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ISSN : 1598-5504(Print)
ISSN : 2383-8272(Online)
Journal of Agriculture & Life Science Vol.53 No.5 pp.1-12

Endophyte-assisted phytoremediation of Organic pollutants

Jun Won Kang1, Yeong Dae Park2*
1School of Forest Sciences and Landscape Architecture, Kyungpook National University, Daegu 41566, Republic of Korea
2Department of Forest Resources, Daegu University, Gyeongsan, Gyeongbuk 38453, Republic of Korea
Corresponding author: Yeong Dae Park Tel: +82-53-850-6731 Fax: +82-53-210-8840 E-mail:
August 6, 2019 August 27, 2019 August 30, 2019


Rapid industrialization and urbanization have generated huge amount of environmental pollution. Especially, synthetic organic chemicals have been a serious international problem for over half a century due to their toxic and hazardous chemicals. Eco-friendly strategies for removing the chemicals from the soil and water are becoming a top priority around the world and biological treatment such as phytoremediation and bioremediation is less expensive and more sustainable than other conventional remediation techniques. Recently, many pollutant diminishing microbial endophytes have been discovered from various plants grown in contaminated area and the function of microbes to improve phytoremediation of organic pollutants has been reported. Thus, we classify synthetic organic pollutants into groups of similar compounds and discuss the contribution of endophytes to enhance phytoremediation.


    Kyungpook National University


    Organic chemicals (OCs) are made primarily of carbon along with other elements. Many of the naturally occurring organic compounds, produced by plants or animals, are benign, but most synthetic organic compounds, generated by a variety of human activities including agriculture and industry, are posing serious threats to human and environment due to their toxicity (Adeola, 2011). Important synthetic organic pollutants include chlorinated hydrocarbons (CHCs), polycyclic aromatic hydrocarbons (PAHs), explosives, and pesticides / herbicides. In addition, naturally occurring and man-made industrial chemicals such as benzene, toluene, ethylbenzene, and xylene (BTEX) can contaminate water resources. Especially, over 60% of the OCs detected in urban areas and these contaminants can accumulate and persist for long periods of time in environment (van Afferden et al., 2011). The removal of these organic compounds from soil and water is one of the main issues in the field of environmental sciences and engineering (Wei et al., 2014;Zhu et al., 2014, Glick, 2015). Various physical and chemical engineering techniques have been applied to clean up the pollutants. However, these approaches are expensive and cause secondary contamination or damage to the environment (Kang, 2014). In this regard, advanced environmental-friendly decontamination methods such as bioremediation and phytoremediation are often considered to be cost-effective, especially for remediating large contaminated areas.

    Generally, it has been known that toxic organic compounds can be naturally transformed or mineralized by a wide variety of living organisms such as plants and microbes. Exclusively, some microorganisms can utilize organic compounds as carbon and energy sources, or co-metabolize them in the presence of applicable growth substrates under aerobic condition (Maszenan et al., 2011;Díaz et al., 2013;Ijaz et al., 2016;Li et al., 2014). Moreover, oxidative cometabolism or reductive dehalogenation occurs under anaerobic conditions (Khalid et al., 2011;Tierney & Young, 2010).

    Plant associated endophytic bacteria refer to microbes which live the internal tissues of plants without causing any harm. These microorganisms have enormous potential to degrade organic pollutants (Doty, 2015;Feng et al., 2017) and promote plant growth (Harman & Uphoff, 2019). In addition, they have various types of organic degradation pathways like soil bacteria, so these microorganisms can increase plant tolerance to pollutant stress and utilize pollutant as well as promote plant growth (Akbar et al., 2015;Feng et al., 2017). Mostly, pollutant-degrading bacteria have various specific genes for efficient degradation of organic contaminants (Table 1). One of the most important enzyme complexes in the aerobic degradation of many aromatic compounds is aromatic ring dioxygenase (Peng et al., 2015). Fig. 1

    All these specific enzymes have significant potential for degrading a wide range of toxic chemicals. Interestingly, some of natural endophytic bacteria may not possess these capacity but they could acquire specific genes for degradation through horizontal gene transfer within endophytic communities (Taghavi et al., 2005;Wang et al., 2010). Moreover, they can utilize plant’s phenolic compounds such as flavonoids, terpenoids, phenolic acids, and resin acids as growth substrates and / or regulators (Kang & Doty, 2014;Kang et al., 2012;Matsuura & Fett-Neto, 2015). Indeed, the release of root exudates such as phenolic compounds is one of the factors that contribute to the enhanced microbial xenobiotic degradation (Pagé et al., 2015). These biological processes are characteristics of microbes to rapidly adapt to the new environment (Zhalnina et al., 2018).

    Recently, many pollutant degrading endophytic bacteria have been isolated from various plants grown in contaminated area and the function of endophytic bacteria to enhance phytoremediation of organic pollutants has been reported. In this review, we classify synthetic organic pollutants into groups of similar compounds and discuss the contribution of endophytes to enhance phytoremediation.

    Polycyclic Aromatic Hydrocarbons (PAHs)

    PAHs are a class of chemicals that encompass hundreds of compounds including pyrene, naphthalene, and phenanthrene. They are one of the most widespread organic pollutants, recorded as priority pollutants by both the United States Environmental Protection Agency (EPA) and the European Community (Samanta et al., 2002). The most part of these chemicals are highly intractable molecules due to their low water solubility. These hydrophobic chemicals are commonly detected in the environment from the incomplete combustion of petroleum compounds (Andreoni & Gianfreda, 2007;Kamal et al., 2015).

    Several PAHs degrading endophytes have been isolated from the plants grown in the PAHscontaminated soils. Phenanthrene is one of the most abundant PAHs in the environment. Recently, Khan et al. (2014) isolated Pseudomonas putida PD1 from poplar tree. Willow and grasses inoculated with the PD1 could dramatically remove phenanthrene from soil when compared to the uninoculated controls. In a similar research, Liu et al. (2014a) found a phenanthrene-degrading. microbial endophyte, Pn2, from water foxtail (Alopecurus aequalis) grown in the PAHs polluted soils. When the bacterium Pn2 was applied to the hydroponic Hoagland medium with 2 mg l-1 of phenanthrene, the phenanthrene concentrations in ryegrass were decreased by 57%, compared with the control treatment. Sun et al. (2014a;2015a), also, reported a phenanthrene-degrading endophytic bacterium Pseudomonas sp. Ph6 which was isolated from clover (Trifolium pratense L.) grown in a PAH-contaminated site. In another study, an endophytic fungus, Ceratobasidum stevensii, was isolated from the Eupharbiaceae plants. This endophyte removed 89.51% of phenanthrene when added to fungal cultures after 10 days of incubation (Dai et al., 2010). Recently, Sun et al. (2015b) reported that the surface and inside of cowpea root nodules were colonized with bacterial consortia that utilized phenanthrene.

    Pyrene is one of the high molecular weight PAHs. It is frequently more difficult to degrade pyrene compared to other low molecular weight PAH, due to their lower solubility and biodegradability. Sheng et al. (2008) isolated pyrene-degrading endophytic bacteria, Enterobacter sp. 12J1, from Allium macrostemon Bunge, which showed 83.8% degradation of pyrene (5 mg l-1) for 7 days. Recently, Sun et al. (2014b), also, found pyrene degrading endophyte, Staphylococcus sp. BJ06, from Alopecurus aequalis and could degrade 56.0 % of pyrene (s50 mg l-1) within 15 days.

    Anthracene (ANT), a tricyclic PAH, is also found in high concentrations in PAH-contaminated sediments, surfaces soils, and waste sites (Cui et al., 2014). Bisht et al. (2014) have reported several PAHs degrading endophytes from the roots of Populus deltoides growing in non-contaminated sites. The isolates showed 83.4% degradation of anthracene while 75.1% decrease in naphthalene concentration after 6 days of incubation.

    Recently, several studies have reported the use of intentional inoculations of plants with specific pollutant degrading soil bacteria. Hybrid poplar and Arabidopsis inoculated with Burkholderia fungorum DBT1 (Andreolli et al., 2013) and Achromobacter xylosoxidans F3B (Ho et al., 2012), respectively, greatly enhanced phytoremediation efficiency of PAH. Application of engineered naphthalene-degrading endophytic bacteria to enhance phytoremediation has been reported by Germaine et al. (2009). The inoculation of plants with the engineered strain facilitated higher (40%) naphthalene degradation rates compared with the uninoculated plants in the artificially contaminated soil.

    Chlorinated hydrocarbons

    Chlorinated hydrocarbons are the most commonly detected organic compounds in the environment. They are suspected of and known for toxic and carcinogenic. Trichloroethylene (TCE) is widely present in the environment and one of the main pollutants listed by the US EPA. Weyens et al. (2010a) investigated TCE degradation and evapotranspiration of yellow lupine plants inoculated with Burkholderia cepacia VM1468 which possesses constitutive TCE degrading pTOM-Bu61 plasmid Treated with the B. cepacia VM1468 diminished phytotoxicity and TCE evapotranspiration, and strongly increased Ni uptake by its host yellow lupine. In a similar approach, poplar cuttings inoculated with the TCE-degrading Pseudomonas putida W619-TCE improved TCE degradation. Inoculation with P. putida W619-TCE promoted plant growth, reduced TCE phytotoxicity and the amount of TCE present in the leaves (Weyens et al., 2010b). Recently, they evaluated Ni uptake and TCE degradation of Ni-TCE-exposed poplar cuttings with P. putida W619-TCE and reported similar results (Weyens et al., 2015). A novel endophyte, Enterobacter sp. strain PDN3, from hybrid poplar was also reported to degrade TCE effectively Kang et al. (2012). Without the addition of inducers such as toluene or phenol, the PDN3 reduced 80% of TCE levels in medium with chloride ion production. In addition, three-year field trial of endophyte-assisted phytoremediation on the superfund study area, the PDN3 treated poplar trees showed heightened growth and diminished TCE phytotoxic effects with a 32% increase in trunk diameter compared to control treatments. And the PDN3 treated trees secreted 50% more chloride ion into the root zone, demonstrative of elevated TCE metabolism in plants (Doty et al., 2017).

    BTEX chemicals

    BTEX refers to the chemicals such as benzene, toluene, ethylbenzene and xylene. BTEX is both naturally occuring and man-made. BTEX are typical hazardous organic compounds that are found mainly in petroleum products such as gasoline. These pollutants have been found to cause many serious health effects to humans (ata Mitra & Roy, 2011). Several studies have examined the possibilities of using endophytes for assisting the phytoremediation of BTEX contaminated soil and groundwater. The first engineered endophyte study was reported by Barac et al. (2004). Burkholderia cepacia L.S.2.4, a natural microbial endophyte of yellow lupine (Lupinus luteus) was conceived with toluene degrading plasmid of B.cepacia G4. The bacteria actively removed toluene, resulting in a notably reduction in its phytotoxicity, and a 50-70% reduction of its evapotranspiration through the leaves. In another study, Moore and his colleagues (2006) described 121 endophytes from hybrid poplar at a site contaminated with BTEX. Some of the isolates from the site demonstrated the ability to degrade BTEX compounds or to grow in the presence of TCE. Recently, Iqbal et al. (2019) reported thirteen (13) endophytic bacterial strains were isolated from Echinochloa crus-galli (Cockspur grass) and Cynodon dactylon (Bermuda grass) growing in an oil-contaminated site at a petroleum storage and transportation facility. Of the 13 microbial endophytes were isolated from Cockspur grass (Echinochloa crus-galli) and Bermuda grass (Cynodon dactylon) growing in petroleum contaminated area. Of the 13 strains evaluated their capacity to diminish mono-aromatic hydrocarbons such as phenol, toluene, and xylene. Interestingly, Pseudomonas sp. J10 removed 69% diesel in four days. These results could be applied to support Biodegradation of diesel oil.


    Explosives are extremely reactive chemical compounds. Improper waste disposal of the chemicals are easily released into the nature. In particular, explosive residues can affect various environmental factors (Crocker et al., 2006) since they can easily move to water and groundwater (Clausen et al., 2004). The main explosives at the military training zones are 2,4,6-trinitrotoluene (TNT), hexahydro-1,3,5-trinitro-1,3,5-triazine or royal demolition explosive (RDX), and octahydro-1,3,5,7- tetranitro-1,3,5,7-tetrazocine or high-melting-point explosive (HMX) (Van Aken et al., 2004). They are listed as priority pollutants by the U.S. EPA.

    Many studies have reported the fate of explosives and its metabolites in plants (Vanek et al., 2006;Van Aken, 2009) as well as bioremediation of explosives (Kanekar et al., 2014, Nõlvak et al., 2013). However, there has been a little research conducted on explosivedegrading endophyte. Van Aken et al. (2011) reported a methylotrophic bacterium, Methylobacterium sp. strain BJ001, isolated from hybrid poplar (P. deltoides × P. nigra DN34). The microbial endophyte could mineralize the RDX and HMX to carbon dioxide approximately 60% in 2 months.

    Synthetic pesticides and herbicides

    Synthetic pesticides are most commonly used for pest control in agricultural plantations and have been caused significant environmental problems. Wide ranges of human health hazards including cancer are related with abuse and misuse of chemical synthetic pesticides (Gilden et al., 2010). Especially, organophosphorus compounds like chlorpyrifos, organochlorine and dichlorodiphenyl trichloroethane (DDT) are most widely used chemical synthetic pesticides in the field of agriculture and forestry for controlling diseases and insect pests (Mauriz et al., 2006). Germaine et al. (2006) described the inoculation of a model plant, Pisum sativum, with a genetically tagged bacterial endophyte that naturally possesses the capability to remove 2,4- dichlorophenoxyacetic acid (2,4-D). Their consequence showed that the inoculated plants had a higher capacity for degrading 2,4-D from the soil and their aerial tissues totally removed 2,4-D. Quinclorac (3,7- dichloro-8-quinoline-carboxylic) is also, a extremely selective synthetic auxin herbicide and it is broadly used for controlling weeds in rice fields (Grossmann, 1998). Liu et al. (2014b) reported the first endophyte Bacillus megaterium Q3 that is able to degrade quinclorac. The Q3 could remove 93% of quinclorac from the initial concentration of 20 mg/L in seven days under the optimal degrading condition.

    Chlorpyrifos is a broad-spectrum and moderately toxic organophosphate insecticide. It is the most frequent contaminants of a wide range of environments (Wang et al., 2015). Recently, Jabeen et al. (2016) reported the first chlorpyrifos (CP) and 3,5,6- trichloro-2-pyridinol (TCP) degrading microbial strain Mesorhizobium sp. HN3. They also demonstrated the capacity of microbial endophytes for removing of CP chemicals taken up by the plants and boosted the remediation of CP polluted soil (Jabeen et al., 2015).


    Environmental pollution by man-made organic chemicals has been a serious international problems for over half a century. The organic chemicals are prevalent in air, water, soil, and organisms including animals and plants throughout the world. Exposure to most synthetic organic chemicals may result in serious environmental and health effects including carcinogenicity and neurotoxicity. Therefore, innovative and efficient removing methods that are costeffective and easily accepted by the public should be developed to reduce synthetic organic pollutants. Recently, the application of beneficial endophytic bacteria for improving the plant growth and removing pollutants has been proven that microbial endophytes could be more dependable genetic resources. In addition, they have been recognized as essential materials for promoting agriculture and phytoremediation. The systematic informations and discussions regarding on the phytoremediation of organic pollutants with microbial endophytes in this paper may provide practical consideration and guidance for application of eco-friendly green technology. However, further research is needed to clearly define the environmental functions and roles of specific endophytes.


    This research was supported by Kyungpook National University Research Fund, 2019.



    Plant-endophyte partnerships for phytoremediation of soils contaminated with organic pollutants.


    List of organic compound degrading enzymes from the microorganisms


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