bacteria, and some bacteria play pivotal roles in the biogeochemical cycles of carbon, oxygen, nitrogen, phosphorous, sulfur, and iron. Some biotechnological potentials of marine bacteria include the bioremediation of hydrocarbon- and plastic-polluted environments, and the discovery and production of new biosurfactants, which are natural compounds that enhance the solubilization of hydrophobic molecules (e.g., hydrocarbons)

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Marine bacterial diversity

Bacteria are ubiquitous in oceans; they can be free-living in the water column (pelagic bacteria) and sediments, can form biofilms, and can be associated with higher organisms (Alvarez-Yela et al. 2019; Thiele et al. 2015; Zhang et al. 2019). DNA-sequencing technologies have allowed us to understand marine bacterial diversity and how it is influenced by changes in environmental conditions, such as light, temperature, nutrient and oxygen availability (Salazar and Sunagawa 2017), season (Cram et al. 2015; Ladau et al. 2013), depth (Walsh et al. 2016), and anthropogenic activities (Won et al. 2017).

The Tara Oceans exploration, which was conducted between 2009 and 2013, is among the most comprehensive projects investigating global marine microbial diversity (Karsenti et al. 2011). Based on metagenomics analyses of 139 marine samples collected at 68 locations distributed in all oceans (except for the Arctic Ocean), Sunagawa et al. (2015) estimated that the richness of free-living marine microbes (archaea and bacteria) in the water column includes 37,470 species and identified that, globally, the Alphaproteobacteria and Gammaproteobacteria classes and the Cyanobacteria phylum were the dominant taxa in surface waters. Similar results have been recently reported from particular marine environments, such as the southwestern Gulf of Mexico (Raggi et al. 2020), North Pacific gyre and Equatorial Pacific (Walsh et al. 2016), and Canadian Arctic ocean (Fu et al. 2019). In particular, the alphaproteobacterial SAR11 group (Pelagibacterales) is the most abundant bacterial group in ocean surface waters (< 300 m depth), representing approximately 20–40% of all planktonic cells (Giovannoni 2017). Cyanobacteria represent approximately 20% of the relative abundance on ocean surfaces, and Prochlorococcus and Synechococcus are the dominant genera (Sunagawa et al. 2015). In the mesopelagic zone (200–1000 m depth), Alphaproteobacteria, Gammaproteobacteria, Deltaproteobacteria, and Deferribacteres are the most abundant groups (Sunagawa et al. 2015; Walsh et al. 2016).

Marine sediments also contain a considerable proportion of the bacterial biomass on Earth, with an estimated global bacterial richness of 32,800 species (Hoshino et al. 2020). The bacterial diversity in the ocean floor is influenced by the depth below the surface sediment, oxygen availability, and carbon concentration (Hoshino et al. 2020). Generally, members of Gammaproteobacteria, Alphaproteobacteria, Deltaproteobacteria, Actinobacteria, Nitrospira, and Plantomycetes are highly abundant in marine sediments (Godoy-Lozano et al. 2018; Hoshino et al. 2020; Walsh et al. 2016). Although different metagenomics studies have been performed, the current knowledge regarding the bacterial diversity in marine sediments and the ecological roles of these species remains limited (partially due to the difficulty of sampling), and it is expected that new bacterial species will be identified in the future (Baker et al. 2021). For instance, Dharamshi et al. (2020) recently reported a high abundance of diverse lineages of the Chlamydiae phylum in anoxic sediments from the Arctic Ocean, some of which were likely not associated with eukaryotic hosts, suggesting that these species could play an important ecological role in marine sediments.

As mentioned above, anthropogenic activities also affect marine bacterial diversity. For instance, oil spills in oceans rapidly induce an increase in specialized hydrocarbon-degrading Gammaproteobacteria, such as Alcanivorax, Pseudomonas, Oleispira, and Colwellia, contributing to hydrocarbon biodegradation. Usually, these bacterial communities are present in marine waters and sediments in low abundance (Dubinsky et al. 2013; Godoy-Lozano et al. 2018). Furthermore, plastic wastes in marine environments affect bacterial communities and their function in biogeochemical cycles. Plastic leachates inhibit the growth of some Prochlorococcus species, thereby affecting carbon fixation and oxygen production by these bacteria (Tetu et al. 2019), while microplastics (< 5 mm in size) in marine sediments can disrupt the composition of bacterial communities and impact nitrification and denitrification processes (Seeley et al. 2020). Furthermore, microplastic wastes are rapidly colonized by different bacteria forming biofilms, which can transport bacteria to long distances both vertically and horizontally in oceans (Dussud et al. 2018; Oberbeckmann and Labrenz 2020).

Biodegradation of hydrocarbons by marine bacteria

Oil spills severely affect environments due to the high toxicity of crude oil. Although some physical and chemical treatments are used for the restoration of oil-polluted sites, biological-based strategies are more ecofriendly and efficient than these methods (Mapelli et al. 2017). Endogenous bacterial populations from contaminated sites play an important role in hydrocarbon degradation, contributing to the restoration of the environment. However, bioremediation is affected by some environmental conditions, such as pH, temperature, osmolarity, and pressure. Therefore, marine bacteria are of special interest due to their capacity to degrade petroleum hydrocarbons under different stress conditions (Dash et al. 2013). Some of these bacteria can be isolated by adding hydrocarbons as nutrients (as a sole carbon source) to the culture media used for the inoculation of marine samples obtained from water o sediments. Under this restrictive condition, it is expected that bacteria able to degrade hydrocarbons will be enriched and can be isolated and identified by 16S ribosomal RNA gene or genome sequencing (Fig. 2). Some other species that are unable to use contaminants as nutrients could also be present in the cultures in a reduced proportion (Wang et al. 2008); these other species may work with pollutant degraders to establish metabolic fluxes and enhance the performance of the degraders (Rosas-Díaz et al. 2021; Deines et al. 2020). It is important to note that traditional rich nutrient media usually allow the isolation of faster-growing marine bacteria inhibiting the growth of slower-growing species, and some oligotrophic marine bacteria could be inhibited by nutrient-rich conditions. Therefore, some mineral media such as ONR7a and Bushnell Haas or filtered seawater (low-nutrient medium) may be used for the isolation of hydrocarbon degrading marine bacteria.

Fig. 2
figure 2

Isolation of marine hydrocarbon-degrading bacteria. Samples from seawater or sediments are inoculated in culture media supplemented with hydrocarbons as the sole carbon source. Some mineral media such as ONR7a and Bushnell Haas or filtered seawater (low-nutrient medium) are commonly used for inoculation of marine samples. Incubation conditions affect the structure of bacterial communities. Therefore, we recommend inoculating more than one culture container per sample and incubated them at different temperatures and times (e.g., 4–8 °C for several weeks, or 20–30 °C during 2–4 days) to enrich different bacterial populations. After an incubation period, marine bacteria capable of degrading hydrocarbons will be enriched in the culture. Some species can be isolated by dilutions of the culture and spreading aliquots onto agar plates and further identified by 16S gene sequencing and/or biochemical tests (e.g., Gram staining, morphology, motility, carbohydrate fermentation, catalase, and oxidase). Furthermore, the extraction and sequencing of metagenomic DNA from enriched culture and bioinformatics analyses allow the determination of bacterial diversity and metabolic pathways

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Marine bacterial species belonging to the Alcanivorax, Cycloclasticus, and Marinobacter genera are well known as efficient hydrocarbon degraders and have been isolated from different ecosystems (Table 1). Other marine species have been recently reported to efficiently degrade different hydrocarbons, exhibiting particular traits, such as degradation over a wide range of pH values, temperatures, and NaCl concentrations and biosurfactant production (Table 1). For instance, some species, including Achromobacter (Deng et al. 2014), Halomonas (Cheffi et al. 2020; Mnif et al. 2009), and Staphylococcus (Hentati et al. 2021), degrade alkanes and aromatic hydrocarbons in the presence of high NaCl concentrations (Table 1), which is an important trait because salinity reduces hydrocarbon bioavailability, affecting their degradation (McGenity 2010). High hydrostatic pressure (e.g., in deep-sea sediments) also reduces hydrocarbon availability and impairs the growth of hydrocarbonoclastic bacteria that are sensitive to variations in pressure (Scoma and Boon 2016). Therefore, recent studies have focused on characterizing piezotolerant hydrocarbon-degrading strains. For instance, Alcanivorax venustensis R-72943, an obligate alkane degrader isolated from 530-m-deep marine sediment, exhibited comparable growth at ambient pressure (0.1 Megapascal pressure units-MPa) versus 10 and 30 MPa (Van Landuyt et al. 2020), and the Nesiotobacter exalbescens COD22 strain, which was isolated from marine sediment at a 2100 m depth, efficiently degraded toluene at 0.1 and 10 MPa (Ganesh Kumar et al. 2019) (Table 1). Thus, these species have great potential use for the bioremediation of deep-sea oil spills; however, more research is necessary to understand the piezotolerance-related molecular mechanisms involved during the bacterial degradation of hydrocarbons.

Table 1 Marine hydrocarbon-degrading bacterial strains
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Several reports have demonstrated that a bacterial community may be more efficient for bioremediation than single species because they cannot degrade all compounds in crude oil (Chen et al. 2017; Santisi et al. 2019; Wang et al. 2008). Bacterial consortia, both natural and synthetic, have been tested for oil degradation, for instance, Chen et al. (2017) designed a synthetic consortium comprising five strains (Pseudomonas aeruginosa, Exiguobacterium sp., Bacillus sp., and two Alcaligenes sp.) isolated from crude oil-polluted marine water, which degraded approximately 75% of crude oil, while the five strains individually grown degraded 50–65% of petroleum hydrocarbons. Nevertheless, several combinations of strains should first be evaluated to identify possible competitions among the strains that may affect the consortium’s biodegradation efficiency (Chen et al. 2017), or to identify key strains that increase the hydrocarbons degradation rates when they are in consortia. In addition, the immobilization of consortia or individual species on biodegradable composites, such as untreated cotton fibers (Lin et al. 2014), alginate microspheres (Chen et al. 2017), puffed foxtail millet (Hou et al. 2013), and coconut fibers (Nhi-Cong et al. 2020), protects bacteria from environmental stresses, such as salinity, pH, and temperature, enhancing hydrocarbon degradation. Therefore, marine hydrocarbon-degrading bacteria play a crucial role in the restoration of polluted marine sites and are useful for the design of biotechnological tools for bioremediation.

Hydrocarbon-degrading enzymes from marine bacteria

The molecular and biochemical characterization of enzymes from marine hydrocarbon-degrading bacteria is important for understanding their potential use for bioremediation. Aerobic bacterial degradation of aliphatic hydrocarbons (n-alkanes) involves an initial key step of hydroxylation carried out by alkane hydroxylase enzymes (Rojo 2009). AlkB-type alkane hydroxylases are membrane-embedded enzymes widely distributed among marine alkane-degrading bacteria and exhibit a substrate preference depending on the alkane chain length (Nie et al. 2014). For instance, AlkB from Alcanivorax sp. 2B5 is active on C14, C16, and C18 n-alkanes (Liu et al. 2010), while in Alcanivorax hongdengensis A-11–3 (Wang and Shao 2012) and Alcanivorax dieselolei B-5 (Liu et al. 2010), which contain two homologous AlkB hydroxylases (AlkB1 and AlkB2), these enzymes are induced in the presence of C12-C26. In the P. aeruginosa GOM1 strain, the expression of the alkB1 and alkB2 genes was induced by C8 to C28 n-alkanes (Muriel-Millán et al. 2019). The differences in the substrate preference of AlkB enzymes from distinct strains may be associated with the presence of bulky amino acids lining the substrate-binding site (alkane pocket), limiting the recognition of alkanes based on the hydrocarbon length (van Beilen et al. 2005). Flavin-binding AlmA monooxygenase is another type of alkane hydroxylase that oxidizes long-chain alkanes. In the genomes of both A. hongdengesis A-11–3 and A. dieseolei B-5, one copy of the almA gene is present, and its expression was induced when the strains grew in the presence of C22–C36 n-alkanes (Liu et al. 2010; Wang and Shao 2012). The marine P. aeruginosa GOM1 strain, which exhibits high degradation activity on C18-C38 alkanes, has two copies of the almA gene (Muriel-Millán et al. 2019), which differs from other P. aeruginosa strains isolated from hydrocarbon-polluted environments that contain one copy of almA (Liu et al. 2014; Thomas et al. 2014). The bacterial metabolic capacity of long-chain alkane degradation is of special interest for the implementation of bioremediation strategies because these compounds are highly persistent in the marine environment after oil spills (Thessen and North 2017).

Crude oil also contains aromatic hydrocarbons (AHs), such as benzene, toluene, ethylbenzene, and xylene (BTEX), and polycyclic aromatic hydrocarbons (PAHs; with two or more aromatic rings), which are highly toxic to humans and animals (Ghosal et al. 2016). Bacterial aerobic degradation of these hydrocarbons involves the following two major steps: a peripheral or upper pathway, which consists of the activation (hydroxylation and dehydrogenation) of the aromatic compounds by mono- or dioxygenases, transforming them into intermediates, such as catechols (or closely related compounds), and a lower pathway through which ring-cleaving dioxygenases produce intermediates, which are incorporated into the tricarboxylic acid cycle for energy production (George and Hay 2011). Genomic analyses have revealed the molecular mechanisms used by some marine bacteria to degrade aromatic compounds. Cao et al. (2015) identified that Celeribacter indicus P73T, a strain isolated from deep-sea sediment, contains 138 genes involved in aromatic compound degradation, of which fourteen genes encode dioxygenases, including a 7,8-fluoranthene dioxygenase from the upper pathway that catalyzes the deoxygenation of a wide range of aromatic hydrocarbons, such as biphenyl, naphthalene, phenanthrene, anthracene, fluorene, and fluoranthene (Lai et al. 2014). Therefore, new metabolic pathways and PAH-degrading enzymes can be found in marine bacteria, with potential applications in enzyme technology, design of biosensors, and synthetic consortia.

Catechol dioxygenases from the lower pathway are key enzymes in aromatic hydrocarbon degradation. Based on the cleavage position of the aromatic ring, catechol dioxygenases are classified into 1,2-dioxygenases (C12DO, ortho-cleavage) and 2,3-dioxygenases (C23DO, meta-cleavage) (George and Hay 2011). The molecular and biochemical characterization of C12DOs is valuable for applications in bioremediation, environmental monitoring, and industrial processes (Guzik et al. 2013; Rodríguez-Salazar et al. 2021). Recently, we characterized C12DO from a marine P. stutzeri strain. The enzyme was active as a trimer (in contrast to other C12DOs from terrestrial Pseudomonas whose quaternary structures are dimers) and exhibited good activity in pH values from neutral to alkaline, in the presence of different ions, salinity, resistance to metal inhibitors and EDTA, rendering this enzyme a potential candidate for bioremediation applications (Rodríguez-Salazar et al. 2020). C23DO-coding genes are considered markers used to identify AH- and PAH-degrading bacteria and have been detected in different marine species from genera, such as Cycloclasticus (Hu et al. 2017), Pseudomonas (Bosch et al. 2000), Novosphingobium (Yun et al. 2014), and Celeribacter (Cao et al. 2015). Furthermore, C23DO activity can be visually detected because ring cleavage by these enzymes produces 2‐hydroxymuconic semialdehyde, which is a yellow compound. For instance, we carried out C23DO screening in several bacterial strains isolated from both seawater and sediment samples collected from the southwestern Gulf of Mexico by spraying a catechol solution on colonies grown on agar plates and identified a strain that exhibited a yellow pigment, which is indicative of C23DO activity (Millán-López 2021) (Fig. 3). The genome analysis (GenBank accession number JAHHFP000000000) revealed that the strain belonged to the species Pseudomonas chloritidismutans and contains genes that encode enzymes involved in both the upper and lower pathways of toluene degradation and the transcriptional activators XylR and XylS, which respond to the presence of toluene and benzoate, respectively (Gawin et al. 2017) (Fig. 3). Therefore, the detection of C23DO activity allows the identification of marine bacteria able to degrade aromatic hydrocarbons with potential applications in bioremediation.

Fig. 3
figure 3

Identification of aromatic hydrocarbon-degrading bacteria by the detection of catechol 2,3-dioxygenase activity. The spraying of a catechol solution (10 mM) on bacterial colonies allowed the identification of a marine bacterial strain that produces a bright yellow color due to the formation of 2-hydroxymuconate semialdehyde, compatible with catechol 2,3-dioxygenase activity. Genome analyses revealed that this strain belongs to the species Pseudomonas chloritidismutans (GOM4 strain—GenBank accession number JAHHFP000000000) and holds two gene clusters that encode enzymes belonging to both the upper and lower pathways of toluene degradation. In addition, the genes coding the transcriptional regulators XylR and XylS are present between the two operons. The XylR protein senses toluene and activates the transcription of the gene cluster that encodes enzymes of the upper pathway that convert toluene into benzoate. AlkS senses this last compound to activate the transcription of the lower pathway operon (Gawin et al. 2017)

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Biosurfactant/bioemulsifier production

Biosurfactants (BSs) and bioemulsifiers (BEs) are natural compounds with both hydrophilic and hydrophobic moieties that have surface/interface and emulsifying activity, respectively, allowing the solubilization of hydrophobic substrates and serving as ecofriendly alternatives to synthetic surfactants and emulsifiers due to their biodegradability, biocompatibility, and nontoxicity. BSs and BEs exhibit differences in chemical compositions; BSs are low molecular weight products composed of amino acids, sugars, or fatty acids linked to a functional group, such as a carboxylic acid (e.g., rhamnolipids), while BEs are a complex mixture of (lipo)polysaccharides and (lipo)proteins and have a higher molecular weight than BSs (Uzoigwe et al. 2015). Both BSs and BEs have several applications in bioremediation (crude oil and heavy metal removal), the pharmaceutical industry (antimicrobial and antitumoral activity), and cosmetic and food formulations (Tripathi et al. 2018).

Marine bacteria are a substantial source of BSs/BEs; several strains belonging to the Acinetobacter genus have been reported to produce some of these compounds (Satpute et al. 2010), including the commercial product “Emulsan,” which is a heteropolysaccharide BE synthesized by the Acinetobacter calcoaceticus RAG1 strain (a species isolated from the Mediterranean Sea) (Reisfeld et al. 1972) and used for microbial enhanced oil recovery (MEOR) (Mujumdar et al. 2019), which consists of the implementation of microorganisms (or their metabolites) to modify the conditions of the oil reservoir and physico-chemical properties of crude oil, thereby improving its extraction (Nikolova and Gutierrez 2020). Some of the most well-characterized BSs with high surface activity are rhamnolipids (RLs), which are glycolipids composed of one or two rhamnose moieties covalently linked to one or two hydroxyl fatty acids. These compounds are mainly synthesized by the Pseudomonas species and can be used for MEOR (Amani 2015) and bioremediation because RLs enhance hydrocarbon degradation (Liu et al. 2018). In P. aeruginosa, which is the best RL producer, the synthesis of RLs is carried out by three enzymes; RhlA produces fatty acid dimers, which are conjugated with dTDP-L-rhamnose by the rhamnosyltransferase RhlB to produce monorhamnolipids (mono-RLs). A second rhamnosyltransferase, RhlC, produces di-rhamnolipids (di-RLs) using mono-RLs and dTDP-L-rhamnose as substrates (Soberón-Chávez et al. 2021).

Some marine hydrocarbon-degrading Pseudomonas species with high surfactant activity have been isolated and shown to produce RLs (Chakraborty and Das 2016; Muriel-Millán et al. 2019; Twigg et al. 2018). For instance, the aromatic hydrocarbon-degrading Pseudomonas MCTG214(3b1) strain produces five RL congeners, four of which are short-chain di-RLs that reduce the surface tension of water from 60 to 30 milliNewtons per meter (mN m−1). Interestingly, P. aeruginosa rhlA and rhlB homologs were detected in the MCTG214(3b1) strain but not rhlC, suggesting the presence of a novel second rhamnosyltransferase in this species (Twigg et al. 2018). The marine P. aeruginosa GOM1 strain, which degrades medium- and long-chain alkanes, holds rhlA, rhlB, and rhlC genes and synthesizes RLs using hexadecane as a raw material, which reduce the surface tension from 73 to 23 mN m−1 (Muriel-Millán et al. 2019). Antoniou et al. (2015) reported the production of both mono-RLs and di-RLs by an Alcanivorax borkumensis strain using crude oil as a carbon source. The identification of RL-related genes in this strain will be interesting because previous genome analyses of its closest relative, the A. borkumensis SK2 strain, revealed that this species contains genes necessary for the synthesis of glucose lipids but not RLs (Antoniou et al. 2015; Schneiker et al. 2006). Tripathi et al. (2019) recently reported the first Marinobacter species able to synthesize RLs, preferably di-RL congeners (95% of total RLs), extending the bacterial genera able to produce this class of BSs.

Lipopeptide surfactants are also produced by some hydrocarbon degraders; the naphthalene-degrading Halomonas pacifica Cnaph3 strain synthesizes surfactin and pumilacidin lipopeptides, which are active in high salinity and over a wide range of temperatures (4–104 °C) and pH values (2–12). In addition, these BSs showed higher efficiency in removing hydrocarbons from contaminated soil than synthetic surfactants, such as SDS, Tween 80, and Triton X-100 (Cheffi et al. 2020). Alcanivorax dieselolei B-5 produces proline lipid BS using diesel as the sole carbon source and is stable within a broad range of temperatures and pH values and in the presence of high concentrations of NaCl, CaCl2, and MgCl2 (Qiao and Shao 2010). Given the traits of these types of BSs, they are potential candidates for application in extreme environments.

Therefore, marine bacteria are a great source of new BS/BE with potential applications in bioremediation; however, their discovery will depend on the experimental conditions used due to the synthesis of BS and BE is affected by nutrients, temperature, pH, etc. In this sense, experimental designs could be implemented to stablish the suitable conditions for discovery and production of BS/BE (Bertrand et al. 2018).

Biodegradation of synthetic plastics by marine bacteria

Plastic pollution is another current global issue due to its toxicity and high resistance to biodegradation. It is estimated that eight million metric tons of petroleum-based plastics are discharged annually into the oceans, severely affecting marine life (Jambeck et al. 2015). Plastic debris is colonized by different marine bacteria (plastisphere), including species from genera containing known hydrocarbon degraders, such as Alcanivorax, Erythrobacter, and Marinobacter (Dussud et al. 2018; Jacquin et al. 2019; Roager and Sonnenschein 2019). Some species from the plastisphere have the potential to degrade different types of plastics. For instance, an A. borkumensis strain isolated from a bacterial consortium obtained from marine plastic wastes was able to degrade 3.4% of low-density polyethylene (LDPE) after 80 days of incubation (Delacuvellerie et al. 2019). Zadjelovic et al. (2020b) isolated the strain Alcanivorax sp. 24 from marine plastic debris and exhibited some capacity to degrade polyethylene succinate (PES) and bis[2-hydroxyethyl] terephthalate, an intermediate produced from polyethylene terephthalate (PET) cleavage (Zadjelovic et al. 2020a). Two marine Pseudomonas and Arthrobacter species were isolated from polyethylene (PE) wastes, and were able to reduce the weight of high-density polyethylene (HDPE) by 12 and 15%, respectively (Balasubramanian et al. 2010). Other species isolated from marine sites not apparently contaminated with plastics have been characterized and exhibited some ability to degrade different synthetic polymers. For instance, Auta et al. (2018) reported that the strains Bacillus sp. 27 and Rhodococcus sp. 36 isolated from mangrove sediment reduced the weight of polypropylene (PP) microplastics by 4 and 6.4% after 40 days of incubation, respectively. Harshvardhan and Jha (2013) isolated the Bacillus subtilis H1584, Bacillus pumilus M27, and Kocuria palustris M16 strains from seawater, which degraded 1.75, 1.5, and 1% of LDPE films at 30 days of incubation, respectively. Other species belonging to the Cobetia, Halomonas, and Exiguobacterium genera have been isolated and exhibited some ability to partially degrade LDPE (Khandare et al. 2021). In addition, both natural and synthetic bacterial consortia have been reported to partially degrade different polymers, including PET and LDPE. The acclimation periods of these consortia in culture media supplemented with hydrocarbons or plastic substrates allowed the enrichment of plastic-degrading bacterial communities and an increase in plastic degradation (Denaro et al. 2020; Raghul et al. 2014; Syranidou et al. 2017). Despite this evidence, bacterial degradation of plastics occurs at low rates over long periods (Roager and Sonnenschein 2019). In this sense, characterization of metabolic pathways as well as of regulatory mechanisms involved in plastic degradation could contribute to optimizing the plastic-degrading capacity of known bacterial strains. In addition, it is necessary to continue exploring marine environments to identify new bacterial strains that can degrade synthetic plastic.

Plastic-degrading enzymes from marine bacteria

The biodegradation of plastic depends on both abiotic and biotic factors. Some environmental conditions, such as temperature, oxygen, and ultraviolet radiation, produce intramolecular changes in polymers (e.g., chemical transformation and bond cleavage), favoring polymer breakdown by enzymes, such as laccases, hydrolases, and cutinases (Wei and Zimmermann 2017). In the case of bacteria, several extracellular hydrolases (lipases, esterases, and proteases) active on synthetic polymers have been recently identified and characterized. A representative example of these enzymes is PET hydrolase (PETase) from the soil bacterium Idionella sakaiensis 201-F6, which is an esterase that converts PET to mono(2-hydroxyethyl) terephthalic acid (MHET) (Yoshida et al. 2016). Recent metagenomics studies have shown that marine environments have a high abundance of potential bacterial PETases, mainly at 1000 m depth in Pseudomonadales (Alam et al. 2020; Danso et al. 2018). Furthermore, Danso et al. (2018) identified an I. sakaiensis PETase homolog (49% amino acid sequence identity) in a marine uncultured bacterium that was heterologously expressed and characterized. The purified enzyme (PET2) was active on nanoparticles and films of PET and hydrolyzed para-nitrophenyl esters (pNP esters) from C2 to C12. In addition, PET2 exhibited good activity of pNP octanoate hydrolysis over a wide range of temperatures (17–90 °C) and pH values from 7 to 10 (Danso et al. 2018). By conducting in silico analyses, Almeida et al. (2019) identified the SM14est PET hydrolase in the genome of marine sponge-derived Streptomyces sp. SM14. The enzyme exhibited an identity of 41% with I. sakaiensis PETase and conserved both a serine hydrolase motif and catalytic triad to carry out ester bond hydrolysis. The authors also expressed SM14est in E. coli, which was active on polycaprolactone (PCL), a biodegradable polyester used as an indicator of the possible activity of PET hydrolysis (Almeida et al. 2019; Danso et al. 2018). Zadjelovic et al. (2020a) analyzed the proteins secreted by the marine Alcanivorax sp. 24 strain grown in the presence of synthetic (PES) and natural polyesters (polyhydroxyalkanoates) and identified the ALC24_4107 enzyme, an esterase that hydrolyzes PES and PCL.

One strategy used to increase plastic biodegradation is enhancing bacterial plastic-degrading enzyme activity. Structural studies, protein engineering, and laboratory evolution strategies have improved the activity of PETase from I. sakaiensis (Austin et al. 2018; Knott et al. 2020). In the case of marine PET-degrading enzymes, Bollinger et al. (2020) recently identified and characterized a PET hydrolase (PE-H) from the hydrocarbon-degrading strain Pseudomonas aestusnigri VGXO14T. The enzyme belongs to the IIa family of PET hydrolases and showed an identity of 47% with I. sakaiensis PETase. The recombinant enzyme hydrolyzed monomeric bis(2-hydroxyethyl) terephthalate (BHET) and amorphous PET films but not commercial PET. By site-directed mutagenesis, the authors introduced the amino acid substitution Y250S next to the histidine of the catalytic triad, resulting in a variant of PE-H that showed enhanced activity on amorphous PET and was able to hydrolyze commercial PET films (Bollinger et al. 2020). Therefore, these reports suggest that plastic-degrading enzymes seem to be commonly found in marine hydrocarbonoclastic bacteria, which incite to look for these enzymes in genomes from known and studied hydrocarbon-degrading bacterial strains. In addition, it is expected that more plastic-active enzymes from new marine bacteria will be identified and functionally characterized in the near future, expanding the repertoire of this type of molecule.

Conclusions and perspectives

Oceans are vast and contain an almost limitless diversity of bacterial species, many of which play important functions in the regulation of the Earth system. In addition, some bacteria may be implemented as a part of the strategies to address current global problems, such as environmental pollution. Several marine bacterial strains with specialized alkane- and PAH-degrading metabolic pathways and other strains with the capacity to partially degrade synthetic plastics (e.g. PET and PE) have been characterized. However, more research is needed to optimize these bioremediation technologies. In this sense, protein engineering provides promising strategies (e.g., direct evolution and rational mutagenesis) to enhance the catalytic activity of marine bacterial PETases. On the other hand, some synthetic biology approaches, such as genome editing and metabolic reconstruction (Jaiswal and Shukla 2020), may be applied to optimize hydrocarbon-degradation pathways of several marine bacterial strains, and to design synthetic consortia with efficient marine hydrocarbon degraders under stressing conditions such as Alcanivorax, Pseudomonas, and Halomonas species. Evaluation of these enhanced technologies by mesocosm experiments will be valuable to better approximate their real activity in open environments (e.g., seas and oceans) (Rodríguez-Salazar et al. 2021). (Meta)genome mining to search for biosynthetic gene clusters and their subsequent functional characterization is a good strategy to increase the number of newly identified BSs and BEs from marine bacteria. In conclusion, marine bacteria will continue to provide a myriad of potential biotechnological tools with applications in diverse fields, and their discovery and characterization will be successfully accomplished by multidisciplinary approaches that integrate culture methods, biochemical analyses, omics technologies, and bioinformatics tools.