Science China Earth Sciences

, Volume 61, Issue 3, pp 285–291 | Cite as

Reductive dechlorination of polychlorinated biphenyls is coupled to nitrogen fixation by a legume-rhizobium symbiosis

  • Chen Tu
  • YongMing LuoEmail author
  • Ying Teng
  • Peter Christie
Research Paper


Chlorinated persistent organic pollutants, including polychlorinated biphenyls (PCBs), represent a particularly serious environmental problem and human health risk worldwide. Leguminous plants and their symbiotic bacteria (rhizobia) are important components of the biogeochemical cycling of nitrogen in both agricultural and natural ecosystems. However, there have been relatively few detailed studies of the remediation of PCB-contaminated soils by legume-rhizobia symbionts. Here we report for the first time evidence of the reductive dechlorination of 2,4,4′-trichlorobiphenyl (PCB 28) by an alfalfa-rhizobium nitrogen fixing symbiont. Alfalfa (Medicago sativa L.) inoculated with wild-type Sinorhizobium meliloti had significantly larger biomass and PCB 28 accumulation than alfalfa inoculated with the nitrogenase negative mutant rhizobium SmY. Dechlorination products of PCB 28, 2,4′-dichlorobiphenyl (PCB 8), and the emission of chloride ion (Cl−) were also found to decrease significantly in the ineffective nodules infected by the mutant strain SmY. We therefore hypothesize that N2-fixation by the legume-rhizobium symbiont is coupled with the reductive dechlorination of PCBs within the nodules. The combination of these two processes is of great importance to the biogeochemical cycling and bioremediation of organochlorine pollutants in terrestrial ecosystems.


Biogeochemical cycling Legume-rhizobia symbiosis Microbe-assisted phytoremediation Nitrogen fixation Polychlorinated biphenyls Soil pollution and remediation Reductive dechlorination 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.



The authors thank Prof. Yu G Q for kindly providing S. meliloti wild-type and SmY mutant strains. This work was supported by the National Natural Science Foundation of China (Grant Nos. 41201313 & 41230858).


  1. Ahmad D, Mehmannavaz R, Damaj M. 1997. Isolation and characterization of symbiotic N2-fixing Rhizobium meliloti from soils contaminated with aromatic and chloroaromatic hydrocarbons: PAHs and PCBs. Int Biodeter Biodegr, 39: 33–43CrossRefGoogle Scholar
  2. Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert J V, Vangronsveld J, van der Lelie D. 2004. Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nat Biotechnol, 22: 583–588CrossRefGoogle Scholar
  3. Barbour J P, Smith J A, Chiou C T. 2005. Sorption of aromatic organic pollutants to grasses from water. Environ Sci Technol, 39: 8369–8373CrossRefGoogle Scholar
  4. Becerra-Castro C, Prieto-Fernández Á, Kidd P S, Weyens N, Rodríguez-Garrido B, Touceda-González M, Acea M J, 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: 247–260CrossRefGoogle Scholar
  5. Borja J, Taleon D M, Auresenia J, Gallardo S. 2005. Polychlorinated biphenyls and their biodegradation. Process Biochem, 40: 1999–2013CrossRefGoogle Scholar
  6. Chekol T, Vough L R. 2001. A study of the use of alfalfa (Medicago sativa L.) for the phytoremediation of organic contaminants in soil. Remediation, 11: 89–101CrossRefGoogle Scholar
  7. Chen Y, Adam A, Toure O, Dutta S K. 2005. Molecular evidence of genetic modification of Sinorhizobium meliloti: Enhanced PCB bioremediation. J Ind Microbiol Biotechnol, 32: 561–566CrossRefGoogle Scholar
  8. Dercová K, Čičmanová J, Lovecká P, Demnerová K, Macková M, Hucko P, Kušnír P. 2008. Isolation and identification of PCB-degrading microorganisms from contaminated sediments. Int Biodeter Biodegr, 62: 219–225CrossRefGoogle Scholar
  9. Gao J, Luo Y M, Li Q B, Zhang H B, Wu L H, Song J, Qian W, Christie P, Chen S M. 2006. Distribution patterns of polychlorinated biphenyls in soils collected from Zhejiang province, east China. Environ Geochem Health, 28: 79–87CrossRefGoogle Scholar
  10. Hussien Y A, Tewfik M S, Hamdi Y A. 1974. Degradation of certain aromatic compounds by rhizobia. Soil Biol Biochem, 6: 377–381CrossRefGoogle Scholar
  11. Keum Y S, Seo J S, Hu Y, Li Q X. 2006. Degradation pathways of phenanthrene by Sinorhizobium sp. C4. Appl Microbiol Biotechnol, 71: 935–941CrossRefGoogle Scholar
  12. Kurzawova V, Stursa P, Uhlik O, Norkova K, Strohalm M, Lipov J, Kochankova L, Mackova M. 2012. Plant-microorganism interactions in bioremediation of polychlorinated biphenyl-contaminated soil. New Biotech, 30: 15–22CrossRefGoogle Scholar
  13. Kuzma M M, Hunt S, Layzell D B. 1993. Role of oxygen in the limitation and inhibition of nitrogenase activity and respiration rate in individual soybean nodules. Plant Physiol, 101: 161–169CrossRefGoogle Scholar
  14. Leigh M B, Prouzová P, Macková M, Macek T, Nagle D P, Fletcher J S. 2006. Polychlorinated biphenyl (PCB)-degrading bacteria associated with trees in a PCB-contaminated site. Appl Environ Microbiol, 72: 2331–2342CrossRefGoogle Scholar
  15. Liu J Y, Hu D F, Jiang G B, Schnoor J L. 2009. In vivo Biotransformation of 3,3′,4,4′-Tetrachlorobiphenyl by Whole Plants-Poplars and Switchgrass. Environ Sci Technol, 43: 7503–7509CrossRefGoogle Scholar
  16. Luo Y M. 2016. Remediation Mechanism and Technological Development of Toxic Organic Substance Polluted Soil (in Chinese). Beijing: Science Press. 1–80Google Scholar
  17. Macek T, Macková M, Káš J. 2000. Exploitation of plants for the removal of organics in environmental remediation. Biotech Adv, 18: 23–34CrossRefGoogle Scholar
  18. Magee K D, Michael A, Ullah H, Dutta S K. 2008. Dechlorination of PCB in the presence of plant nitrate reductase. Environ Toxicol Pharmacology, 25: 144–147CrossRefGoogle Scholar
  19. Marx J. 2004. The roots of plant-microbe collaborations. Science, 304: 234–236CrossRefGoogle Scholar
  20. Mehmannavaz R, Prasher S O, Ahmad D. 2002. Rhizospheric effects of alfalfa on biotransformation of polychlorinated biphenyls in a contaminated soil augmented with Sinorhizobium meliloti. Process Biochem, 37: 955–963CrossRefGoogle Scholar
  21. Meggo R E, Schnoor J L, Hu D. 2013. Dechlorination of PCBs in the rhizosphere of switchgrass and poplar. Environ Pollut, 178: 312–321CrossRefGoogle Scholar
  22. Passatore L, Rossetti S, Juwarkar A A, Massacci A. 2014. Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): State of knowledge and research perspectives. J Hazard Mater, 278: 189–202CrossRefGoogle Scholar
  23. Poonthrigpun S, Pattaragulwanit K, Paengthai S, Kriangkripipat T, Juntongjin K, Thaniyavarn S, Petsom A, Pinphanichakarn P. 2006. Novel intermediates of acenaphthylene degradation by Rhizobium sp. strain CU-A1: Evidence for naphthalene-1,8-dicarboxylic acid metabolism. Appl Environ Microbiol, 72: 6034–6039CrossRefGoogle Scholar
  24. Ramos J, Bisseling T. 2004. Symbiotic nitrogen fixation. In: Amâncio S, Stulen I, eds. Nitrogen Acquisition and Assimilation in Higher Pants. The Netherland: Kluwer Academic Publishers. 99–131Google Scholar
  25. Reid B, Nuccitelli R, Zhao M. 2007. Non-invasive measurement of bioelectric currents with a vibrating probe. Nat Protoc, 2: 661–669CrossRefGoogle Scholar
  26. Schnoor J L, Licht L A, McCutcheon S C, Wolfe N L, Carreira L H. 1995. Phytoremediation of organic and nutrient contaminants. Environ Sci Technol, 29: 318A–323ACrossRefGoogle Scholar
  27. Sun J, Chen S, Dai S, Wang R, Li N, Shen X, Zhou X, Lu C, Zheng X, Hu Z, Zhang Z, Song J, Xu Y. 2009. NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt-sensitive poplar species. Plant Physiol, 149: 1141–1153CrossRefGoogle Scholar
  28. Sun X H, Teng Y, Luo Y M, Tu C, Li Z G. 2011. Accumulation, distribution and chemical speciation of PCBs in different parts of alfalfa (in Chinese). Soils, 43: 595–599Google Scholar
  29. Teng Y, Wang X M, Li L N, Li Z G, Luo Y M. 2015. Rhizobia and their bio-partners as novel drivers for functional remediation in contaminated soils. Front Plant Sci, 6: 32CrossRefGoogle Scholar
  30. Teng Y, Luo Y M, Sun X H, Tu C, Xu L, Liu W X, Li Z G, Christie P. 2010. Influence of arbuscular mycorrhiza andrhizobium on phytoremediation by alfalfa of an agricultural soil contaminated with weathered PCBs: A field study. Int J Phytoremediat, 12: 516–533CrossRefGoogle Scholar
  31. Thijs S, Sillen W, Rineau F, Weyens N, Vangronsveld J. 2016. Towards an enhanced understanding of plant-microbiome interactions to improve phytoremediation: Engineering the metaorganism. Front Microbiol, 7Google Scholar
  32. Tu C, Teng Y, Luo Y M, Li X H, Sun X H, Li Z G, Liu W X, Christie P. 2011. Potential for biodegradation of polychlorinated biphenyls (PCBs) by Sinorhizobium meliloti. J Hazard Mater, 186: 1438–1444CrossRefGoogle Scholar
  33. Van Aken B, Correa P A, Schnoor J L. 2010. Phytoremediation of Polychlorinated Biphenyls: New Trends and Promises†. Environ Sci Technol, 44: 2767–2776CrossRefGoogle Scholar
  34. Wang S, Chng K R, Wilm A, Zhao S, Yang K L, Nagarajan N, He J. 2014. Genomic characterization of three unique Dehalococcoides that respire on persistent polychlorinated biphenyls. Proc Natl Acad Sci USA, 111: 12103–12108CrossRefGoogle Scholar
  35. Wang X M, Teng Y, Luo Y M, Dick R P. 2016. Biodegradation of 3,3′,4,4′- tetrachlorobiphenyl by Sinorhizobium meliloti NM. Bioresource Tech, 201: 261–268CrossRefGoogle Scholar
  36. Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J. 2009. Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotech, 27: 591–598CrossRefGoogle Scholar
  37. Wiegel J, Wu Q. 2000. Microbial reductive dehalogenation of polychlorinated biphenyls. Fems Microbiol Ecology, 32: 1–15CrossRefGoogle Scholar
  38. Xu L, Teng Y, Li Z G, Norton J M, Luo Y M. 2010. Enhanced removal of polychlorinated biphenyls from alfalfa rhizosphere soil in a field study: The impact of a rhizobial inoculum. Sci Total Environ, 408: 1007–1013CrossRefGoogle Scholar
  39. Xu Y, Sun T, Yin L P. 2006. Application of non-invasive microsensing system to simultaneously measure both H+ and O2 fluxes around the pollen tube. J Integrative Plant Biol, 48: 823–831CrossRefGoogle Scholar
  40. Yang C T, Yu G Q, Shen S J, Zhu J B. 2004. Functional difference between Sinorhizobium meliloti NifA and Enterobacter cloacae NifA. Sci China Ser C-Life Sci, 47: 44–51CrossRefGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Chen Tu
    • 1
  • YongMing Luo
    • 1
    • 2
    Email author
  • Ying Teng
    • 2
  • Peter Christie
    • 2
  1. 1.Key Laboratory of Coastal Environmental Processes and Ecological Remediation, Yantai Institute of Coastal Zone ResearchChinese Academy of SciencesYantaiChina
  2. 2.Key Laboratory of Soil Environment and Pollution Remediation, Institute of Soil ScienceChinese Academy of SciencesNanjingChina

Personalised recommendations