Abstract
High toxicity, bioaccumulation factor and widespread dispersal of persistent organic pollutants (POPs) cause environmental and human health hazards. The combined use of plants and bacteria is a promising approach for the remediation of soil and water contaminated with POPs. Plants provide residency and nutrients to their associated rhizosphere and endophytic bacteria. In return, the bacteria support plant growth by the degradation and detoxification of POPs. Moreover, they improve plant growth and health due to their innate plant growth-promoting mechanisms. This review provides a critical view of factors that affect absorption and translocation of POPs in plants and the limitations that plant have to deal with during the remediation of POPs. Moreover, the synergistic effects of plant–bacteria interactions in the phytoremediation of organic pollutants with special reference to POPs are discussed.
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
After World War II, economic boost due to advances in science and technology has resulted in the use of a wide range of synthetic chemicals and thus, in an exponential increase in their production. Although these chemicals proved to be beneficial in agricultural and industrial processes, several studies reported their harmful effects on living organisms and the environment. Among these chemicals, POPs are of increasing concern due to their persistent behavior and high toxicity in natural settings. POPs are defined as “intentionally or unintentionally produced lipophilic chemicals capable of accumulating in the environment and are resistant to photochemical degradation with long-range dispersal potential” (Sharma et al. 2014a). POPs are categorized into three major groups on the basis of their origin and use: organochlorine pesticides (OCPs), industrial chemicals (ICs), and unintended by-products (UIBPs) (UNEP 2003) (Table 1).
The first report of harmful effects of POPs was the publication of Carson and Darling “Silent Spring” (Carson and Darling 1962). They traces the impact of DDT as it is absorbed by creature after creature in the food chain, until eventually birds’ eggs are unable to hatch, because their shells have become so brittle that they break when the birds sit on them. As a result of this report, DDT was banned in 1973 (Staniforth 2013). In later years, mass-poisoning episodes by diseases, Yusho and Yu-Cheng, in Japan and Taiwan, respectively, strengthened the discouragement of the release of POPs in the environment (Bradberry et al. 2014). Considering the aspects of human and environmental health deterioration, the Stockholm Convention of POPs was organized by the United Nations Environment Program (UNEP) in 2001. The convention was signed to regulate and ban the use of a preliminary list of 12 chemicals—collectively referred to as the dirty dozen—that showed high persistence, bioaccumulation in fatty tissues, and toxicity (Johansen 2003; Xu et al. 2013) (Table 1). The dirty dozen included aldrin, dieldrin, DDT, chlordane, mirex, endrin, heptachlor, toxaphene, hexachlorobenzene (HCB), polychlorinated biphenyls (PCBs), dibenzodioxins, and dibenzofurans. In the following years, 11 more chemicals (Table 1) were added to the list due to their persistence and toxicity (Haffner and Schecter 2014). Although many of the developed countries have banned the production of most of the POPs, their use is still a common practice in most of the developing countries (Sharma et al. 2014b).
Phytoremediation is a promising approach for the remediation of soil and water contaminated with organic and inorganic pollutants (Khan et al. 2014; McCutcheon and Schnoor 2004; Schwitzguébel and Schröder 2009). However, the presence of organic pollutants including POPs in soil and water decreases plant growth and phytoremediation efficacy (Gerhardt et al. 2009; Ibáñez et al. 2012; Mench et al. 2009; Saleh et al. 2004). Moreover, plants have certain limits with respect to their capabilities to remove organic pollutants from the environment (Carvalho et al. 2014; Chaudhry et al. 2005; Khoudi et al. 2013). The combined use of plants and bacteria has been recently proposed to enhance the efficiency of remediation of soil contaminated with organic pollutants including POPs (Becerra-Castro et al. 2013; Glick 2010; Haslmayr et al. 2014; Weyens et al. 2009a). Rhizobacteria colonize the roots, whereas endophytic bacteria reside inside the plant tissues (Compant et al. 2010). Plants provide the space and nutrients to the bacteria. In return, rhizosphere and endophytic bacteria improve the bioavailability and allow to mineralization of organic pollutants. The bacteria also improve plant growth due to their plant growth-promoting activities such as siderophore and 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase production and nitrogen fixation. Moreover, the bacteria reduce the toxicity and evapotranspiration of the pollutants in the environment (Afzal et al. 2014a; Khan et al. 2013a; Shehzadi et al. 2015; Vangronsveld et al. 2009; Weyens et al. 2009b; Yousaf et al. 2014).
This review is structured to discuss the occurrence, fate, and degradation of POPs by plant and plant–bacteria synergism. Moreover, the role of rhizosphere and endophytic bacteria to accelerate the phytoremediation of POPs is emphasized.
POPs in the environment
POPs are carbon-based compounds that show resistance to degradation under natural conditions and thus stay in the environment for long periods of time (Weber et al. 2011). The fundamental reason behind their stability is the presence of carbon–chlorine bond that resist against hydrolysis (El-Shahawi et al. 2010). The stability is further increased by increasing the number of chlorine atoms in the compound. Therefore, the compounds with higher halogenation are more resistant to degradation as compared to the compounds with lower halogenation (Wikoff et al. 2012).
In addition to stability, the semivolatile and insoluble nature of POPs allow their long distance dispersal and worldwide distribution (Wang 2012). They have been found in the areas where they were never used, e.g., the Arctic of Alaska. This unexpected occurrence is because of the transportation of many of the POPs from the USA and Canada to Alaska, where they sank and settled in the ice sheets without being degraded (Braune et al. 2005; Newton et al. 2014). In general, POPs tend to evaporate in hot places and then condense back in colder regions (Nurzhanova et al. 2013; Qiu 2013).
Due to high stability and long-range transportation characteristics, POPs find their ways from water and air into the soil ecosystem where they are taken up by plants and living organisms (Hao et al. 2014; McLeod et al. 2014; Morris et al. 2014). They follow the usual process of bioaccumulation and biomagnification as they move up in each trophic level of the food chain. The first report on the bioaccumulation of POPs in biotic elements was put forward in 1970 when polar bears were found to have pesticides in their fat tissues (Lie et al. 2003). Later on, many studies highlighted the trans-boundary nature of POPs along with their deteriorating effects on wildlife and human health (Bowes and Jonkel 1975; El-Shahawi et al. 2010; Li and Macdonald 2005; Muir et al. 1988; Norstrom and Muir 1994; Voldner and Li 1995). Although most of the studies were related to arctic region, these findings reduced the release of these chemicals in natural environments.
Humans along with other tertiary carnivores reside at the top of the food chain and, thereby, are at high risk of exposure to POPs as compared to the organisms at lower trophic levels (Lee et al. 2014a; Wang et al. 2014). Human exposure to POPs begins prenatally as many of them possess ability to cross the placenta. Soon after birth, exposure occurs through breastfeeding and later by ingestion, inhalation, and dermal contact (Man et al. 2014; Vafeiadi et al. 2014). Once they are within the body, POPs are taken up by adipocytes due to their lipophilic nature where they finally become a part of the adipose tissues and liver (Dewailly et al. 1999; Lee et al. 2014b). Their continuous accumulation can lead to metabolic disorders triggering cardiovascular diseases and physical health illness including larger body burdens. Usually, the accumulated POPs are slowly released into the blood stream. However, during the period of large mobilization of adipose tissue, such as pregnancy, weight loss, and breastfeeding, they are released at a faster rate and cause severe damages to fetuses or infants (La Merrill et al. 2012). Therefore, the remediation of POPs-contaminated soil and water is one of the key topics in the field of environment science and engineering (Abhilash et al. 2013; Agyekum et al. 2014; Becerra-Castro et al. 2013; Chhikara et al. 2010; Florence et al. 2015).
Phytoremediation of POPs
Phytoremediation is an eco-friendly technology that utilizes plants, to transform, translocate, sequester, extract, and/or detoxify the pollutants present in sediments, soil, groundwater, surface water, and even in the atmosphere (Chigbo and Batty 2014; Samardjieva et al. 2015; Susarla et al. 2002) and thus remediate or restore the contaminated sites. Plants may take up POPs from the environment and translocate in their different tissues (Ahmad et al. 2012; Chhikara et al. 2010; Germaine et al. 2009). The uptake of POPs in plants depends on a number of physicochemical characteristics of these compounds (Admire et al. 2014; Campanella et al. 2002; Zhan et al. 2015). These physicochemical characteristics are octanol–water partition coefficient (log K ow), acidity constant (pK a), aqueous solubility (Sw), octanol solubility (So), and the concentration of the pollutant (Admire et al. 2014; Alkorta and Garbisu 2001; Zeng et al. 2012). Among all these characteristics, the role of log K ow value is of significant concern due to its direct involvement in determining how hydrophobic or lipophilic the compound is. Usually, the compounds having lower log K ow values (0.5–3.0) are easily taken up by plants as compared to those having higher log K ow values. In the case of POPs, log K ow value of most of the compounds range between 3.0 and 8.3, making them resilient for phytouptake (Takaki et al. 2014; White and Zeeb 2007) (Table 2). Consequently, POPs bind to lipid membranes of plant roots (Chaudhry et al. 2002; White and Zeeb 2007).
In addition to log K ow value, the uptake and translocation of POPs in plants depend upon POP and plant type (Gleba et al. 1999; Mitton et al. 2014; Pilon-Smits 2005). POPs, like aldrin, dieldrin, heptachlor, chlordane, lindane, DDT, etc., have been found to be taken up at different rate by different plants irrespective of their high log K ow values (Agyekum et al. 2014; Calabrese and Blain 2009; Mattina et al. 2000). Moreover, plant physiology and transpiration rate affect the uptake of POPs in plants. For example, lichens accumulated higher levels of POPs than pine needles (Ockenden et al. 1998). Similarly, zucchini and pumpkin accumulated high concentration of DDT than tall fescue, alfalfa, and rye grass (Lunney et al. 2004). In conditions where uptake of POPs is not feasible, the main route of POP uptake could be the direct absorption by plant roots, volatilization from soil and absorption by leaves, and particle-facilitated transportation along with deposition on aerial parts (Ficko et al. 2010; Ockenden et al. 1998; Smith and Jones 2000; Whitfield Åslund et al. 2007).
Although POPs could enter plants through roots and leaves (Wang and Liu 2007), these are mainly taken up by roots and translocated to the aboveground parts (Lunney et al. 2004; Mo et al. 2008). As POPs are manmade chemicals, specific transporter proteins for their transportation are absent in plants; hence, their uptake by roots occurs via simple diffusion through the cell wall from where they enter the xylem stream (Campos et al. 2008). Different plant species can absorb different POPs at different extents (Burken et al. 2005; Mikes et al. 2009; Nash and Beall 1970). The detailed description of different plants and their abilities to absorb and/or translocate different POPs has been presented in Table 3.
After uptake and translocation, to avoid the toxicity associated with absorbed pollutants, plants usually follow one of the two procedures, evapotranspiration and/or phytodegradation. For most of the pollutants, evapotranspiration is the major mechanism in which plants release the pollutants in the atmosphere through their leaves. During the course of evolution, plants were not under selection pressure and hence have not adopted pathways for mineralization of organic pollutants (Burken 2003; Gerhardt et al. 2009). Regarding phytodegradation, partial degradation of pollutants within plants takes place through in planta detoxification mechanisms, i.e., transformation (phase 1), conjugation (phase 2), and compartmentalization (phase 3) (Fig. 1).
Up take and degradation of organic pollutants within the plant tissues
This mechanism is generally termed as green-liver model (Sandermann 1992, 1994). Phytodegradation of POPs takes place by the virtue of oxidation reactions, hydrolysis, and epoxide formation (Chaudhry et al. 2002). Among these, oxidation is more prevalent and takes place by the action of different plant-derived microsomal enzymes such as cytochromes P450, peroxidases, and flavin-dependent monooxygenases (Durst and Benveniste 1993; Khandare et al. 2012; Naumann et al. 2002). These plant-derived microsomal enzymes are capable of degrading numerous POPs due to their reactive nature. For example, cytochrome P450 can act on organophosphate (P=S → P=O) insecticides with the release of atomic sulfur (Neal 1980). This mechanism of desulfuration has been observed as a cytochrome P450-catalyzed reaction in maize and sorghum during the degradation of methidathion, malathion, diazinon, and isozafos (Moreland et al. 1993, 1995). Furthermore, the cytochrome P450 system is reported to be involved in the metabolism of different PCB congeners and carbamate compounds (Chaudhry et al. 2002; Lee and Fletcher 1992).
To improve the overall potential of plant-based phytoremediation, the combined use of plants and bacteria has been recently proposed which can significantly enhance the degradation of organic pollutants including POPs in planta as well as ex planta (Afzal et al. 2014b; Glick 2010; Khan et al. 2013a; Mitter et al. 2013). The following sections elucidate the importance of plant-bacteria partnerships for the remediation of POPs-contaminated environment.
Plant–bacteria partnership for the remediation of POPs
In plant–bacteria partnerships, POPs could be degraded by plant-associated bacteria, mainly rhizobacteria (Afzal et al. 2014a; Glick 2010; Mackova et al. 2009; Weyens et al. 2009a). In this association, bacteria possessing catabolic genes survive and proliferate in the close vicinity of roots and in some cases in the internal tissues of host plant without causing pathogenicity (Naveed et al. 2014; Sessitsch et al. 2005). Plants provide optimum conditions to these microorganisms to proliferate by offering nutrients and residency while allowing them to feed upon pollutants in the rhizosphere as well as in the endosphere. Therefore, the combined use of plants and the associated bacteria (pollutant-degrading and/or plant growth-promoting) strengthens the role of each partner. In this sense, bacteria help host plant to overcome contaminant-induced stress responses and develop high shoot and root biomass, which ultimately enhances microbial population and the degradation of organic pollutants including POPs (Weyens et al. 2009a). Furthermore, it is well established that, in this partnership, the rate of pollutant degradation is higher than the individual contribution of each partner in remediation processes (Khan et al. 2013b; Lunney et al. 2004).
The interactions between plants and bacteria having catabolic genes have led to the evolution of a diverse variety of catabolic enzymes that can metabolize and detoxify the xenobiotics (Hong et al. 2015; Singer et al. 2003; Xun et al. 2015). These synergistic relationships between plants and plant-associated bacterial communities in rhizosphere and/or endosphere have been widely investigated (Compant et al. 2010; Fahad et al. 2015; Khan et al. 2013a). Recently, the combined use of plants and bacteria has been exploited to enhance the phytoremediation of soil and water contaminated with different organic pollutants (Afzal et al. 2014b; Arslan et al. 2014; Khan et al. 2013b; Shehzadi et al. 2014). Similarly, several studies were performed to explore the potential of plant–bacteria partnership for the remediation of POPs-contaminated soil and water (Aken et al. 2009; Becerra-Castro et al. 2013; Jha and Jha 2015; Jha et al. 2014). Both rhizosphere and endophytic bacteria can enhance plant growth and POP degradation.
Plant–rhizobacteria partnerships
Although rhizobacteria have previously been studied for their plant growth-promoting mechanisms, they have recently gained attention for improving the efficiency of phytoremediation of contaminated soil and water (Glick 2010; Gurska et al. 2009; Khan et al. 2013a). Rhizobacteria capable of degrading different POPs have been isolated from rhizospheric soil of different plants and well-studied for POP degradation pathways and genes involved in POP degradation have been identified (Brazil et al. 2005; Fatima et al. 2015; Nicoară et al. 2014). Although these bacteria showed high potential to degrade different POPs, these are unable to survive and proliferate in the contaminated soils (Pandey et al. 2009). Therefore, effective mineralization and degradation of the pollutants can be achieved by employing rhizobacteria in association with plants. In such a relationship, rhizobacteria having catabolic genes feed upon the organic pollutants as a sole carbon source for their cell functioning and metabolism, whereas plants facilitate the survival of rhizobacteria by adjusting the rhizosphere environment through production of root exudates, rhizosphere oxidation, co-metabolite induction, H+/OH− ion excretion, organic acid production, and release of biogenic surfactants (Fig. 2) (Afzal et al. 2013a; Hinsinger et al. 2003; Khan et al. 2013a).
Plant–rhizobacteria partnership and mineralization of POPs
The plant–rhizobacteria interactions enhance the abundance and expression of catabolic genes in the rhizosphere, leading to an increase in mineralization, degradation, stabilization, and/or sequestration of variety of organic compounds including POPs (Jha and Jha 2015; Passatore et al. 2014; Sprocati et al. 2014; Yateem 2013). In addition to this, rhizobacteria possessing plant growth-promoting activities improve plant health and biomass production. Improved plant growth facilitates the colonization of rhizobacteria in rhizoplane leading an increase of the organic pollutants degradation (Afzal et al. 2013b; Compant et al. 2010; Khan et al. 2013a; Yousaf et al. 2010). Importantly, during degradation of recalcitrant compounds, most of the pollutants cannot be used as carbon and energy sources for rhizobacteria; therefore, their degradation is often facilitated by co-metabolism of a similar but harmless structural analog that is a secondary metabolite of the host plant. The structural analogs act as inducers and enhance the bacterial population which then could degrade the organic pollutant (Singer et al. 2003; Bedard et al. 1986). Plant terpenes, flavonoids, and salicylic acid have also been found to act as inducer and enhance the degradation of different POPs (Gilbert and Crowley 1997, 1998; Hernandez et al. 1997; Koh et al. 2000; Master and Mohn 2001; Singer et al. 2000; Tandlich et al. 2001).
Recently, several studies have been conducted to explore the potential of plant–rhizobacteria partnerships for the remediation of POPs-contaminated soil and water (Abhilash et al. 2013; Gerhardt et al. 2009; Jha and Jha 2015; Qin et al. 2014). Among POPs, PCBs that released into the environment as a consequence of their use as hydraulic fluids, plasticizers, adhesives, flame retardants, etc. are well-studied pollutants. They have been reported to be successfully degraded by the combined use of plants and rhizobacteria (Leigh et al. 2002). The partnerships of alfalfa with Pseudomonas fluorescens sp. strain F113 and Arabidopsis with Pseudomonas putida strain Flav1-1 enhanced the degradation of a variety of PCBs (Villacieros et al. 2005; Narasimhan et al. 2003). Similarly, enhanced biotransformation of a number of aroclor compounds (e.g., 1242, 1248, 1254, and 1260) by alfalfa inoculated with a symbiotic N2-fixing rhizobacterium, Sinorhizobium meliloti strain A-025, has been reported (Mehmannavaz et al. 2002). Many other studies also reported the enhanced degradation of POPs by plant–rhizobacteria partnerships as shown in Table 4.
Many chemicals in the root exudates of plants stimulate rhizospheric microbes to perform degradation of xenobiotic pollutants including POPs (Donnelly et al. 1994; Isidorov and Jdanova 2002). Degradation of POPs is attributable to the chemical composition of root exudates as well as the rate of exudation, which facilitates pollutant-degrading rhizobacteria enormously in the rhizosphere (Rao 1990; Salt et al. 1998). More importantly, these factors tend to vary from one plant to another as most of the plant species contain phenols in their exudates, which support the proliferation of POPs-degrading rhizobacteria (Fletcher and Hegde 1995; Salt et al. 1998). Similarly as in the case of PCBs, a common component of root exudates, salicylate, is reported to elevate the expression of bphA gene encoding biphenyl dioxygenase in Pseudomonas sp. Cam-1, while inhibition of the same gene occurs by the presence of terpenes in root exudates (Master and Mohn 2001).
Another factor that governs the removal of POPs from the contaminated environment is the bioavailability of the pollutant (Federici et al. 2012). A number of mobilizing agents such as plant oils, synthetic surfactants and biogenic surfactants have been applied to enhance the bioavailability of POPs in the soil (Berselli et al. 2004; Fava and Ciccotosto 2002; Fava and Gioia 1998, 2001; Federici et al. 2012). A rhizobacteria having potential to produce biosurfactants can enhance the bioavaiability of POPs and ultimately their degradation (Aslund and Zeeb 2010). Biosurfactants make POP-H2O soluble aggregates which ultimately release the pollutant from soil particles. However, the release of surfactants in the root exudates seems more promising as it may provide easy solubilization of POPs in plant rhizosphere (Passatore et al. 2014). These studies reveal that the combined use plants and biosurfactant-producing bacteria can improve the bioavailability of organic pollutants through biosurfactant exudation and/or production and consequently the remediation of POPs-contaminated environment. Recently, rhizoengineering has gained attention to enhance the removal of POPs from the environment (Thijs and Vangronsveld 2015). In rhizoengineering, the aim is to favor the population of rhizobacteria by adopting many possible strategies including nutrient adjustments, flavonoid regulations, and facilitating degradation by the inoculation of transgenic strains (Fu et al. 2012). Many POPs, especially PCBs, have been reported to be successfully remediated by the adjustment of flavonoids, apigenin, and naringenin (Narasimhan et al. 2003).
Plant–endophyte partnership
Plant–endophyte partnership is a promising approach for the remediation of a wide range of xenobiotics (Afzal et al. 2014a; Glick 2010; Weyens et al. 2009b). In plant–endophyte partnership, plants provide nutrients and residency to endophytic bacteria whereas endophytic bacteria protect plants from the toxic effects of the pollutants taken up by the plants (Afzal et al. 2014a; Rylott 2014). Endophytic bacteria degrade the pollutants in the rhizosphere as well as in the endosphere and contribute significantly in pollutant degradation (Afzal et al. 2011; Compant et al. 2010; Yousaf et al. 2011). Furthermore, endophytic bacteria were found to have significant effects on plant growth and development in the contaminated soil and water, especially due to their plant growth-promoting activities (Afzal et al. 2012; Ryan et al. 2008; Shehzadi et al. 2014). Usually, endophytic bacteria can be found in plant endosphere, mainly root cortex and/or xylem, and are involved in the mineralization of pollutants as shown in Fig. 3 (Schulz and Boyle 2006; Sessitsch et al. 2005; Weyens et al. 2009b). Due to beneficial effects of endophytic bacteria, their innate immune system facilitates the colonization of the bacteria in root and shoot (Moore et al. 2006).
Plant–endophyte partnerships for the remediation of POPs
Recently, plant–endophyte partnership has gained popularity compared to other mechanisms of remediation (Afzal et al. 2014a; Weyens et al. 2009b; Zhu et al. 2014). Plant–endophyte partnership has advantages over plant–rhizobacteria partnership during the remediation of organic pollutants which are easily taken up by plants (Weyens et al. 2009c; Afzal et al. 2014a). In such circumstances, although rhizoremediation seems possible, the pollutant is not available to the rhizospheric microfloradue to its lower residency time in rhizosphere and optimum lipophilicity. Consequently, endophytic communities get the opportunity to degrade the contaminants by the action of intracellular dioxygenases before the contaminants are evapotranspired (Trapp et al. 2000; Weyens et al. 2009b). Furthermore, a major advantage of endophytic bacteria over free-living rhizobacteria is that they reside in internal tissues of the host plant and hence have less competition for nutrients and space, whereas rhizobacterial population have more competition by a large numbers of soil microorganisms which often results in reduction of the desired species (Doty 2008).
The first laboratory study on the degradation of POPs using plant–endophyte partnership was conducted by Germaine and coworkers (2006), who applied endophytic bacterium, Pseudomonas putida VM1450, to pea plant for the degradation of 2,4-dichlorophenoxyacetic acid (2,4-D). The strain was able to colonize plant endosphere resulting in significant degradation of 2,4-D in plant tissues. Furthermore, a naphthalene-degrading endophytic bacterial strain, Pseudomonas putida VM1441, has been reported to efficiently colonized root and shoot interior of the host plant and enhanced plant growth and naphthalene degradation (Germaine et al. 2009). In later years, several endophytic bacteria having POPs-degrading catabolic genes and having potential to degrade POPs were isolated and characterized (Andria et al. 2009; Wang et al. 2014; Weyens et al. 2010a; Yousaf et al. 2011). Recently, the combined use of plants and endophytic bacteria has been found to remediate hexachlorocyclohexane (HCH) (Becerra-Castro et al. 2013). Two endophytic bacteria, Rhodococcus erythropolis ET54b and Sphingomonas sp. D4, were inoculated to Cytisuss triatus vegetated in HCH-contaminated soil. Bacterial inoculation improved plant growth and HCH degradation both in the rhizosphere and endosphere. Examples of successful degradation of a number of POPs by the application of endophytic bacteria in association with different plants are listed in Table 5.
Abovementioned studies reveal that both rhizospheric and endophytic bacteria have potential to facilitate and enhance the degradation of POPs. Until now, relatively less number of endophytes with POP degradation abilities have been isolated as compared to rhizobacteria. Therefore, further studies are needed to explore the ecology of POPs degrading endophytic bacteria.
Conclusions
The combined use of plants and POPs-degrading rhizosphere and/or endophytic bacteria provides an effective approach for the remediation of POPs-contaminated sites. In bacterial-assisted phytoremediation of POPs, rhizobacteria and endophytic bacteria that possess appropriate genes for the degradation, transformation, and mineralization of pollutants allow to alleviate toxicity to the plant or their direct phytovolatilization. Although many POPs, especially PCBs, have been remediated from a wide range of ecosystems through bacterial-assisted phytoremediation, this endeavor still faces numerous challenges. A better understanding of improving bioavailability of POPs by bacteria, the mechanisms by which these POPs are tolerated by certain plants or bacterial species, and how relevant traits like the survival of the inoculated bacteria in POPs environments as well as maximum detoxification by the use of combinations of different POPs-degrading bacteria will provide a broader and more efficient application of phytoremediation of POPs-contaminated environment. Moreover, the knowledge about metabolic activities of the bacteria and their diversity by using metagenomic techniques can further help us to design more sustainable bacterial assisted phytoremediation strategies.
References
Abhilash PC, Singh B, Srivastava P, Schaeffer A, Singh N (2013) Remediation of lindane by Jatropha curcas L: utilization of multipurpose species for rhizoremediation. Biomass Bioenergy 51:189–193
Admire B, Lian B, Yalkowsky SH (2014) Estimating the physicochemical properties of polyhalogenated aromatic and aliphatic compounds using UPPER: Part 2. Aqueous solubility, octanol solubility and octanol–water partition coefficient. Chemosphere 119:1441–1446
Afzal M, Khan QM, Sessitsch A (2014a) Endophytic bacteria: prospects and applications for the phytoremediation of organic pollutants. Chemosphere 117:232–242
Afzal M, Khan S, Iqbal S, Mirza MS, Khan QM (2013a) Inoculation method affects colonization and activity of Burkholderia phytofirmans PsJN during phytoremediation of diesel-contaminated soil. Int Biodeterior Biodegrad 85:331–336
Afzal M, Shabir G, Tahseen R, Ejazul I, Iqbal S, Khan QM, Khalid ZM (2014b) Endophytic Burkholderia sp. strain PsJN improves plant growth and phytoremediation of soil irrigated with textile effluent. Clean Soil Air Water 42:1304–1310
Afzal M, Yousaf S, Reichenauer TG, Kuffner M, Sessitsch A (2011) Soil type affects plant colonization, activity and catabolic gene expression of inoculated bacterial strains during phytoremediation of diesel. J Hazard Mater 186:1568–1575
Afzal M, Yousaf S, Reichenauer TG, Sessitsch A (2012) The inoculation method affects colonization and performance of bacterial inoculant strains in the phytoremediation of soil contaminated with diesel oil. Int J Phytorem 14:35–47
Afzal M, Yousaf S, Reichenauer TG, Sessitsch A (2013b) Ecology of alkane-degrading bacteria and their interaction with the plant. In: Bruijn FJD (ed) Molecular microbial ecology of the rhizosphere. John Wiley & Sons. Hoboken, NJ, USA, pp 975–89
Agyekum AA, Ayernor GS, Saalia FK, Bediako-Amoa B (2014) Translocation of pesticide residues in tomato, mango and pineapple fruits. Compr Res J Agric Sci 2:40–45
Ahmad F, Iqbal S, Anwar S, Afzal M, Islam E, Mustafa T, Khan QM (2012) Enhanced remediation of chlorpyrifos from soil using ryegrass (Lollium multiflorum) and chlorpyrifos-degrading bacterium Bacillus pumilus C2A1. J Hazard Mater 237-238:110–115
Aken BV, Correa PA, Schnoor JL (2009) Phytoremediation of polychlorinated biphenyls: New trends and promises. Environ Sci Technol 44:2767–2776
Alkorta I, Garbisu C (2001) Phytoremediation of organic contaminants in soils. Bioresour Technol 79:273–276
Andria V, Reichenauer TG, Sessitsch A (2009) Expression of alkane monooxygenase (alkB) genes by plant-associated bacteria in the rhizosphere and endosphere of Italian ryegrass (Lolium multiflorum L.) grown in diesel contaminated soil. Environ Pollut 157:3347–3350
Arslan M, Afzal M, Amin I, Iqbal S, Khan QM (2014) Nutrients can enhance the abundance and expression of alkane hydroxylase CYP153 gene in the rhizosphere of ryegrass planted in hydrocarbon-polluted soil. PLoS ONE 9:e111208
Aslund MW, Zeeb BA (2010) A review of recent research developments into the potential for phytoextraction of persistent organic pollutants (Pops) from weathered, contaminated soil. In: Kulakow P, Pidlisnyuk V (eds) Application of phytotechnologies for cleanup of industrial, agricultural, and wastewater contamination. NATO Science for Peace and Security Series C: Environmental Security. Springer, Netherlands, pp 35–59
Becerra-Castro C, Prieto-Fernández Á, Kidd PS, Weyens N, Rodríguez-Garrido B, Touceda-González M, Acea MJ, Vangronsveld J (2013) Improving performance of Cytisus striatus on substrates contaminated with hexachlorocyclohexane (HCH) isomers using bacterial inoculants: Developing a phytoremediation strategy. Plant Soil 362:247–260
Bedard DL, Unterman R, Bopp LH, Brennan MJ, Haberl ML, Johnson C (1986) Rapid assay for screening and characterizing microorganisms for the ability to degrade polychlorinated biphenyls. Appl Environ Microbiol 51:761–768
Berselli S, Milone G, Canepa P, Di Gioia D, Fava F (2004) Effects of cyclodextrins, humic substances, and rhamnolipids on the washing of a historically contaminated soil and on the aerobic bioremediation of the resulting effluents. Biotechnol Bioeng 88:111–120
Böltner D, Godoy P, Muñoz-Rojas J, Duque E, Moreno-Morillas S, Sánchez L, Ramos JL (2008) Rhizoremediation of lindane by root-colonizing Sphingomonas. Microb Biotechnol 1:87–93
Bowes GW, Jonkel CJ (1975) Presence and distribution of polychlorinated biphenyls (PCBs) in arctic and subarctic marine food chains. J Fish Res Board Can 32:2111–2123
Bradberry SM, Vale PA, Jefferson RD, Buckley N, Bateman DN, Thanacoody HR, Wood D (2014) Common chemical poisonings. Oxford Desk Reference: Toxicology, 205
Braune BM, Outridge PM, Fisk AT, Muir DCG, Helm PA, Hobbs K, Hoekstra PF, Kuzyk ZA, Kwan M, Letcher RJ, Lockhart WL, Norstrom RJ, Stern GA, Stirling I (2005) Persistent organic pollutants and mercury in marine biota of the Canadian Arctic: an overview of spatial and temporal trends. Sci Total Environ 351–352:4–56
Brazil GM, Kenefick L, Callanan M, Haro A, De Lorenzo V, Dowling DN, O’Gara F (1995) Construction of a rhizosphere pseudomonad with potential to degrade polychlorinated biphenyls and detection of bph gene expression in the rhizosphere. Appl Environ Microb 61:1946–1952
Brazil GM, Kenefick L, Callanan M, Haro A, de Lorenzo V, Dowling DN, O’Gara F (2005) Construction of a rhizosphere pseudomonad with potential to degrade polychlorinated biphenyls and detection of bph gene expression in the rhizosphere. Appl Environ Microbiol 61:1946–52
Burken J (2003) Uptake and metabolism of organic compounds. In: Mccutcheon S, Schnoor JL, Smith J (eds) Green-liver model, in phytoremediation: transformation and control of contaminants. Wiley, New York, pp 59–84
Burken JG, Ma X, Struckhoff GC, Gilbertson AW (2005) Volatile organic compound fate in phytoremediation applications: Natural and engineered systems. Z Naturforsch 60:208–215
Cabidoche YM, Achard R, Cattan P, Clermont-Dauphin C, Massat F, Sansoulet J (2009) Long-term pollution by chlordecone of tropical volcanic soils in the French West Indies: a simple leaching model accounts for current residue. Environ Pollut 157:1697–1705
Calabrese EJ, Blain RB (2009) Hormesis and plant biology. Environ Pollut 157:42–48
Campanella BF, Bock C, Schröder P (2002) Phytoremediation to increase the degradation of PCBs and PCDD/Fs. Environ Sci Pollut Res 9:73–85
Campos V, Merino I, Casado R, Gómez L (2008) Phytoremediation of organic pollutants. Span J Agric Res 6:38–47
Carson R, Darling L (1962) Silent Spring. Riverside Press, Boston, Houghton Mifflin, Cambridge, MA, pp 20–27
Carvalho P, Basto MC, Almeida CM, Brix H (2014) A review of plant–pharmaceutical interactions: from uptake and effects in crop plants to phytoremediation in constructed wetlands. Environ Sci Pollut Res 21:11729–11763
Chaudhry Q, Schröder P, Werck-Reichhart D, Grajek W, Marecik R (2002) Prospects and limitations of phytoremediation for the removal of persistent pesticides in the environment. Environ Sci Pollut Res 9:4–17
Chaudhry Q, Blom-Zandstra M, Gupta S, Joner EJ (2005) Utilising the synergy between plants and rhizosphere microorganisms to enhance breakdown of organic pollutants in the environment. Environ Sci Pollut Res 12:34–48
Chekol T, Vough LR, Chaney RL (2004) Phytoremediation of polychlorinated biphenyl-contaminated soils: The rhizosphere effect. Environ Int 30:799–804
Chhikara S, Paulose B, White JC, Dhankher OP (2010) Understanding the physiological and molecular mechanism of persistent organic pollutant uptake and detoxification in cucurbit species (Zucchini and Squash). Environ Sci Technol 44:7295–7301
Chigbo C, Batty L (2014) Phytoremediation for co-contaminated soils of chromium and benzo[a]pyrene using Zea mays L. Environ Sci Pollut Res 21:3051–3059
Chu WK, Wong MH, Zhang J (2006) Accumulation, distribution and transformation of DDT and PCBs by Phragmites australis and Oryza sativa L. Whole plant study. Environ Geochem Health 28:159–168
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo-and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678
Dams RI, Paton GI, Killham K (2007) Rhizoremediation of pentachlorophenol by Sphingobium chlorophenolicum ATCC 39723. Chemosphere 68:864–870
DeLorenzo ME, Taylor LA, Lund SA, Pennington PL, Strozier ED, Fulton MH (2002) Toxicity and bioconcentration potential of the agricultural pesticide endosulfan in phytoplankton and zooplankton. Arch Environ Contam Toxicol 42:173–181
Dewailly É, Mulvad G, Pedersen HS, Ayotte P, Demers A, Weber J-P, Hansen JC (1999) Concentration of organochlorines in human brain, liver, and adipose tissue autopsy samples from Greenland. Environ Health Perspect 107:823–828
Donnelly PK, Hegde RS, Fletcher JS (1994) Growth of PCB-degrading bacteria on compounds from photosynthetic plants. Chemosphere 28:981–988
Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179:318–333
Durst F, Benveniste I (1993) Cytochrome P450 in plants. In: Schenkman J, Greim H (eds) Cytochrome P450. Handbook of experimental pharmacology. Springer, Berlin Heidelberg, pp 293–310
El-Shahawi MS, Hamza A, Bashammakh AS, Al-Saggaf WT (2010) An overview on the accumulation, distribution, transformations, toxicity and analytical methods for the monitoring of persistent organic pollutants. Talanta 80:1587–1597
Fahad S, Hussain S, Bano A, Saud S, Hassan S, Shan D, Khan F, Khan F, Chen Y, Wu C, Tabassum M, Chun M, Afzal M, Jan A, Jan M, Huang J (2015) Potential role of phytohormones and plant growth-promoting rhizobacteria in abiotic stresses: consequences for changing environment. Environ Sci Pollut Res 22:4907–4921
Fatima K, Afzal M, Imran A, Khan QM (2015) Bacterial rhizosphere and endosphere populations associated with grasses and trees to be used for phytoremediation of crude oil contaminated soil. Bull Environ Contam Toxicol 94:314–20
Fava F, Gioia DD (1998) Effects of triton X-100 and quillaya saponin on the ex situ bioremediation of a chronically polychlorobiphenyl-contaminated soil. Appl Microbiol Biotechnol 50:623–630
Fava F, Gioia DD (2001) Soya lecithin effects on the aerobic biodegradation of polychlorinated biphenyls in an artificially contaminated soil. Biotechnol Bioeng 72:177–184
Fava F, Ciccotosto V (2002) Effects of randomly methylated-β-cyclodextrins (RAMEB) on the bioavailability and aerobic biodegradation of polychlorinated biphenyls in three pristine soils spiked with a transformer oil. Appl Microbiol Biotechnol 58:393–399
Federici E, Giubilei MA, Covino S, Zanaroli G, Fava F, D’Annibale A, Petruccioli M (2012) Addition of maize stalks and soybean oil to a historically PCB-contaminated soil: effect on degradation performance and indigenous microbiota. New Biotechnol 30:69–79
Ficko SA, Rutter A, Zeeb BA (2010) Potential for phytoextraction of PCBs from contaminated soils using weeds. Sci Total Environ 408:3469–3476
Finizio A, Vighi M, Sandroni D (1997) Determination of n-octanol/water partition coefficient (Kow) of pesticide critical review and comparison of methods. Chemosphere 34:131–161
Fisk AT, Rosenberg B, Cymbalisty CD, Stern GA, Muir DCG (1999) Octanol/water partition coefficients of toxaphene congeners determined by the “slow-stirring” method. Chemosphere 39:2549–2562
Fletcher JS, Hegde RS (1995) Release of phenols by perennial plant roots and their potential importance in bioremediation. Chemosphere 31:3009–3016
Florence C, Philippe L, Magalie L-J (2015) Organochlorine (chlordecone) uptake by root vegetables. Chemosphere 118:96–102
Fu D, Teng Y, Luo Y, Tu C, Li S, Li Z, Christie P (2012) Effects of alfalfa and organic fertilizer on benzo[a]pyrene dissipation in an aged contaminated soil. Environ Sci Pollut Res 19:1605–1611
Garten CT, Trabalka JR (1983) Evaluation of models for predicting terrestrial food chain behavior of xenobiotics. Environ Sci Technol 17:590–595
Gerhardt KE, Huang X-D, Glick BR, Greenberg BM (2009) Phytoremediation and rhizoremediation of organic soil contaminants: potential and challenges. Plant Sci 176:20–30
Germaine KJ, Liu X, Cabellos GG, Hogan JP, Ryan D, Dowling DN (2006) Bacterial endophyte-enhanced phytoremediation of the organochlorine herbicide 2,4-dichlorophenoxyacetic acid. FEMS Microbiol Ecol 57:302–310
Germaine KJ, Keogh E, Ryan D, Dowling DN (2009) Bacterial endophyte-mediated naphthalene phytoprotection and phytoremediation. FEMS Microbiol Lett 296:226–234
Gilbert ES, Crowley DE (1997) Plant compounds that induce polychlorinated biphenyl biodegradation by Arthrobacter sp. strain B1B. Appl Environ Microbiol 63:1933–8
Gilbert ES, Crowley DE (1998) Repeated application of carvone-induced bacteria to enhance biodegradation of polychlorinated biphenyls in soil. Appl Microbiol Biotechnol 50:489–494
Gleba D, Borisjuk NV, Borisjuk LG, Kneer R, Poulev A, Skarzhinskaya M, Dushenkov S, Logendra S, Gleba YY, Raskin I (1999) Use of plant roots for phytoremediation and molecular farming. Proc Natl Acad Sci U S A 96:5973–5977
Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374
Gurska J, Wang W, Gerhardt KE, Khalid AM, Isherwood DM, Huang X-D, Glick BR, Greenberg BM (2009) Three year field test of a plant growth promoting rhizobacteria enhanced phytoremediation system at a land farm for treatment of hydrocarbon waste. Environ Sci Technol 43:4472–4479
Haffner D, Schecter A (2014) Persistent organic pollutants (POPs): a primer for practicing clinicians. Curr Environ Health 1:123–131
Hao Q, Sun Y-X, Xu X-R, Yao Z-W, Wang Y-S, Zhang Z-W, Luo X-J, Mai B-X (2014) Occurrence of persistent organic pollutants in marine fish from the Natuna Island, South China Sea. Mar Pollut Bull 85:274–279
Haslmayr HP, Meißner S, Langella F, Baumgarten A, Geletneky J (2014) Establishing best practice for microbially aided phytoremediation. Environ Sci Pollut Res 21:6765–6774
Hayward SJ, Lei YD, Wania F (2006) Comparative evaluation of three high-performance liquid chromatography–based Kow estimation methods for highly hydrophobic organic compounds: Polybrominated diphenyl ethers and hexabromocyclododecane. Environ Toxicol Chem 25:2018–2027
Heinrich K, Schulz E (1996) Uptake of selected organochlorine pesticides from a sandy soil (deep loam grey soil) by maize in a pot experiment. Mitteilungen der Deutschen Bodenkundlichen Gesellschaft 79:283–286 [in German]
Hernandez BS, Koh SC, Chial M, Focht DD (1997) Terpene-utilizing isolates and their relevance to enhanced biotransformation of polychlorinated biphenyls in soil. Biodegradation 8:153–158
Hinsinger P, Plassard C, Tang C, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints. Plant Soil 248:43–59
Ho Y-N, Shih C-H, Hsiao S-C, Huang C-C (2009) A novel endophytic bacterium, Achromobacter xylosoxidans, helps plants against pollutant stress and improves phytoremediation. J Biosci Bioeng 108:9–16
Hong Y, Liao D, Chen J, Khan S, Su J, Li H (2015) A comprehensive study of the impact of polycyclic aromatic hydrocarbons (PAHs) contamination on salt marsh plants Spartina alterniflora: implication for plant-microbe interactions in phytoremediation. Environ Sci Pollut Res 22:7071–7081
Ibáñez S, Alderete LS, Medina M, Agostini E (2012) Phytoremediation of phenol using Vicia sativa L. plants and its antioxidative response. Environ Sci Pollut Res 19:1555–1562
Ionescu M, Beranova K, Dudkova V, Kochankova L, Demnerova K, Macek T, Mackova M (2009) Isolation and characterization of different plant associated bacteria and their potential to degrade polychlorinated biphenyls. Int Biodeterior Biodegrad 63:667–672
Isidorov V, Jdanova M (2002) Volatile organic compounds from leaves litter. Chemosphere 48:975–979
Isnard P, Lambert S (1988) Estimating bioconcentration factors from octanol-water partition coefficient and aqueous solubility. Chemosphere 17:21–34
Jacobsen C (1997) Plant protection and rhizosphere colonization of barley by seed inoculated herbicide degrading Burkholderia (Pseudomonas) cepacia DBO1 (pRO101) in 2,4-D contaminated soil. Plant Soil 189:139–144
Jha P, Jha P (2015) Plant-microbe partnerships for enhanced biodegradation of polychlorinated piphenyls. In: Arora NK (ed) Plant microbes symbiosis. Applied facets. Springer, India, pp 95–110
Jha P, Panwar J, Jha PN (2014) Secondary plant metabolites and root exudates: guiding tools for polychlorinated biphenyl biodegradation. Int J Environ Sci Technol 25:1–14
Johansen BE (2003) The dirty dozen: toxic chemicals and the Earth’s future. Praeger, Westport, CT
Kang JW, Khan Z, Doty SL (2012) Biodegradation of trichloroethylene by an endophyte of hybrid poplar. Appl Environ Microbiol 78:3504–3507
Khan S, Afzal M, Iqbal S, Khan QM (2013a) Plant–bacteria partnerships for the remediation of hydrocarbon contaminated soils. Chemosphere 90:1317–1332
Khan S, Afzal M, Iqbal S, Mirza MS, Khan QM (2013b) Inoculum pretreatment affects bacterial survival, activity and catabolic gene expression during phytoremediation of diesel contaminated soil. Chemosphere 91:663–668
Khan MU, Sessitsch A, Harris M, Fatima K, Imran A, Arslan M, Shabir G, Khan QM, Afzal M (2014) Cr-resistant rhizo-and endophytic bacteria associated with Prosopis juliflora and their potential as phytoremediation enhancing agents in metal-degraded soils. Front Plant Sci 5:755
Khandare R, Rane N, Waghmode T, Govindwar S (2012) Bacterial assisted phytoremediation for enhanced degradation of highly sulfonated diazo reactive dye. Environ Sci Pollut Res 19:1709–1718
Khoudi H, Maatar Y, Brini F, Fourati A, Ammar N, Masmoudi K (2013) Phytoremediation potential of Arabidopsis thaliana, expressing ectopically a vacuolar proton pump, for the industrial waste phosphogypsum. Environ Sci Pollut Res 20:270–280
Kiflom WG, Wandiga SO, Nganga PK, Kamau GN (1999) Variation of plant p, p′-DDT uptake with age and soil type and dependence of dissipation on temperature. Environ Int 25:479–487
Koh S-C, Park Y-I, Koo Y-M, So J-S (2000) Plant terpenes and lignin as natural cosubstrates in biodegradation of polyclorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs). Biotechnol Bioprocess Eng 5:164–168
La Merrill M, Emond C, Kim MJ, Antignac J-P, Le Bizec B, Clément K, Birnbaum LS, Barouki R (2012) Toxicological function of adipose tissue: focus on persistent organic pollutants. Environ Health Perspect 121:162–169
Lee D-H, Porta M, Jacobs DR, Vandenberg LN (2014a) Chlorinated persistent organic pollutants, obesity, and type 2 diabetes. Endocr Rev 35:557–601
Lee I, Fletcher J (1992) Involvement of mixed function oxidase systems in polychlorinated biphenyl metabolism by plant cells. Plant Cell Rep 11:97–100
Lee S-H, Ra J-S, Choi J-W, Yim B-J, Jung M-S, Kim S-D (2014b) Human health risks associated with dietary exposure to persistent organic pollutants (POPs) in river water in Korea. Sci Total Environ 470–471:1362–1369
Leigh MB, Fletcher JS, Fu X, Schmitz FJ (2002) Root turnover: an important source of microbial substrates in rhizosphere remediation of recalcitrant contaminants. Environ Sci Technol 36:1579–1583
Leigh MB, Prouzová P, Macková M, Macek T, Nagle DP, Fletcher JS (2006) Polychlorinated biphenyl (PCB)-degrading bacteria associated with trees in a PCB-contaminated site. Appl Environ Microbiol 72:2331–2342
Li YF, Macdonald RW (2005) Sources and pathways of selected organochlorine pesticides to the arctic and the effect of pathway divergence on HCH trends in biota. Sci Total Environ 342:87–106
Lie E, Bernhoft A, Riget F, Belikov SE, Boltunov AN, Derocher AE, Garner GW, Wiig Ø, Skaare JU (2003) Geographical distribution of organochlorine pesticides (OCPs) in polar bears (Ursus maritimus) in the Norwegian and Russian Arctic. Sci Total Environ 306:159–170
Liu C-Y, Jiang X, Fan J-L, Ziadi N (2013) Hexachlorobenzene accumulation in rice plants as affected by farm manure and urea applications in dissimilar soils. Can J Soil Sci 93:631–638
Lunney AI, Zeeb BA, Reimer KJ (2004) Uptake of weathered DDT in vascular plants: Potential for phytoremediation. Environ Sci Technol 38:6147–6154
Mackay D (1982) Correlation of bioconcentration factors. Environ Sci Technol 16:274–278
Mackova M, Prouzova P, Stursa P, Ryslava E, Uhlik O, Beranova K, Rezek J, Kurzawova V, Demnerova K, Macek T (2009) Phyto/rhizoremediation studies using long-term PCB-contaminated soil. Environ Sci Pollut Res 16:817–829
Man YB, Chan JKY, Wang HS, Wu SC, Wong MH (2014) DDTs in mothers’ milk, placenta and hair, and health risk assessment for infants at two coastal and inland cities in China. Environ Int 65:73–82
Master ER, Mohn WW (2001) Induction of bphA, encoding biphenyl dioxygenase, in two polychlorinated biphenyl-degrading bacteria, psychrotolerant Pseudomonas strain Cam-1 and mesophilic Burkholderia strain LB400. Appl Environ Microbiol 67:2669–2676
Maqbool F, Wang Z, Xu Y, Zhao J, Gao D, Zhao Y-G, Bhatti ZA, Xing B (2012) Rhizodegradation of petroleum hydrocarbons by Sesbania cannabina in bioaugmented soil with free and immobilized consortium. J Hazard Mater 237–238:262–269
Mattina MJI, Iannucci-Berger W, Dykas L (2000) Chlordane uptake and its translocation in food crops. J Agric Food Chem 48:1909–1915
McCutcheon S, Schnoor J (2004) Phytoremediation: transformation and control of contaminants. Environ Sci Pollut Res 11:40–40
McLeod AM, Paterson G, Drouillard KG, Haffner GD (2014) Ecological factors contributing to variability of persistent organic pollutant bioaccumulation within forage fish communities of the Detroit River, Ontario, Canada. Environ Toxicol Chem 33:1825–1831
Mehmannavaz R, Prasher SO, Ahmad D (2002) Rhizospheric effects of alfalfa on biotransformation of polychlorinated biphenyls in a contaminated soil augmented with Sinorhizobium meliloti. Process Biochem 37:955–963
Mench M, Schwitzguébel JP, Schroeder P, Bert V, Gawronski S, Gupta S (2009) Assessment of successful experiments and limitations of phytotechnologies: contaminant uptake, detoxification and sequestration, and consequences for food safety. Environ Sci Pollut Res 16:876–900
Mikes O, Cupr P, Trapp S, Klanova J (2009) Uptake of polychlorinated biphenyls and organochlorine pesticides from soil and air into radishes (Raphanus sativus). Environ Pollut 157:488–496
Mitter B, Brader G, Afzal M, Compant S, Naveed M, Trognitz F, Sessitsch A (2013) Advances in elucidating beneficial interactions between plants, soil, and bacteria. Adv Agron 121:381–445
Mitton FM, Miglioranza KSB, Gonzalez M, Shimabukuro VM, Monserrat JM (2014) Assessment of tolerance and efficiency of crop species in the phytoremediation of DDT polluted soils. Ecol Eng 71:501–508
Mo C-H, Cai Q-Y, Li H-Q, Zeng Q-Y, Tang S-R, Zhao Y-C (2008) Potential of different species for use in removal of DDT from the contaminated soils. Chemosphere 73:120–125
Moore FP, Barac T, Borremans B, Oeyen L, Vangronsveld J, van der Lelie D, Campbell CD, Moore ERB (2006) Endophytic bacterial diversity in poplar trees growing on a BTEX-contaminated site: The characterisation of isolates with potential to enhance phytoremediation. Syst Appl Microbiol 29:539–556
Moreland DE, Corbin FT, McFarland JE (1993) Oxidation of multiple substrates by corn shoot microsomes. Pest Biochem Physiol 47:206–214
Moreland DE, Corbin FT, Fleischmann TJ, McFarland JE (1995) Partial characterization of microsomes isolated from mung bean cotyledons. Pest Biochem Physiol 52:98–108
Morris AD, Muir DCG, Solomon KR, Teixeira C, Duric M, Wang X (2014) Trophodynamics of current use pesticides and ecological relationships in the Bathurst region vegetation-caribou-wolf food chain of the Canadian Arctic. Environ Toxicol Chem 33:1956–1966
Muir DCG, Norstrom RJ, Simon M (1988) Organochlorine contaminants in arctic marine food chains: Accumulation of specific polychlorinated biphenyls and chlordane-related compounds. Environ Sci Technol 22:1071–1079
Narasimhan K, Basheer C, Bajic VB, Swarup S (2003) Enhancement of plant-microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132:146–153
Nash RG, Beall ML (1970) Chlorinated hydrocarbon insecticides: root uptake versus vapor contamination of soybean foliage. Science 168:1109–1111
Naumann C, Hartmann T, Ober D (2002) Evolutionary recruitment of a flavin-dependent monooxygenase for the detoxification of host plant-acquired pyrrolizidine alkaloids in the alkaloid-defended arctiid moth Tyria jacobaeae. Proc Natl Acad Sci U S A 99:6085–6090
Naveed M, Mitter B, Yousaf S, Pastar M, Afzal M, Sessitsch A (2014) The endophyte Enterobacter sp. FD17: a maize growth enhancer selected based on rigorous testing of plant beneficial traits and colonization characteristics. Biol Fertil Soils 50:249–262
Neal RA (1980) Microsomal metabolism of thiono-sulfur compounds: mechanisms and toxicological significance. Rev Biochem Toxicol 2:131–171
Newton S, Bidleman T, Bergknut M, Racine J, Laudon H, Giesler R, Wiberg K (2014) Atmospheric deposition of persistent organic pollutants and chemicals of emerging concern at two sites in northern Sweden. Environ Sci 16:298–305
Nicoară A, Neagoe A, Stancu P, De Giudici G, Langella F, Sprocati A, Iordache V, Kothe E (2014) Coupled pot and lysimeter experiments assessing plant performance in microbially assisted phytoremediation. Environ Sci Pollut Res 21:6905–6920
Norstrom RJ, Muir DCG (1994) Chlorinated hydrocarbon contaminants in arctic marine mammals. Sci Total Environ 154:107–128
Nurzhanova A, Kalugin S, Zhambakin K (2013) Obsolete pesticides and application of colonizing plant species for remediation of contaminated soil in Kazakhstan. Environ Sci Pollut Res 20:2054–2063
Ockenden WA, Steinnes E, Parker C, Jones KC (1998) Observations on persistent organic pollutants in plants: implications for their use as passive air samplers and for POP cycling. Environ Sci Technol 32:2721–2726
Pandey J, Chauhan A, Jain RK (2009) Integrative approaches for assessing the ecological sustainability of in situ bioremediation. FEMS Microbiol Rev 33:324–375
Passatore L, Rossetti S, Juwarkar AA, Massacci A (2014) Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): state of knowledge and research perspectives. J Hazard Mater 278:189–202
Phillips LA, Germida JJ, Farrell RE, Greer CW (2008) Hydrocarbon degradation potential and activity of endophytic bacteria associated with prairie plants. Soil Biol Biochem 40:3054–3064
Pilon-Smits E (2005) Phytoremediation. Ann Rev Plant Biol 56:15–39
Qin H, Brookes PC, Xu J (2014) Cucurbita spp. and Cucumis sativus enhance the dissipation of polychlorinated biphenyl congeners by stimulating soil microbial community development. Environ Pollut 184:306–312
Qiu J (2013) Organic pollutants poison the roof of the world. Accumulation of DDT in Himalayas exceeds that seen in Arctic. Nat News. doi:10.1038/nature.2013.12776
Rahman F, Langford KH, Scrimshaw MD, Lester JN (2001) Polybrominated diphenyl ether (PBDE) flame retardants. Sci Total Environ 275:1–17
Rao A (1990) Root flavonoids. Bot Rev 56:1–84
Ritter L, Solomon K, Forget J, Stemeroff M, O’Leary C (1995) An assessment report on DDT, aldrin, dieldrin, endrin, chlordane, heptachlor, hexachlorobenzene, mirex, toxaphene, polychlorinated biphenyls, dioxins and furans. International Programme on Chemical Safety (IPCS) within the framework of the Inter-Organization Programme for the Sound Management of Chemicals (IOMC), Geneva, PCS/95.39. pp 1-43
Ruegg EF, Lord KA, Mesquita TB (1977) Uptake and movement of 14C-lindane in coffee plants. Arquivos do Instituto Biologico 44:235–246
Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9
Rylott E (2014) Endophyte consortia for xenobiotic phytoremediation: the root to success? Plant Soil 385:389–394
Saleh S, Huang X-D, Greenberg BM, Glick BR (2004) Phytoremediation of persistent organic contaminants in the environment. In: Ajay S, Ward S (eds) Applied bioremediation and phytoremediation. Springer, pp 115-134
Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Annu Rev Plant Physiol Plant Mol Biol 49:643–668
Samardjieva K, Tavares F, Pissarra J (2015) Histological and ultrastructural evidence for zinc sequestration in Solanum nigrum L. Protoplasma 252:345–357
Sandermann H Jr (1992) Plant metabolism of xenobiotics. Trends Biochem Sci 17:82–84
Sandermann H Jr (1994) Higher plant metabolism of xenobiotics: the ‘green liver’ concept. Pharmacog Genom 4:225–241
Schell MA (1985) Transcriptional control of the nah and sal hydrocarbon-degradation operons by the nahR gene product. Gene 36:301–309
Schulz B, Boyle C (2006) What are endophytes? In: Schulz BE, Boyle CC, Sieber T (eds) Microbial root endophytes. Springer, Berlin Heidelberg, pp 1–13
Schwitzguébel JP, Schröder P (2009) Phytotechnologies to promote sustainable land use and improve food safety: Outcomes and outlook from the European COST Action 859. Environ Sci Pollut Res 16:743–744
Sessitsch A, Coenye T, Sturz A, Vandamme P, Barka EA, Salles J, Van Elsas J, Faure D, Reiter B, Glick B (2005) Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187–1192
Sharma BM, Bharat GK, Tayal S, Nizzetto L, Čupr P, Larssen T (2014a) Environment and human exposure to persistent organic pollutants (POPs) in India: a systematic review of recent and historical data. Environ Int 66:48–64
Sharma BM, Bharat GK, Tayal S, Nizzetto L, Larssen T (2014b) The legal framework to manage chemical pollution in India and the lesson from the persistent organic pollutants (POPs). Sci Total Environ 490:733–747
Shehzadi M, Afzal M, Khan MU, Islam E, Mobin A, Anwar S, Khan QM (2014) Enhanced degradation of textile effluent in constructed wetland system using Typha domingensis and textile effluent-degrading endophytic bacteria. Water Res 58:152–159
Shehzadi M, Fatima K, Imran A, Mirza MS, Khan QA, Afzal M (2015) Ecology of bacterial endophytes associated with wetland plants growing in textile effluent for pollutant-degradation and plant growth-promotion potentials. Plant Biosyst (in press). doi:10.1080/11263504.2015.1022238
Sheng X, Chen X, He L (2008) Characteristics of an endophytic pyrene-degrading bacterium of Enterobacter sp. 12J1 from Allium macrostemon Bunge. Int Biodeterior Biodegrad 62:88–95
Siciliano SD, Germida JJ (1998) Mechanisms of phytoremediation: biochemical and ecological interactions between plants and bacteria. Environ Rev 6:65–79
Siciliano SD, Goldie H, Germida JJ (1998) Enzymatic activity in root exudates of Dahurian wild rye (Elymus dauricus) that degrades 2-chlorobenzoic acid. J Agric Food Chem 46:5–7
Simpson CD, Wilcock RJ, Smith TJ, Wilkins AL, Langdon AG (1995) Determination of octanol-water partition coefficients for the major components of technicale chlordane. Bull Environ Contam Toxicol 55:149–153
Singer AC, Gilbert ES, Luepromchai E, Crowley DE (2000) Bioremediation of polychlorinated biphenyl-contaminated soil using carvone and surfactant-grown bacteria. Appl Microbiol Biotechnol 54:838–843
Singer AC, Crowley DE, Thompson IP (2003) Secondary plant metabolites in phytoremediation and biotransformation. Trends Biotechnol 21:123–130
Singh G, Dowman A, Higginson FR, Fenton IG (1992) Translocation of aged cyclodiene insecticide residues from soil into forage crops and pastures at various growth stages under field conditions. J Environ Sci Health 27:711–728
Smith KEC, Jones KC (2000) Particles and vegetation: implications for the transfer of particle-bound organic contaminants to vegetation. Sci Total Environ 246:207–236
Sprocati A, Alisi C, Pinto V, Montereali M, Marconi P, Tasso F, Turnau K, De Giudici G, Goralska K, Bevilacqua M, Marini F, Cremisini C (2014) Assessment of the applicability of a “toolbox” designed for microbially assisted phytoremediation: the case study at Ingurtosu mining site (Italy). Environ Sci Pollut Res 21:6939–6951
Staniforth S (2013) Historical perspectives on preventive conservation. Readings in conservation. Los Angeles: Getty Conservation Institute
Susarla S, Medina VF, McCutcheon SC (2002) Phytoremediation: an ecological solution to organic chemical contamination. Ecol Eng 18:647–658
Takaki K, Wade AJ, Collins CD (2014) Assessment of plant uptake models used in exposure assessment tools for soils contaminated with organic pollutants. Environ Sci Technol 48:12073–12082
Talekar NS, Chen JS, Lee EM, Lee TM (1985) Absorption of certain insecticide residues from contaminated soil by sweet potato roots. Plant Prot Bull (China) 27:423–432
Tandlich R, Brežná B, Dercová K (2001) The effect of terpenes on the biodegradation of polychlorinated biphenyls by Pseudomonas stutzeri. Chemosphere 44:1547–1555
Thijs S, Van Dillewijn P, Sillen W, Truyens S, Holtappels M, D´Haen J, Carleer R, Weyens N, Ameloot M, Ramos J-L, Vangronsveld J (2014) Exploring the rhizospheric and endophytic bacterial communities of Acer pseudoplatanus growing on a TNT-contaminated soil: towards the development of a rhizocompetent TNT-detoxifying plant growth promoting consortium. Plant Soil 385:15–36
Thijs S, Vangronsveld J (2015) Rhizoremediation. In: Lugtenberg B (ed) Principles of plant-microbe interactions. Springer International Publishing, pp 277-286
Trapp S, Zambrano KC, Kusk KO, Karlson U (2000) A phytotoxicity test using transpiration of willows. Arch Environ Contam Toxicol 39:154–160
UNEP (2003) Global report on regionally based assessment of persistent toxic substances. UNEP Chemicals, Geneva, Switzerland
Vafeiadi M, Vrijheid M, Fthenou E, Chalkiadaki G, Rantakokko P, Kiviranta H, Kyrtopoulos SA, Chatzi L, Kogevinas M (2014) Persistent organic pollutants exposure during pregnancy, maternal gestational weight gain, and birth outcomes in the mother–child cohort in Crete, Greece (RHEA study). Environ Int 64:116–123
Van Aken B, Yoon J, Schnoor J (2004) Biodegradation of nitro-substituted explosives 2,4,6-trinitrotoluene, hexahydro-1,3,5-trinitro-1,3,5-triazine, and octahydro-1,3,5,7-tetranitro-1,3,5-tetrazocine by a phytosymbiotic Methylobacterium sp. associated with poplar tissues (Populus deltoides x nigra DN34). Appl Environ Microbiol 70:508–517
Vangronsveld J, Herzig R, Weyens N, Boulet J, Adriaensen K, Ruttens A, Thewys T, Vassilev A, Meers E, Nehnevajova E, Van Der Lelie D, Mench M (2009) Phytoremediation of contaminated soils and groundwater: Lessons from the field. Environ Sci Pollut Res 16:765–794
Villacieros M, Whelan C, Mackova M, Molgaard J, Sánchez-Contreras M, Lloret J, Aguirre de Cárcer D, Oruezábal RI, Bolaños L, Macek T, Karlson U, Dowling DN, Martín M, Rivilla R (2005) Polychlorinated biphenyl rhizoremediation by Pseudomonas fluorescens F113 derivatives, using a Sinorhizobium meliloti nod system to drive bph gene expression. Appl Environ Microbiol 71:2687–2694
Voerman S, Besemer AFH (1975) Persistence of dieldrin, lindane, and DDT in a light sandy soil and their uptake by grass. Bull Environ Contam Toxicol 13:501–505
Voldner EC, Li Y-F (1995) Global usage of selected persistent organochlorines. Sci Total Environ 160–161:201–210
Vrkoslavová J, Demnerová K, Macková M, Zemanová T, Macek T, Hajšlová J, Pulkrabová J, Hrádková P, Stiborová H (2010) Absorption and translocation of polybrominated diphenyl ethers (PBDEs) by plants from contaminated sewage sludge. Chemosphere 81:381–386
Walsh G, Hollister T, Forester J (1974) Translocation of four organochlorine compounds by red mangrove (Rhizophora mangle L.) seedlings. Bull Environ Contam Toxicol 12:129–135
Wang YH, Wong PK (2002) Mathematical relationships between vapor pressure, water solubility, Henry's law constant, n-octanol/water partition coefficient and gas chromatographic retention index of polychlorinated-dibenzo-dioxins. Water Res 36:350–355
Wang C, Liu Z (2007) Foliar uptake of pesticides—present status and future challenge. Pest Biochem Physiol 87:1–8
Wang Y, Li H, Zhao W, He X, Chen J, Geng X, Xiao M (2010) Induction of toluene degradation and growth promotion in corn and wheat by horizontal gene transfer within endophytic bacteria. Soil Biol Biochem 42:1051–1057
Wang RQ (2012) Degradation of persistent organic pollutants: mechanism summary. Adv Mater Res 356:620–623
Wang Y, Xu M, Jin J, He S, Li M, Sun Y (2014) Concentrations and relationships between classes of persistent halogenated organic compounds in pooled human serum samples and air from Laizhou Bay, China. Sci Total Environ 482–483:276–282
Weber R, Watson A, Forter M, Oliaei F (2011) Persistent organic pollutants and landfills—a review of past experiences and future challenges. Waste Manag Res 29:107–121
Weiss P, Lorbeer G, Scharf S (1998) Semivolatile organic compounds in spruce needles and forest soil of Austrian background forest sites. Organohalogen Compd 39:381–384
Westcott ND (1985) Gamma‐HCH in rape seedlings grown from treated seeds. Pest Sci 16:416–421
Weyens N, Van Der Lelie D, Taghavi S, Newman L, Vangronsveld J (2009a) Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27:591–598
Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009b) Phytoremediation: plant–endophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254
Weyens N, Taghavi S, Barac T, van der Lelie D, Boulet J, Artois T, Carleer R, Vangronsveld J (2009c) Bacteria associated with oak and ash on a TCE-contaminated site: characterization of isolates with potential to avoid evapotranspiration of TCE. Environ Sci Pollut Res 16:830–843
Weyens N, Croes S, Dupae J, Newman L, van der Lelie D, Carleer R, Vangronsveld J (2010a) Endophytic bacteria improve phytoremediation of Ni and TCE co-contamination. Environ Pollut 158:2422–2427
Weyens N, Truyens S, Dupae J, Newman L, Taghavi S, van der Lelie D, Carleer R, Vangronsveld J (2010b) Potential of the TCE-degrading endophyte Pseudomonas putida W619-TCE to improve plant growth and reduce TCE phytotoxicity and evapotranspiration in poplar cuttings. Environ Pollut 158:2915–2919
White JC (2000) Phytoremediation of weathered p, p′-DDE residues in soil. Int J Phytorem 2:133–144
White JC, Mattina MI, Lee W-Y, Eitzer BD, Iannucci-Berger W (2003) Role of organic acids in enhancing the desorption and uptake of weathered p, p′-DDE by Cucurbita pepo. Environ Pollut 124:71–80
White JC, Parrish ZD, Isleyen M, Gent MPN, Iannucci-Berger W, Eitzer BD, Mattina MI (2005) Influence of nutrient amendments on the phytoextraction of weathered 2,2-bis(p-chlorophenyl)-1,1-dichloroethylene by cucurbits. Environ Toxicol Chem 24:987–994
White J, Zeeb B (2007) Plant phylogeny and the remediation of persistent organic pollutants. In: Willey N (ed) Phytoremediation: methods in biotechnology. Humana Press, pp 71-87
Whitfield Åslund ML, Zeeb BA, Rutter A, Reimer KJ (2007) In situ phytoextraction of polychlorinated biphenyl — (PCB) contaminated soil. Sci Total Environ 374:1–12
Wikoff D, Fitzgerald L, Birnbaum L (2012) Persistent organic pollutants: an overview, Dioxins and Health. John Wiley & Sons, Inc., pp. 1-35
WWF (2005) Toxic Fact Sheets. World Wildlife Fund.http://www.worldwildlife.org/toxics/ pubs.cfm
Wu J-P, Luo X-J, Zhang Y, Luo Y, Chen S-J, Mai B-X, Yang Z-Y (2008) Bioaccumulation of polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) in wild aquatic species from an electronic waste (e-waste) recycling site in South China. Environ Int 34:1109–1113
Xu W, Wang X, Cai Z (2013) Analytical chemistry of the persistent organic pollutants identified in the Stockholm Convention. Anal Chim Acta 790:1–13
Xun F, Xie B, Liu S, Guo C (2015) Effect of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) inoculation on oats in saline-alkali soil contaminated by petroleum to enhance phytoremediation. Environ Sci Pollut Res 22:598–608
Yateem A (2013) Rhizoremediation of oil-contaminated sites: a perspective on the Gulf War environmental catastrophe on the State of Kuwait. Environ Sci Pollut Res 20:100–107
Yousaf S, Afzal M, Anees M, Malik RN, Campisano A (2014) Ecology and functional potential of endophytes in bioremediation: a molecular perspective. In: Verma VC, Gange AC (eds) Advances in endophytic research. Springer, India, pp 301–320
Yousaf S, Afzal M, Reichenauer TG, Brady CL, Sessitsch A (2011) Hydrocarbon degradation, plant colonization and gene expression of alkane degradation genes by endophytic Enterobacter ludwigii strains. Environ Pollut 159:2675–2683
Yousaf S, Ripka K, Reichenauer T, Andria V, Afzal M, Sessitsch A (2010) Hydrocarbon degradation and plant colonization by selected bacterial strains isolated from Italian ryegrass and birdsfoot trefoil. J Appl Microbiol 109:1389–1401
Zeng X-L, Wang H-J, Wang Y (2012) QSPR models of n-octanol/water partition coefficients and aqueous solubility of halogenated methyl-phenyl ethers by DFT method. Chemosphere 86:619–625
Zhan X, Yuan J, Yue L, Xu G, Hu B, Xu R (2015) Response of uptake and translocation of phenanthrene to nitrogen form in lettuce and wheat seedlings. Environ Sci Pollut Res 22:6280–6287
Zhu X, Ni X, Liu J, Gao Y (2014) Application of endophytic bacteria to reduce persistent organic pollutants contamination in plants. Clean Soil Air Water 42:306–310
Acknowledgments
This study was financially supported by the Higher Education Commission (HEC, research grant number 1997), Pakistan, and International Foundation of Science (IFS) Sweden and Organization for the Prohibition of Chemical Weapons (OPCW) (research grant number W/5104-2) to Muhammad Afzal. The authors are thankful to the editor and anonymous reviewers of Environmental Science and Pollution Research for their comments and suggestions.
Compliance with ethical standards
The authors declare that they have no conflict of interest. It is declared that the research was not involved human participation and/or animals. The manuscript is neither published nor is under consideration to publish, elsewhere. Moreover, the content and authorship of the submitted manuscript has been approved by all the authors as well as by responsible authorities.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Hongwen Sun
Rights and permissions
About this article
Cite this article
Arslan, M., Imran, A., Khan, Q.M. et al. Plant–bacteria partnerships for the remediation of persistent organic pollutants. Environ Sci Pollut Res 24, 4322–4336 (2017). https://doi.org/10.1007/s11356-015-4935-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-4935-3