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  • Bioremediation of Polychlorinated Biphenyls- Impact on Ecosystem and Biodegradation Pathways

  • 1Department of Biosciences, JIS University, 81, Nilgunj Rd, Agarpara, Kolkata, West Bengal 700109, India
    2Department of Microbiology, Scottish Church College, Manicktala, Kolkata, West Bengal 700006
     

Abstract

Polychlorinated biphenyls (PCBs) are a group of chlorinated aromatic compounds found in nature as byproduct of several industrial reactions. They are persistent organic pollutants, sparingly water soluble and can be found far away from point source of pollution. They are a great nuisance to the environment and ecosystem. Chemically they are hydrophobic in nature with severe toxicity and high bioaccumulation rate. They have varied congeners which depends on the number and position of the chlorine atoms in the aromatic ring. Usually the high molecular weight congeners pose real threat to soil and biotic life associated with it as they are recalcitrant over the low molecular weight compounds. Inspite of the restricted usage, their presence is sensed as a byproduct of certain chemical reactions of anthropogenic origin. Excessive exposure of humans to PCBs, impairs the immune system. They have negative impact on agricultural land like loss of soil health, soil microbes and soil protein. Moreover they gain entry into the food chain and being highly hydrophobic accumulate in the lipid biomass. Bioremediation strategies are designed and formulated to circumvent their effect from the ecosystem. In this review an attempt has been made to discuss on the impact of PCBs on ecosystem, its bioremediation trail and mitigation solutions.

Keywords

PCBs, Ecosystem, Bioremediation, Congeners, Biodegradation

Introduction

PCBs are one of the most persistent organohalide groups of environment pollutants which are present in natural gas, coal tar and crude oil. They are produced during the synthesis of plastics and crop protection products and also used in heat transfer fluids. PCBs are accumulating in high percentage in the biota, taking entry in the food chain and causing multiple health hazards1,2,3. They are hydrophobic in nature and tend to accumulate in fat bodies of human system. Their presence has been noted in human’s blood, tissues, and even breast milk and is introduced into the food chain via consumption of meat, fish, and dairy products4-7. Now a days the use of biphenyl and PCBs have been significantly reduced but they still remain in the environment because of their stable chemical structure. PCB molecules consist of a biphenyl nucleus carrying 1 to 10 chlorines, which can create more than 200 possible congeners which differ only in the number and position of the chlorines. Thus, quick removal of these organic pollutants from contaminated environments is urgently required to cover up their damage to our ecosystems8.The source of origin of man-made PCB, its impact on soil and humans along with bioremediation solutions are depicted in the illustrative Fig.1.

Figure 1. Showing the various congener sources, impact and mitigation strategies of PCB

Agricultural lands consist of heterogeneous mixture of soil components both biotic and abiotic in nature. PCBs have direct influence on soil abiotic components like texture, moisture, porosity and soil organic matter whereas enzyme activity of biotic components are hindered by indirect process9-11. Bioremediation of PCBs through microbial degradation is regarded as one of the most cost-effective and energy-efficient methods for their removal from the environment. The process is achieved through naturally occurring microbes like bacteria, fungi and algae to degrade, convert and/or remove toxic PCBs into non-toxic ones12-16. Therefore, primary focus lies on the selection of highly efficient PCB-degrading microbes. Many isolates have already been reported, including Gram-negative strains, such as Pseudomonas, Alcaligenes, Achromobacter, Janibacter, Burkholderia, Acinetobacter, Comamonas, Sphingomonas, Paenibacillus, and Ralstonia, and Gram-positive strain, such as Arthrobacter, Corynebacterium, Rhodococcus, and Bacillus17-18. Advanced degradation of PCB was achieved to 67.7 and 71.7% by eliminating the electronegative contaminants from the soil sample and supplementing with methanol and cowdung as electron donor was also reported by researchers. PCB are present in air, water, biota and agricultural fields but can be transported far away from their generation site to non-point sources like the Arctic regions. Long time PCB exposure causes chronic inflammatory diseases affecting cardiovascular system, disruption of endocrine system19-21.

Properties and Sources

PCBs have two linked aromatic rings substituted by 1-10 chlorine atoms. The less chlorinated congeners are less toxic, whereas more chlorinated congeners show higher toxicity. About twenty-nine of these congeners are found more stable.  Toxicological problems of PCB are associated with its co-planar congeners, that show more toxicity carry 5-10 chlorine atoms, in para and meta positions22. According to EPA, 202423 PCB contamination occurr during the manufacture of plastics and crop protection products, heat transfer fluids and disposals of crude oil extracts and coal tars. It has been reported that human activities are the reasons for accumulation of PCBs near the shorelines and in water. PCBs bio-accumulate in fish and gets attached strongly to soil and remain there for several years as a result of its lipophilicity. Another possible source of PCB exposure is the workplace, which occurs during the course of maintenance and repair of transformers, accidents, fires and spills. Old appliances and electrical equipments are also believed to be the source of household contamination of PCBs24-29.

Ecosystem Impact

About twenty-nine of PCB congeners are of environmental interest due to their toxicity and have been studied extensively in vitro and in vivo using animal models as well as cell culture models. It has been reported that being a possible mutagen, Biphenyls can impair nervous systems, cause kidney dysfunctions and reduce hemoglobin levels. Lethality, toxicity on reproduction, growth inhibition, induction of enzyme, hepato-toxicity, thymic atrophy, dermal toxicity and other biochemical responses have all been also reported in almost all the multiple PCB studies. Absorption of PCBs by human and animals is done through the skin, the lungs, and the gastrointestinal tract. Once PCBs take entry inside the body, with the help of blood stream they are transported to liver and to different muscles and also to adipose tissues for deposition. Occupational studies also proved for increase rate of cancer mortality in workers who were frequently exposed to PCBs 30-32. PCB deposition effects also studied in case of mass mortality in seabirds. Due to having anti-estrogenic properties PCB can inhibit calcium deposition during egg shell development and that leads to insufficient thickening of the shells and premature loss of the eggs33. PCBs also affect the composition of phytoplankton communities. The PCBs are taking entry to the food chain from phytoplankton to invertebrates, to fishes and to mammals and also contaminate agricultural soils34. Recent studies reveal high percentage of PCBs present in various biota of India which is reported in Table 1.

Table 1. Highlights the various sources and concentration of PCB and its effect on humans

Source of PCB

Types of PCB

PCB concentration (ng?g−1)

Effect on humans

References

Agricultural soil

dominant were PCB 11, 44, 47, 65, 68, and 209

64.3–4358 pg/g

Bioaccumulation through food chain in humans, responsible for cancer

[34]

Agricultural crops

PCB 110, 118, 138, 149, 153 and 180

90.9–234 ng/g

Potent health impacts through consumption of leafy vegetables

[35]

Steel making industry

Variable PCB (POPs) from fly ash and flue gas

Variable concentration

Strong health impacts with respiratory distress due to inhalation

[27]

Household dust (Industrial)

hexa- and hepta-PCBs

19176 ± 1141 ng/g

Hormonal imbalance in body due to pthalates

[25]

Household (ceiling fan dust)

PCB 28,52, 101, 153, 138,180

34.39 ng/g

Risks of cancer through inhalation or direct contact

[29]

Indoor air from school room

Aroclor and non-Aroclor sources from paints, pigments and surface coatings

39.2-124

Usually affects neurodevelopmental changes, inhalation affects respiratory mechanism

[28]

Indoor Dust of Electronic repair workshops

Mixtures of Aroclor 1252, 1254 and/ or 1260.

96.6-3949

Cancer, Liver damage and fatty liver due to phenylated ethers

[26]

Biodegradation Pathways

While the production of PCBs has been banned in industrial countries due to the health hazards, these toxic pollutants are persistent in the environment. Biphenyl degrading microorganisms have been identified as the most useful tool for detoxifying contaminated environments because they are very environment friendly, cost-effective and energy efficient. Two different types of metabolic pathways are established in these types of microbes. They are aerobic pathway and anaerobic pathway, which are regulated by the degree of chlorination of the PCBs, the types of microbes involved and by the soil specific oxygen concentrations36-38.

Anaerobic PCB-dechlorination

PCB congeners containing four or more chlorine substituent undergo anaerobic reductive dechlorination, where PCB serves as the electron accepters for oxidation of organic substrates. Anaerobic bacteria acquire characteristics that are required for high carbon concentration of pollutants. Theoretically, the biological degradation of PCBs produces carbon dioxide, chlorine, and water. This process involves the removal of chlorine from the biphenyl ring followed by cleavage and oxidation of the resulting compound. After formation of chlorinated organic compounds in absence of oxygen during reductive dehalogenation, the halogenated organic compounds serve as the electron acceptor and the halogen substituent is replaced with hydrogen39,40. Thus, anaerobic dechlorination can degrade large number of chlorinated aliphatic and aromatic hydrocarbons. Several types of bacteria are isolated which can perform this kind of biochemical reactions, like Disulfiro bacterium, Dehalobacter restricus, Dehalococcoides ethenogenes and the facultative anaerobes Enterobacter strain MS1 and Enterobacter agglomeraus, Dehalospirillum multivoran, Desulforomanas chloroethenica, Desulfomanile tiedjel41. Most of these bacteria reductively dechlorinate the chlorinated compounds in a co-metabolism reaction and others are able to utilize the chlorinated compounds as electron acceptors by their metabolism. The dechlorination event by these bacteria is manifested in two ways- (a) Less chlorinated congeners are produced as a result of dechlorination and then that can be degraded by indigenous bacteria; (b) Dechlorination greatly reduces bioaccumulation capacity of PCB compounds by production of such congeners that will significantly restrict entry into food chain.

Aerobic PCB-dechlorination

The less chlorinated PCB congeners formed by dechlorination of the higher congeners are utilized as substrates by PCB degrading aerobic bacteria. These less chlorinated PCB congeners are subjected to co-metabolic aerobic oxidation with the help of the enzyme deoxygenase. This enzyme finally opens up ring structure which leads to complete degradation of the molecule. Several studies have revealed different bacterial isolates that can carry on oxidative degradation of PCBs, namely Pseudomonas, Burkholderia, Comamonas, Rhodococcus, and Bacillus etc. PCB congeners with high number of chlorines require reductive dechlorination before starting oxidative mineralization. Aerobic PCB degradation pathway involves two different gene clusters. The first one converts PCB congeners to chlorobenzoic acid and the second one degrades chlorobenzoic acid to other non-toxic products. PCB degrading bacteria commonly require biphenyls or mono-chloro-phenyls as their substrates. In most studied bacteria namely Pseudomonas sp. and Micrococcus sp. a meta ring cleavage product is used to form through 1, 2-dioxygenative ring cleavage; benzoate is produced as a common by-product of biphenyl degradation. Further breakdown of Benzoic acids differs from organisms to organisms with production of less toxic compounds. The complete degradation of PCB requires various microbial strains with specific congener preferences. In addition, the position and number of chlorines on the molecule can impact on the rate of the oxygenase activit 42-45. Apart from this different environmental factor such as temperature, pH and the presence of other substances influence growth of the PCB degrading microorganisms. Therefore, these factors should be standardized to achieve high degradation rate of these PCB degrading microorganisms. The microbial degradation pathway of PCB has been explored in Table 2.

Table 2. Highlights the microbial degradation of PCB and the enzymatic reaction processes

Microbe Type

Name

PCB source

Enzymes involved

Remarks

References

 
 

Bacteria

PGPR bacteria, Rhodococcus sp. (Rhodococcus jostii) and Arthrobacter sp.

Plant-biostimulated soil (SIN Brescia Caffaro) in Italy from Phalaris arundinacea rhizosphere

Expression of bphA gene and emulsification gene

Rhodococcus jostii dominated as PGPR bacteria on Phalaris arundinacea degrading PCB. Genera Gordonia, Arthrobacter and Rhodococcus exhibited emulsifying activity.

[40]

 

Bacteria

Consortium (Achromobacter sp., Ochrobactrum and Lysinibacillus sp.)

Commercially procured Aroclor 1260

-

PCBs degraded (49.2?±?2.5%) by short exposure to anaerobic and aerobic conditions after 2?weeks

[48]

 

Bacteria

Three pseudomonas sp., Burkholderia sp. and Rhodococcus sp.

soil sample

extradiol dioxygenase

All the bacterial strains metabolized monochlorinated biphenyl

[49]

 

Algae

Nostoc sp.

dielectric oil

-

90% PCB removal

[50]

 

Fungus

Penicillium chrysogenu, P. citreosulfuratum, and others

Commercial PCB congeners 28, 52, 101, 118, 138, 153, and 180

laccase and peroxidase

tri- to hexachlorinated PCB efficiently degraded

[51]

 

Fungus

Pleurotus ostreatus and Irpex lacteus

Commercial

Laccase and Manganese peroxidase

PCB degraded

[52]

 

Bacteria

Rhodococcus sp. WAY2

-

bphetb and nah gene clusters

Rhodococcus WAY2 metabolized 23 PCB congeners

[53]

 
  • Indicates no reported source.

BIOREMEDIATION

Phytoremediation and microbe-remediation

In case of plant assisted remediation of PCBs the magic lies in the adsorption and absorption potential of plant roots, the extensive spread of the roots and the enzymatic repertoire of plants roots. Plant roots can also expedite PCBs degradation by enhancing soil porosity and permeability, oxygen transfer capacity and releasing organic exudates, phenolic and surfactants for microbial growth. The process of different bioremediating catabolic routes involve transformation, rhizodegradation or volatilization helps in converting the toxic PCBs into nontoxic intermediate congeners. Various natural and transgenic plant species like Pinus nigra, Salix alaxensis, Alternanthera sessilis, Zea mays, Centinella asiatica, Lathyrus sylvestris, Medicago sativa and Myriophyllum aquaticum have the capability to accumulate PCBs, translocate and degrade in their system. But often the higher molecular weight congeners are hydrophobic in nature making them difficult to be absorbed by plant roots. Biostimulation and Bioaugmentation are the additional processes which help in enhancing microbial degradation by boosting their performances for bioremediation. Thus, PCBs can be degraded by microbe-assisted phytoremediation but each processes have their own challenges and constraints54-58.

CONCLUSION

There are no proper guidelines for controlling PCBs in India, so it becomes quite imperative to formulate specific guide lines for its restricted usage. Public awareness programs especially in rural areas are the urgent need of the hour. More emphasis should be given on cost effective methods of bioremediation like phytoremediation, biostimulation, and bioaugmentation techniques through proper training programs. Instead of diesel pumps, reinforcing the use of solar pumps should be initiated as they contaminate fields by spilling oil and introduce PCBs. Along with it, use of green manure mixed with PCB bio-degrading microorganisms should be encouraged.

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Reference

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Dibyarupa Pal
Corresponding author

Department of Biosciences, JIS University, 81, Nilgunj Rd, Agarpara, Kolkata, West Bengal 700109, India

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Koly Dey
Co-author

Department of Biosciences, JIS University, 81, Nilgunj Rd, Agarpara, Kolkata, West Bengal 700109, India

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Barsha Das
Co-author

Department of Biosciences, JIS University, 81, Nilgunj Rd, Agarpara, Kolkata, West Bengal 700109, India

Koly Dey, Barsha Das, Dibyarupa Pal*, Bioremediation of Polychlorinated Biphenyls- Impact on Ecosystem and Biodegradation Pathways, Int. J. Sci. R. Tech., 2025, 2 (10), 115-123. https://doi.org/10.5281/zenodo.17297622

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