Rhizobia and their bio-partners as novel drivers for functional remediation in contaminated soils

Frontiers in Plant Science

Volumn 6, Issue FEB, 2015, Pages

  Teng, Ying ^a   Wang, Xiaomi ^a   Li, Lina ^a   Li, Zhengao ^a   Luo, Yongming ^b  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b YANTAI INSTITUTE OF COASTAL ZONE RESEARCH   (China)

Author keywords

Bioremediation; Heavy metals; Nitrogen fixation; Organic pollutants; Rhizobia; Rhizospheric degraders; Transgenic rhizobia

Indexed keywords

EID: 84923260976     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00032     Document Type: Review

References (87)

1. Abhilash, P. C., Powell, J. R., Singh, H. B., and Singh, B. K. (2012). Plant-microbe interactions: novel applications for exploitation in multipurpose remediation technologies. Trends Biotechnol. 30, 416-420. doi: 10.1016/j.tibtech.2012.04.004.
2. Ahmad, D., Mehmannavaz, R., and Damaj, M. (1997). Isolation and characterization of symbiotic N2-fixingRhizobium meliloti from soils contaminated with aromatic and chloroaromatic hydrocarbons: PAHs and PCBs. Int. Biodeter. Biodegr. 39, 33-43. doi: 10.1016/S0964-8305(96)00065-0.
3. Aken, B., Van Correa, P. A., and Schnoor, J. L. (2010). Phytoremediation of polychlorinated biphenyls: new trends and promises. Environ. Sci. Technol. 44, 2767-2776. doi: 10.1021/es902514d.
4. Alloway, B. J., and Trevors, J. T. (2013). Heavy Metals in Soils-Trace Metals and Metalloids in Soils and their Bioavailability. New York: Springer Dordrecht Heidelberg.
5. Andeer, P., Stahl, D. A., Lillis, L., and Strand, S. E. (2013). Identification of microbial populations assimilating nitrogen from RDX in munitions contaminated military training range soils by high sensitivity stable isotope probing. Environ. Sci. Technol. 47, 10356-10363. doi: 10.1021/es401729c.
6. Awaya, J. D., Fox, P. M., and Borthakur, D. (2005). pyd Genes of Rhizobium sp. strain TAL1145 are required for degradation of 3-hydroxy-4-pyridone, an aromatic intermediate in mimosine metabolism. J. Bacteriol. 187, 4480-4487. doi: 10.1128/JB.187.13.4480-4487.2005.
7. Becker, A., Bergès, H., Krol, E., Bruand, C., Rüberg, S., Capela, D.,et al. (2004). Global changes in gene expression inSinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Mol. Plant Microbe Interact. 17, 292-303. doi: 10.1094/MPMI.2004.17.3.292.
8. Bright, M., and Bulgheresi, S. (2010). A complex journey: transmission of microbial symbionts. Appl. Soil Ecol. 8, 218-230. doi: 10.1038/nrmicro2262.
9. Camargo, D., Bispo, K. L., and Sene, L. (2011). Association of Rhizobium sp. with two legumes on atrazine tolerance.Rev. Ceres. 58, 425-431. doi: 10.1590/S0034-737X2011000400004.
10. Carrasco, J. A., Armario, P., Pajuelo, E., Burgos, A., Caviedes, M. A., López, R.,et al. (2005). Isolation and characterization of symbiotically effective Rhizobium resistant to arsenic and heavy metals after the toxic spill at the Aznalcollar pyrite mine. Soil Biol. Biochem. 37, 1131-1140. doi: 10.1016/j.soilbio.2004.11.015.
11. Carrasco-Gil, S., Siebner, H., LeDuc, D. L., Webb, S. M., Millaìn, R., Andrews, J. C.,et al. (2013). Mercury localization and speciation in plants grown hydroponically or in a natural environment. Environ. Sci. Technol. 47, 3082-3090. doi: 10.1021/es303310t.
12. Chen, J., Sun, G. X., Wang, X. X., de Lorenzo, V., Rosen, B. P., and Zhu, Y. G. (2014). Volatilization of arsenic from polluted soil by Pseudomonas putida engineered for expression of the arsM arsenic(III) S-adenosine methyltransferase gene. Environ. Sci. Technol. 48, 10337-10344. doi: 10.1021/es502230b.
13. Chen, W. M., Wu, C. H., James, E. K., and Chang, J. S. (2008). Biosorption capability of Cupriavidus taiwanensis and its effects on heavy metal removal by nodulated Mimosa pudica. J. Hazard. Mater. 151, 364-371. doi: 10.1016/j.jhazmat.2007.05.082.
14. Chen, Y. Q., Adam, A., Toure, O., and Dutta, S. K. (2005). Molecular evidence of genetic modification ofSinorhizobium meliloti: enhanced PCB bioremediation. J. Ind. Microbiol. Biotechnol. 32, 561-566. doi: 10.1007/s10295-005-0039-2.
15. Cui, W. T., Gao, C. Y., Fang, P., Lin, G. Q., and Shen, W. B. (2013). Alleviation of cadmium toxicity in Medicago sativa by hydrogen-rich water. J. Hazard. Mater. 260, 715-724. doi: 10.1016/j.jhazmat.2013.06.032.
16. DalCorso, G., Fasani, E., and Furini, A. (2013). Recent advances in the analysis of metal hyperaccumulation and hypertolerance in plants using proteomics. Front. Plant Sci. 4:280. doi: 10.3389/fpls.2013.00280.
17. Damaj, M., and Ahmad, D. (1996). Biodegradation of polychlorinated biphenyls by rhizobia: a novel finding.Biochem. Bioph. Res. Commun. 218, 908-915. doi: 10.1006/bbrc.1996.0161.
18. Dashti, N., Khanafer, M., El-Nemr, I., Sorkhoh, N., Ali, N., and Radwan, S. (2010). The potential of oil-utilizing bacterial consortia associated with legume root nodules for cleaning oily soils. Chemosphere 74, 1354-1359. doi: 10.1016/j.Chemosphere.2008.11.028.
19. De, S., Perkins, M., and Dutta, S. K. (2006). Nitrate reductase gene involvement in hexachlorobiphenyl dechlorination by Phanerochaete chrysosporium. J. Hazard. Mater. 135, 350-354. doi: 10.1016/j.jhazmat.2005.11.073.
20. Deakin, W. J., and Broughton, W. J. (2009). Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Appl. Soil Ecol. 7, 312-320. doi: 10.1038/nrmicro2091.
21. de-Bashan, L. E., Hernandez, J. P., and Bashan, Y. (2011). The potential contribution of plant growth-promoting bacteria to reduce environmental degradation-a comprehensive evaluation. Appl. Soil Ecol. 61, 171-189. doi: 10.1016/j.apsoil.2011.09.003.
22. Donelly, P. K., Hedge, R. S., and Fletcher, J. S. (1994). Growth of PCB-degrading bacteria on compounds from photosynthetic plants. Chemosphere 28, 981-988. doi: 10.1016/0045-6535(94)90014-0.
23. Fan, S. X., Li, P. J., Gong, Z. Q., Ren, W. X., and He, N. (2008). Promotion of pyrene degradation in rhizosphere of alfalfa (Medicago sativa L.). Chemosphere 71, 1593-1598. doi: 10.1016/j.Chemosphere.2007.10.068.
24. Feng, L., Van Zwieten, I., Kennedy, I. R., Rolfe, B. G., and Gartner, E. (1994). Expression of the 2,4-D degrading plasmid pJP4 of Alcaligenes eutrophus in Rhizobium trifolii. Acta Biotechnol. 14, 119-129. doi: 10.1002/abio.370140202.
25. Fester, T., Giebler, J., Wick, L. Y., Schlosser, D., and Kästner, M. (2014). Plant-microbe interactions as drivers of ecosystem functions relevant for the biodegradation of organic contaminants. Curr. Opin. Biotech. 27, 168-175. doi: 10.1016/j.copbio.2014.01.017.
26. Glick, B. R. (2010). Using soil bacteria to facilitate phytoremediation. Biotechnol. Adv. 28, 367-374. doi: 10.1016/j.biotechadv.2010.02.001.
27. Guo, J. K., and Chi, J. (2014). Effect of Cd-tolerant plant growth-promoting rhizobium on plant growth and Cd uptake by Lolium multiflorum Lam. and Glycine max (L.) Merr. in Cd-contaminated soil. Plant Soil 375, 205-214. doi: 10.1007/s11104-013-1952-1.
28. Hamdi, H., Benzarti, S., Aoyama, I., and Jedidi, N. (2012). Rehabilitation of degraded soils containing aged PAHs based on phytoremediation with alfalfa (Medicago sativa L.). Int. Biodeter. Biodegr. 67, 40-47. doi: 10.1016/j.ibiod.2011.10.009.
29. Hao, X. L., Lin, Y. B., Johnstone, L., Baltrus, D. A., Miller, S. J., Wei, G. W.,et al. (2012). Draft genome sequence of plant growth-promoting rhizobium Mesorhizobium amorphae, isolated from zinc-lead mine tailings. J. Bacteriol.194, 736-737. doi: 10.1128/JB.06475-11.
30. Hao, X., Taghavi, S., Xie, P., Orbach, M. J., Alwathnani, H. A., Rensing, C.,et al. (2014). Phytoremediation of heavy and transition metals aided by legume-rhizobia symbiosis. Int. J. Phytoremediat. 16, 179-202. doi: 10.1080/15226514.2013.773273.
31. Harms, H., Schlosser, D., and Wick, L. Y. (2011). Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat. Rev. 9, 177-192. doi: 10.1038/nrmicro2519.
32. Hussien, Y. A., Tewfik, M. S., and Hamdi, Y. A. (1974). Degradation of certain aromatic compounds by rhizobia. Soil Biol. Biochem. 6, 377-381. doi: 10.1016/0038-0717(74)90047-9.
33. Ike, A., Sriprang, R., Ono, H., Murooka, Y., and Yamashita, M. (2007). Bioremediation of cadmium contaminated soil using symbiosis between leguminous plant and recombinant rhizobia with the MTL4 and the PCS genes.Chemosphere 66, 1670-1676. doi: 10.1016/j.Chemosphere.2006.07.058.
34. Jabeen, H., Iqbal, S., and Anwar, S. (2014). Biodegradation of chlorpyrifos and 3, 5, 6-trichloro-2-pyridinol by a novel rhizobial strain Mesorhizobium sp. HN3. Water Environ. J. doi: 10.1111/wej.12081.
35. Jin, Q. J., Zhu, K. K., Cui, W. T., Xie, Y. J., Han, B., and Shen, W. B. (2013). Hydrogen gas acts as a novel bioactive molecule in enhancing plant tolerance to paraquat-induced oxidative stress via the modulation of heme oxygenase-1 signalling system. Plant Cell Environ. 36, 956-969. doi: 10.1111/pce.12029.
36. Johnson, D., Anderson, D., and McGrath, S. (2005). Soil microbial response during the phytoremediation of a PAH contaminated soil. Soil Biol. Biochem. 37, 2334-2336. doi: 10.1016/j.soilbio.2005.04.001.
37. Johnson, D. L., Maguire, K. L., Anderson, D. R., and McGrath, S. P. (2004). Enhanced dissipation of chrysene in planted soil: the impact of a rhizobial inoculum. Soil Biol. Biochem. 36, 33-38. doi: 10.1016/j.soilbio.2003.07.004.
38. Kaiya, S., Utsunomiya, S., Suzuki, S., Yoshida, N., Futamata, H., Yamada, T.,et al. (2012). Isolation and functional gene analyses of aromatic-hydrocarbon-degrading bacteria from a polychlorinated-dioxin-dechlorinating process.Microbes Environ. 27, 127-135. doi: 10.1264/jsme2.ME11283.
39. Keum, Y. S., Seo, J. S., Hu, Y. T., and Li, Q. X. (2006). Degradation pathways of phenanthrene by Sinorhizobium sp.C4. Appl. Microbiol. Biotechnol. 71, 935-941. doi: 10.1007/s00253-005-0219-z.
40. Kinkle, B. K., Sadowsky, M. J., Schmidt, E. L., and Koskinen, W. C. (1993). Plasmids pJP4 and r68.45 can be transferred between populations of bradyrhizobia in nonsterile soil. Appl. Environ. Microbiol. 59, 1762-1766.
41. Larimer, A. L., Bever, J. D., and Clay, K. (2012). Consequences of simultaneous interactions of fungal endophytes and arbuscular mycorrhizal fungi with a shared host grass. Oikos 121, 2090-2096. doi: 10.1111/j.1600-0706.2012.20153.x.
42. Leigh, J. A., Skinner, A. J., and Cooper, R. A. (1988). Partial purification, stereospecificity and stoichiometry of three dehalogenases from a Rhizobium species. FEMS Microbiol. Lett. 49, 353-356. doi: 10.1111/j.1574-6968.1988.tb02756.x.
43. Li, H. Y., Wei, D. Q., Shen, M., and Zhou, Z. P. (2012). Endophytes and their role in phytoremediation. Fungal Divers. 54, 11-18. doi: 10.1007/s13225-012-0165-x.
44. Li, Y., Liang, F., Zhu, Y. F., and Wang, F. P. (2013). Phytoremediation of a PCB-contaminated soil by alfalfa and tall fescue single and mixed plants cultivation. J. Soil. Sediment. 13, 925-931. doi: 10.1007/s11368-012-0618-6.
45. Lohmann, R., Breivik, K., Dachs, J., and Muir, D. (2007). Global fate of POPs: current and future esearch directions.Environ. Pollut. 150, 150-165. doi: 10.1016/j.envpol.2007.06.051.
46. Magee, K. D., Michael, A., Ullah, H., and Dutta, S. K. (2008). Dechlorination of PCB in the presence of plant nitrate reductase. Environ. Toxicol. Pharmacol. 25, 144-147. doi: 10.1016/j.etap.2007.10.009.
47. Maynaud, G., Brunel, B., Mornico, D., Durot, M., Severac, D., Dubois, E.,et al. (2013). Genome-wide transcriptional responses of two metal-tolerant symbiotic Mesorhizobium isolates to zinc and cadmium exposure. BMC Genomics14:292. doi: 10.1186/1471-2164-14-292.
48. Mehmannavaza, R., Prasher, S. O., and 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. doi: 10.1016/S0032-9592(01)00305-3.
49. Moreto, M., Silvestri, S., Ugo, P., Zorzi, G., Abbodanzi, F., Baiocchi, C.,et al. (2005). Polycyclic aromatic hydrocarbons degradation by composting in a soot contaminated alkaline soil. J. Hazard. Mater. 26, 141-148. doi: 10.1016/j.jhazmat.2005.06.020.
50. Morris, R. L., and Schmidt, T. M. (2013). Shallow breathing: bacterial life at low O2. Appl. Soil Ecol. 2013, 11, 205-212. doi: 10.1038/nrmicro2970.
51. Muthukumar, G., Arunakumari, A., and Mahadevan, A. (1982). Degradation of aromatic compounds by Rhizobiumspp. Plant Soil 69, 163-169. doi: 10.1007/BF02374511.
52. Nies, D. H. (1995). The cobalt, zinc, and cadmium efflux system CzcABC from Alcaligenes eutrophus functions as a cation-proton antiporter in Escherichia coli. J. Bacteriol. 177, 2707-2712.
53. Nies, D. H. (2003). Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol. Rev. 27, 313-339. doi: 10.1016/S0168-6445(03)00048-2.
54. O'Hara, G. W., Daniel, R. M., and Steele, K. W. (1983). Effect of oxygen on the synthesis, activity and breakdown of the Rhizobium denitrification system. J. Gen. Microbiol. 129, 2405-2412. doi: 10.1099/00221287-129-8-2405.
55. Parke, D., Rivelli, M., and Ornston, L. N. (1985). Chemotaxis to aromatic and hydroaromatic acids: comparison ofBradyrhizobium japonicum and Rhizobium trifolii. J. Bacteriol. 163, 417-422.
56. Passatore, L., Rossetti, S., Juwarkar, A. A., and Massacci, A. (2014). Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): state of knowledge and research perspectives. J. Hazard. Mater. 278, 189-202. doi: 10.1016/j.jhazmat.2014.05.051.
57. Pereira, S. I. A., Lima, A. I. G., Figueira, E. M., and de Almeida, P. F. (2006). Heavy metal toxicity in Rhizobium leguminosarum biovar viciae isolated from soils subjected to different sources of heavy-metal contamination: effects on protein expression. Appl. Soil Ecol. 33, 286-293. doi: 10.1016/j.apsoil.2005.10.002.
58. Poonthrigpun, S., Pattaragulwanit, K., Paengthai, S., Kriangkripipat, T., Juntongjin, K., Thaniyavarn, S.,et al. (2006). Novel intermediates of acenaphthylene degradation by Rhizobium sp. strain CU-A1: evidence for naphthalene-1,8-dicarboxylic acid metabolism. Appl. Environ. Microbiol. 72, 6034-6039. doi: 10.1128/AEM.00897-06.
59. Prell, J., and Poole, P. (2006). Metabolic changes of rhizobia in legume nodules. Trends Biotechnol. 14, 161-168. doi: 10.1016/j.tim.2006.02.005.
60. Rajkumar, M., Sandhya, S., Prasad, M. N. V., and Freitas, H. (2012). Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol. Adv. 30, 1562-1574. doi: 10.1016/j.biotechadv.2012.04.011.
61. Saini, V. K., Bhandari, S. C., and Tarafdar, J. C. (2004). Comparison of crop yield, soil microbial C, N and P, N-fixation, nodulation and mycorrhizal infection in inoculated and non-inoculated sorghum and chickpea crops. Field Crop. Res. 89, 39-47. doi: 10.1016/j.fcr.2004.01.013.
62. Sato, Y., Monincová, M., Chaloupková, R., Prokop, Z., Ohtsubo, Y., Minamisawa, K.,et al. (2005). Two rhizobial strains, Mesorhizobium loti MAFF303099 and Bradyrhizobium japonicum USDA110, encode haloalkane dehalogenases with novel structures and substrate specificities. Appl. Environ. Microb. 71, 4372-4379. doi: 10.1128/AEM.71.8.4372-4379.2005.
63. Schalk, I. J., Hannauer, M., and Braud, A. (2011). New roles for bacterial siderophores in metal transport and tolerance. Environ. Microbiol. 13, 2844-2854. doi: 10.1111/j.1462-2920.2011.02556.x.
64. Segura, A., and Ramos, J. L. (2013). Plant-bacteria interactions in the removal of pollutants. Curr. Opin. Biotech.24, 467-473. doi: 10.1016/j.copbio.2012.09.011.
65. Segura, A., Rodríguez-Conde, S., Ramos, C., and Ramos, J. L. (2009). Bacterial responses and interactions with plants during rhizoremediation. Microb. Biotechnol. 2, 452-464. doi: 10.1111/j.1751-7915.2009.00113.x.
66. Smith, S. R., and Giller, K. E. (1992). Effective Rhizobium leguminosarum biovar trifolii present in five soils contaminated with heavy metals from long-term applications of sewage sludge or metal mine spoil. Soil Biol. Biochem. 24, 781-788. doi: 10.1016/0038-0717(92)90253-T.
67. Soedarjo, M., and Borthakur, D. (1998). Mimosine, a toxin produced by the tree-legume Leucaena provides a nodulation competition advantage to mimosine-degrading Rhizobium strains. Soil Biol. Biochem. 30, 1605-1613. doi: 10.1016/S0038-0717(97)00180-6.
68. Soedarjo, M., Hemscheidt, T. K., and Borthakur, D. (1995). Mimosine, a toxin present in leguminous trees (Leucaena spp.), induces a mimosine-degrading enzyme activity in some strains of Rhizobium. Appl. Environ. Microbiol. 60, 4268-4272.
69. Souza, M. P., Amini, A., Dojka, M. A., Pickering, I. J., Dawson, S. C., Pace, N. R.,et al. (2001). Identification and characterization of bacteria in a selenium-contaminated hypersaline evaporation pond. Appl. Environ. Microbiol.67, 3785-3794. doi: 10.1128/AEM.67.9.3785-3794.2001.
70. Sriprang, R., Hayashi, M., Yamashita, M., Ono, H., Saeki, K., and Murooka, Y. (2002). A novel bioremediation system for heavy metals using the symbiosis between leguminous plant and genetically engineered rhizobia. J. Biotechnol. 99, 279-293. doi: 10.1016/S0168-1656(02)00219-5.
71. Streeter, J. G., and DeVine, P. J. (1983). Evaluation of nitrate reductase activity in Rhizobium japonicum. Appl. Environ. Microbiol. 46, 521-524. doi: 10.1038/nrmicro2970.
72. Stringfellow, J. M., Cairns, S. S., Cornish, A., and Cooper, R. A. (1997). Haloalkanoate dehalogenase I1 (DehE) of aRhizobium sp. molecular analysis of the gene and formation of carbon monoxide from trihaloacetate by the enzyme. Eur. J. Biochem. 250, 789-793. doi: 10.1111/j.1432-1033.1997.00789.x.
73. Sun, M. M., Fu, D. Q., Teng, T., Shen, Y. Y., Luo, Y. M., Li, Z. G.,et al. (2011a). In situ phytoremediation of PAH-contaminated soil by intercropping alfalfa (Medicago sativa L.) with tall fescue (Festuca arundinacea Schreb.) and associated soil microbial activity. J. Soil. Sediment. 11, 980-989. doi: 10.1007/s11368-011-0382-z.
74. Sun, X. H., Teng, Y., Luo, Y. M., Tu, C., and Li, Z. G. (2011b). Accumulation, distribution and chemical speciation of PCBs in different parts of alfalfa. Soils 43, 595-599.
75. Teng, Y., Luo, Y., Sun, X., Tu, C., Xu, L., Liu, W.,et al. (2010). Influence of arbuscular mycorrhiza and Rhizobium on phytoremediation by alfalfa of an agricultural soil contaminated with weathered PCBs: a field study. Int. J. Phytoremediation 12, 516-533. doi: 10.1080/15226510903353120.
76. Teng, Y., Shen, Y. Y., Luo, Y. M., Sun, X. H., Sun, M. M., Fu, D. Q.,et al. (2011). Influence of Rhizobium meliloti on phytoremediation of polycyclic aromatic hydrocarbons by alfalfa in an aged contaminated soil. J. Hazard. Mater.186, 1271-1276. doi: 10.1016/j.jhazmat.2010.11.126.
77. Teng, Y., Xu, Z. H., Luo, Y. M., and Reverchon, F. (2012). How do persistent organic pollutants be coupled with biogeochemical cycles of carbon and nutrients in terrestrial ecosystems under global climate change? J. Soil. Sediment. 12, 411-419. doi: 10.1007/s11368-011-0462-0.
78. N] DNA-based stable isotope probing and pyrosequencing. Appl. Environ. Microbiol. 77, 4163-4171. doi: 10.1128/AEM.00172-11.
79. Tu, C., Teng, Y., Luo, Y. M., Li, X. H., Sun, X. H., Li, Z. G., et al., (2011). Potential for biodegradation of polychlorinated biphenyls (PCBs) by Sinorhizobium meliloti. J. Hazard. Mater. 186, 1438-1444. doi: 10.1016/j.jhazmat.2010.12.008.
80. Valentín, L., Nousiainen, A., and Mikkonen, A. (2013). "Introduction to organic contaminants in soil: concepts and risks," in Emerging Organic Contaminants in Sludges: The Handbook of Environmental Chemistry, eds A. G. Kostianoy and D. Barceló (Berlin, Heidelberg: Springer-Verlag), 1-29.
81. Wang, X. M., Yang, B., Ren, C, G., Wang, H. W., Wang, J. Y., and Dai, C. C. (2015). Involvement of abscisic acid and salicylic acid in signal cascade regulating bacterial endophyte-induced volatile oil biosynthesis in plantlets ofAtractylodes lancea. Physiol. Plant. 153, 30-42. doi: 10.1111/ppl.12236.
82. Wani, P. A., Khan, M. S., and Zaidi, A. (2007). Effect of metal tolerant plant growth promoting Bradyrhizobium sp.(vigna) on growth, symbiosis, seed yield, and metal uptake by greengram plants. Chemosphere 70, 36-45. doi: 10.1007/s00244-007-9097-y.
83. Xu, L., Teng, T., Luo, Y. M., and Li, Z. G. (2010). Effects of Rhizobium meliloti on PCBs degradation and transformation in solution culture. Environ. Sci. 31, 255-259.
84. Xu, L., Teng, Y., Li, Z. G., Norton, J. M., and Luo, Y. M. (2008). Enhanced removal of polychlorinated biphenyls from alfalfa rhizosphere soil in a field study: the impact of a rhizobial inoculum. Sci. Total Environ. 408, 1007-1013. doi: 10.1016/j.scitotenv.2009.11.031.
85. Yang, H. C., Cheng, J. J., Finan, T. M., Rosen, B. P., and Bhattacharjee, H. (2005). Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J. Bacteriol. 187, 6991-6997. doi: 10.1128/JB.187.20.6991-6997.2005.
86. Zhang, W. W., Chen, L. X., and Liu, D. Y. (2012). Characterization of a marine-isolated mercury-resistantPseudomonas putida strain SP1 and its potential application in marine mercury reduction. Appl. Microbiol. Biotechnol. 93, 1305-1314. doi: 10.1007/s00253-011-3454-5.
87. Zinjarde, S., Apte, M., Mohite, P., and Kumar, A. R. (2014). Yarrowia lipolytica and pollutants: interactions and applications. Biotechnol. Adv. 32, 920-933. doi: 10.1016/j.biotechadv.2014.04.008.