Effect of genetically modified poplars on soil microbial communities during the phytoremediation of waste mine tailings

Applied and Environmental Microbiology

Volumn 77, Issue 21, 2011, Pages 7611-7619

  Hur, Moonsuk ^a   Kim, Yongho ^a   Song, Hae Ryong ^a   Kim, Jong Min ^a   Choi, Young Im ^b   Yi, Hana ^c  

^a National Institute of Environmental Research   (South Korea)

^b Korea Forest Research Institute   (South Korea)

^c Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEAL; CLEAN UP; COMPARATIVE ANALYSIS; CONTAMINATED SOILS; DIRECTIONAL CHANGES; ENVIRONMENTAL POLLUTIONS; GENETICALLY MODIFIED; GENETICALLY MODIFIED ORGANISMS; GROWTH STAGES; METAL ACCUMULATION; METAL MINING; METAL POLLUTANTS; MICROBIAL COMMUNITIES; MICROBIAL COMMUNITY STRUCTURES; MINE TAILINGS; NATURALLY OCCURRING; PHYTOREMEDIATION; PYROSEQUENCING; RATE OF CHANGE; SOIL ENVIRONMENT; SOIL MICROBIAL COMMUNITY; TRANSGENIC PLANTS; WILD TYPES;

BIOREMEDIATION; GENETICALLY MODIFIED PLANTS; HEAVY METALS; MICROORGANISMS; SOIL POLLUTION CONTROL; SOILS; TAILINGS;

SOIL POLLUTION;

ARCHAEAL DNA; ARCHAEAL RNA; BACTERIAL DNA; BACTERIAL RNA; RIBOSOME DNA; RNA 16S;

BIOACCUMULATION; CLEANUP; COMMUNITY STRUCTURE; GENETICALLY MODIFIED ORGANISM; HEAVY METAL; MICROBIAL COMMUNITY; MINE WASTE; PHYTOREMEDIATION; RHIZOSPHERE; SOIL MICROORGANISM; SOIL POLLUTION; TAILINGS;

ARCHAEBACTERIUM; ARTICLE; ASPEN; BACTERIUM; BIODIVERSITY; BIOREMEDIATION; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PHYLOGENY; RHIZOSPHERE; RNA GENE; SEQUENCE HOMOLOGY; TRANSGENIC ORGANISM;

ARCHAEA; BACTERIA; BIODEGRADATION, ENVIRONMENTAL; BIODIVERSITY; CLUSTER ANALYSIS; DNA, ARCHAEAL; DNA, BACTERIAL; DNA, RIBOSOMAL; GENES, RRNA; ORGANISMS, GENETICALLY MODIFIED; PHYLOGENY; POPULUS; RHIZOSPHERE; RNA, ARCHAEAL; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; SOIL MICROBIOLOGY;

EID: 83155185433     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.06102-11     Document Type: Article

References (74)

1. Bittsanszky, A., et al. 2005. Ability of transgenic poplars with elevated glutathione content to tolerate zinc(2+) stress. Environ. Int. 31:251-254.
2. Bruce, N. C., et al. 2007. Impact of transgenic tobacco on trinitrotoluene (TNT) contaminated soil community. Environ. Sci. Technol. 41:5854-5861.
3. Bryan, G. W. 1971. The effects of heavy metals (other than mercury) on marine and estuarine organisms. Proc. R. Soc. Lond. B Biol. Sci. 177:389-410.
4. Cadillo-Quiroz, H., E. Yashiro, J. B. Yavitt, and S. H. Zinder. 2008. Characterization of the archaeal community in a minerotrophic fen and terminal restriction fragment length polymorphism-directed isolation of a novel hydrogenotrophic methanogen. Appl. Environ. Microbiol. 74:2059-2068.
5. Che, D., et al. 2003. Expression of mercuric ion reductase in Eastern cottonwood (Populus deltoides) confers mercuric ion reduction and resistance. Plant Biotechnol. J. 1:311-319.
6. Cherian, S., and M. M. Oliveira. 2005. Transgenic plants in phytoremediation: recent advances and new possibilities. Environ. Sci. Technol. 39:9377-9390.
7. Chun, J., et al. 2007. EzTaxon: a web-based tool for the identification of prokaryotes based on 16S rRNA gene sequences. Int. J. Syst. Evol. Microbiol. 57:2259-2261.
8. Clarke, K. R., and R. M. Warwick. 2001. A further biodiversity index applicable to species lists: variation in taxonomic distinctness. Mar. Ecol.-Prog. Ser. 216:265-278.
9. Conrad, R. 1996. Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol. Rev. 60:609-640.
10. Costello, E. K., and S. K. Schmidt. 2006. Microbial diversity in alpine tundra wet meadow soil: novel Chloroflexi from a cold, water-saturated environment. Environ. Microbiol. 8:1471-1486.
11. Cruz-Martinez, K., et al. 2009. Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland. ISME J. 3:738-744.
12. Di Giovanni, G. D., L. S. Watrud, R. J. Seidler, and F. Widmer. 1999. Comparison of parental and transgenic alfalfa rhizosphere bacterial communities using Biolog GN metabolic fingerprinting and enterobacterial repetitive intergenic consensus sequence-PCR (ERIC-PCR). Microb. Ecol. 37: 129-139.
13. Donegan, K. K., et al. 1995. Changes in levels, species and DNA fingerprints of soil-microorganisms associated with cotton expressing the Bacillus thuringiensis var. Kurstaki endotoxin. Appl. Soil. Ecol. 2:111-124.
14. Donegan, K. K., et al. 1999. A field study with genetically engineered alfalfa inoculated with recombinant Sinorhizobium meliloti: effects on the soil ecosystem. J. Appl. Ecol. 36:920-936.
15. Doty, S. L., et al. 2007. Enhanced phytoremediation of volatile environmental pollutants with transgenic trees. Proc. Natl. Acad. Sci. U. S. A. 104:16816-16821.
16. Dunfield, K. E., and J. J. Germida. 2004. Impact of genetically modified crops on soil- and plant-associated microbial communities. J. Environ. Qual. 33:806-815.
17. Dunfield, K. E., and J. J. Germida. 2003. Seasonal changes in the rhizosphere microbial communities associated with field-grown genetically modified canola (Brassica napus). Appl. Environ. Microbiol. 69:7310-7318.
18. Epelde, L., et al. 2010. Impact of metal pollution and Thlaspi caerulescens growth on soil microbial communities. Appl. Environ. Microb. 76:7843-7853.
19. Fierer, N., and R. B. Jackson. 2006. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. U. S. A. 103:626-631.
20. Fitz, W. J., et al. 2003. Rhizosphere characteristics of the arsenic hyperaccumulator Pteris vittata L. and monitoring of phytoremoval efficiency. Environ. Sci. Technol. 37:5008-5014.
21. French, C. E., S. J. Rosser, G. J. Davies, S. Nicklin, and N. C. Bruce. 1999. Biodegradation of explosives by transgenic plants expressing pentaerythritol tetranitrate reductase. Nat. Biotechnol. 17:491-494.
22. Ganzert, L., A. Lipski, H. W. Hubberten, and D. Wagner. 2011. The impact of different soil parameters on the community structure of dominant bacteria from nine different soils located on Livingston Island, South Shetland Archipelago, Antarctica. FEMS Microbiol. Ecol. 76:476-491.
23. Garcia-Moyano, A., E. Gonzalez-Toril, A. Aguilera, and R. Amils. 2007. Prokaryotic community composition and ecology of floating macroscopic filaments from an extreme acidic environment, Rio Tinto (SW, Spain). Syst. Appl. Microbiol. 30:601-614.
24. Gonzaga, M. I., L. Q. Ma, J. A. Santos, and M. I. Matias. 2009. Rhizosphere characteristics of two arsenic hyperaccumulating Pteris ferns. Sci. Total Environ. 407:4711-4716.
25. Grayston, S. J., D. Vaughan, and D. Jones. 1997. Rhizosphere carbon flow in trees, in comparison with annual plants: the importance of root exudation and its impact on microbial activity and nutrient availability. Appl. Soil. Ecol. 5:29-56.
26. Gremion, F., A. Chatzinotas, K. Kaufmann, W. Von Sigler, and H. Harms. 2004. Impacts of heavy metal contamination and phytoremediation on a microbial community during a twelve-month microcosm experiment. FEMS Microbiol. Ecol. 48:273-283.
27. Griffiths, B. S., I. E. Geoghegan, and W. M. Robertson. 2000. Testing genetically engineered potato, producing the lectins GNA and Con A, on non-target soil organisms and processes. J. Appl. Ecol. 37:159-170.
28. Gyamfi, S., U. Pfeifer, M. Stierschneider, and A. Sessitsch. 2002. Effects of transgenic glufosinate-tolerant oilseed rape (Brassica napus) and the associated herbicide application on eubacterial and Pseudomonas communities in the rhizosphere. FEMS Microbiol. Ecol. 41:181-190.
29. Hamady, M., C. Lozupone, and R. Knight. 2010. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J. 4:17-27.
30. Hammer, D., and C. Keller. 2002. Changes in the rhizosphere of metalaccumulating plants evidenced by chemical extractants. J. Environ. Qual. 31:1561-1569.
31. Hansel, C. M., S. Fendorf, P. M. Jardine, and C. A. Francis. 2008. Changesin bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile. Appl. Environ. Microbiol. 74:1620-1633.
32. He, J. Z., L. M. Zhang, S. S. Jin, Y. G. Zhu, and F. Liu. 2008. Bacterial communities inside and surrounding soil iron-manganese nodules. Geomicrobiol. J. 25:14-24.
33. He, Z., S. Xiao, X. Xie, and Y. Hu. 2008. Microbial diversity in acid mineral bioleaching systems of Dongxiang copper mine and Yinshan lead-zinc mine. Extremophiles 12:225-234.
34. Herrmann, M., A. M. Saunders, and A. Schramm. 2008. Archaea dominate the ammonia-oxidizing community in the rhizosphere of the freshwater macrophyte Littorella uniflora. Appl. Environ. Microbiol. 74:3279-3283.
35. Heuer, H., R. M. Kroppenstedt, J. Lottmann, G. Berg, and K. Smalla. 2002. Effects of T4 lysozyme release from transgenic potato roots on bacterial rhizosphere communities are negligible relative to natural factors. Appl. Environ. Microbiol. 68:1325-1335.
36. Hippe, H. 2000. Leptospirillum gen. nov. (ex Markosyan 1972), nom. rev., including Leptospirillum ferrooxidans sp. nov. (ex Markosyan 1972), nom. rev. and Leptospirillum thermoferrooxidans sp. nov. (Golovacheva et al. Int. J. Syst. Evol. Microbiol. 50:501-503, 1992.
37. International Organization for Standardization. 1995. Soil quality: determination of organic and total carbon after dry combustion (elementary analysis). ISO document 10694:1995. International Organization for Standardization, Geneva, Switzerland.
38. Jain, R. K., et al. 2010. A case study for assessment of microbial community dynamics in genetically modified Bt cotton crop fields. Curr. Microbiol. 61:118-124.
39. Kennedy, A. C., and K. L. Smith. 1995. Soil microbial diversity and the sustainability of agricultural soils. Plant Soil 170:75-86.
40. Kim, M. C., et al. 2008. Molecular analysis of bacterial community structures in paddy soils for environmental risk assessment with two varieties of genetically modified rice, Iksan 483 and Milyang 204. J. Microbiol. Biotechnol. 18:207-218
41. Korea Institute of Geoscience and Mineral Resources. 2005. Reduction, reuse, management technology of wastes: development of demonstration system for the harmlessness and waste reduction from the Sang-Dong mine tailings. Korea Institute of Geoscience and Mineral Resources, Ministry of Environment, Suwon, Republic of Korea.
42. Lauber, C. L., M. Hamady, R. Knight, and N. Fierer. 2009. Pyrosequencingbased assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microb. 75:5111-5120.
43. LeBlanc, P. M., R. C. Hamelin, and M. Filion. 2007. Alteration of soil rhizosphere communities following genetic transformation of white spruce. Appl. Environ. Microbiol. 73:4128-4134.
44. Ledin, M. 2000. Accumulation of metals by microorganisms: processes and importance for soil systems. Earth-Sci. Rev. 51:1-31.
45. Lee, Y. E., et al. 2011. Effects of field-grown genetically modified zoysia grass on bacterial community structure. J. Microbiol. Biotechnol. 21:333-340.
46. 2 affects soil microbial diversity associated with trembling aspen. Environ. Microbiol. 10:926-941.
47. Lottmann, J., et al. 2000. Establishment of introduced antagonistic bacteria in the rhizosphere of transgenic potatoes and their effect on the bacterial community. FEMS Microbiol. Ecol. 33:41-49.
48. Lovley, D. R. 1995. Bioremediation of organic and metal contaminants with dissimilatory metal reduction. J. Ind. Microbiol. 14:85-93.
49. Lukow, T., P. F. Dunfield, and W. Liesack. 2000. Use of the T-RFLP technique to assess spatial and temporal changes in the bacterial community structure within an agricultural soil planted with transgenic and non-transgenic potato plants. FEMS Microbiol. Ecol. 32:241-247.
50. Mendez, M. O., J. W. Neilson, and R. M. Maier. 2008. Characterization of a bacterial community in an abandoned semiarid lead-zinc mine tailing site. Appl. Environ. Microb. 74:3899-3907.
51. Mirete, S., C. G. de Figueras, and J. E. Gonzalez-Pastor. 2007. Novel nickel resistance genes from the rhizosphere metagenome of plants adapted to acid mine drainage. Appl. Environ. Microbiol. 73:6001-6011.
52. Mulligan, C. N., R. N. Yong, and B. F. Gibbs. 2001. Remediation technologies for metal-contaminated soils and groundwater: an evaluation. Eng. Geol. 60:193-207.
53. National Academy of Agriculture Science. 1988. Soil chemistry analysis. National Academy of Agriculture Science, Suwon, Republic of Korea.
54. Nemergut, D. R., et al. 2008. The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environ. Microbiol. 10:3093-3105.
55. Neufeld, J. D., J. Li, and W. W. Mohn. 2008. Scratching the surface of the rare biosphere with ribosomal sequence tag primers. FEMS Microbiol. Lett. 283:146-153.
56. Nriagu, J. O., and J. M. Pacyna. 1988. Quantitative assessment of worldwide contamination of air, water and soils by trace-metals. Nature 333:134-139.
57. Palmroth, M. R. T., et al. 2007. Metabolic and phylogenetic analysis of microbial communities during phytoremediation of soil contaminated with weathered hydrocarbons and heavy metals. Biodegradation 18:769-782.
58. Reference deleted
59. Rugh, C. L., J. F. Senecoff, R. B. Meagher, and S. A. Merkle. 1998. Development of transgenic yellow poplar for mercury phytoremediation. Nat. Biotechnol. 16:925-928.
60. Schmalenberger, A., and C. C. Tebbe. 2002. Bacterial community composition in the rhizosphere of a transgenic, herbicide-resistant maize (Zea mays) and comparison to its non-transgenic cultivar Bosphore. FEMS Microbiol. Ecol. 40:29-37.
61. Shao, H. B., et al. 2010. Understanding molecular mechanisms for improving phytoremediation of heavy metal-contaminated soils. Crit. Rev. Biotechnol. 30:23-30.
62. Siciliano, S. D., and J. J. Germida. 1999. Enhanced phytoremediation of chlorobenzoates in rhizosphere soil. Soil Biol. Biochem. 31:299-305.
63. Smalla, K., et al. 2001. Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl. Environ. Microbiol. 67:4742-4751.
64. Soudek, P., R. Tykva, and T. Vanek. 2004. Laboratory analyses of Cs-137 uptake by sunflower, reed and poplar. Chemosphere 55:1081-1087.
65. Stott, M. B., et al. 2008. Isolation of novel bacteria, including a candidate division, from geothermal soils in New Zealand. Environ. Microbiol. 10: 2030-2041.
66. Tarlera, S., K. Jangid, A. H. Ivester, W. B. Whitman, and M. A. Williams. 2008. Microbial community succession and bacterial diversity in soils during 77,000 years of ecosystem development. FEMS Microbiol. Ecol. 64:129-140.
67. Van Aken, B. 2008. Transgenic plants for phytoremediation: helping nature to clean up environmental pollution. Trends Biotechnol. 26:225-227.
68. Vandecasteele, B., J. Samyn, P. Quataert, B. Muys, and F. M. G. Tack. 2004. Earthworm biomass as additional information for risk assessment of heavy metal biomagnification: a case study for dredged sediment-derived soils and polluted floodplain soils. Environ. Pollution. 129:363-375.
69. Wolfenbarger, L. L., and P. R. Phifer. 2000. The ecological risks and benefits of genetically engineered plants. Science 290:2088-2093.
70. Xie, X. H., S. M. Xiao, and J. S. Liu. 2009. Microbial communities in acid mine drainage and their interaction with pyrite surface. Curr. Microbiol. 59:71-77.
71. Xiong, J. B., et al. 2010. Microbial communities and functional genes associated with soil arsenic contamination and the rhizosphere of the arsenichyperaccumulating plant Pteris vittata L. Appl. Environ. Microb. 76:7277-7284.
72. Yadav, R., P. Arora, S. Kumar, and A. Chaudhury. 2010. Perspectives for genetic engineering of poplars for enhanced phytoremediation abilities. Ecotoxicology 19:1574-1588.
73. Yandell, B. S. 1997. Practical data analysis for designed experiments. Chapman & Hall, London, England.
74. Zhou, J. Z., et al. 2003. Bacterial phylogenetic diversity and a novel candidate division of two humid region, sandy surface soils. Soil Biol. Biochem. 35:915-924.