Bacterial communities associated with Brassica napusL. grown on trace element-contaminated and non-contaminated fields: A genotypic and phenotypic comparison

Microbial Biotechnology

Volumn 6, Issue 4, 2013, Pages 371-384

  Croes, S ^a   Weyens, N ^a   Janssen, J ^a   Vercampt, H ^a   Colpaert, J V ^a   Carleer, R ^a   Vangronsveld, J ^a  

^a HASSELT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

INDOLEACETIC ACID; SOIL POLLUTANT; TRACE ELEMENT;

ARTHROBACTER; ARTICLE; BACILLUS; BACTERIAL STRAIN; CAULOBACTER; COMPARATIVE STUDY; CONTROLLED STUDY; ENDOPHYTE; GENOTYPE; MICROBIAL COMMUNITY; MICROMONOSPORA; NITROGEN FIXATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PANTOEA; PEDOBACTER; PHENOTYPE; PLANT GROWTH; PSEUDOMONAS; RAPESEED; RHIZOBIUM; RHIZOSPHERE; RHODOCOCCUS; ROOT EXUDATE; SOLUBILIZATION; STAPHYLOCOCCUS; UNINDEXED SEQUENCE; BACTERIA; BIOTA; CLASSIFICATION; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; PLANT ROOT; SOIL POLLUTANT;

BACTERIA (MICROORGANISMS); BRASSICA;

BACTERIA; BIOTA; BRASSICA NAPUS; PLANT ROOTS; RHIZOSPHERE; SOIL POLLUTANTS; TRACE ELEMENTS;

EID: 84879011989     PISSN: 17517907     EISSN: 17517915     Source Type: Journal    
DOI: 10.1111/1751-7915.12057     Document Type: Article

References (79)

1. Belimov, A.A., Hontzeas, N., Safronova, V.I., Demchinskaya, S.V., Piluzza, G., Bullitta, S., and Glick, B.R. (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37: 241-250.
2. Benizri, E., Baudoin, E., and Guckert, A. (2001) Root colonization by inoculated plant growth rhizobacteria. Biocontrol Sci Technol 11: 557-574.
3. Bulgarelli, D., Rott, M., Schlaeppi, K., Ver Loren van Themaat, E., Ahmadinejad, N., Assenza, F., etal. (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488: 91-95.
4. Chakravarty, B., and Shrivastava, S. (1994) Response to cadmium toxicity during in vitro growth in Arachis hypogaea. Bull Environ Contam Toxicol 52: 749-755.
5. Compant, S., Clément, C., and Sessitsch, A. (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42: 669-678.
6. Cunningham, J.E., and Kuiack, C. (1992) Production of citric and oxalic acids and solubilization of calcium-phosphate by Penicillium bilaii. Appl Environ Microbiol 58: 1451-1458.
7. Dell'Amico, E., Cavalca, L., and Andreoni, V. (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40: 74-84.
8. Demoling, F., Figueroa, D., and Bååth, E. (2007) Comparison of factors limiting bacterial growth in different soils. Soil Biol Biochem 39: 2485-2495.
9. Döbereiner, J. (1989) Isolation and identification of root associated diazotrophs. In Nitrogen Fixation with Non-Legumes. Skinner, F.A. (ed.). Dordrecht, Boston, London: Kluwer Academic Publishers, pp. 103-108.
10. Fisher, P.J., Petrini, O., and Scott, H.M.L. (1992) The distribution of some fungal and bacterial endophytes in maize. New Phytol 122: 299-305.
11. Germida, J.J., and Theoret, C. (1997) Do enumeration media affect estimates of bacterial diversity in soil? In Annual Meeting of the Canadian Society of Microbiology, 15-19 June 1997, Quebec City, Canada, 65 pp.
12. Germida, J.J., Siciliano, S.D., Renato de Freitas, J., and Seib, A.M. (1998) Diversity of root-associated bacteria associated with field-grown canola (Brassica napus L.) and wheat (Triticum aestivum L.). FEMS Microbiol Ecol 26: 43-50.
13. Glick, B.R. (2003) Phytoremediation: synergistic use of plants and bacteria to clean up the environment. Biotechnol Adv 21: 383-393.
14. Glick, B.R. (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28: 367-374.
15. Gordon, S.A., and Weber, R.P. (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26: 192-195.
16. Granér, G., Persson, P., Meijer, J., and Alström, S. (2003) A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol Lett 224: 269-276.
17. Grayston, S.J., Wang, S., Campbell, C.D., and Edwards, A.C. (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30: 369-378.
18. Grispen, V.M.J., Nelissen, H.J.M., and Verkleij, J.A.C. (2006) Phytoextraction with Brassica napus L.: a tool for sustainable management of heavy metal contaminated soils. Environ Pollut 144: 77-83.
19. Gül, M.K., and Şeker, M.S. (2006) Comparative analysis of phytosterol components from rapeseed (Brassica napus L.) and olive (Olea europaea L.) varieties. Eur J Lipid Sci Technol 108: 759-765.
20. Haack, S.K., Garchow, H., Odelson, D.A., Forney, L.J., and Klug, M.J. (1994) Accuracy, reproducibility and interpretation of fatty acid methyl ester profiles of model bacterial communities. Appl Environ Microbiol 60: 2483-2493.
21. Hallmann, J. (2001) Plant interactions with endophytic bacteria. In Biotic Interactions in Plant-Pathogen Associations. Jeger, M.J., and Spence, N.J. (eds). Wallingford, UK: CABI Publishing, pp. 87-119.
22. Hartmann, A., Schmid, M., van Tuinen, D., and Berg, G. (2009) Plant-driven selection of microbes. Plant Soil 321: 235-257.
23. Iqbal, M., Akhtar, N., Zafar, S., and Ali, I. (2008) Genotypic responses for yield and seed oil quality of two Brassica species under semi-arid environmental conditions. S Afr J Bot 74: 567-571.
24. Jones, D.L., and Darrah, P.R. (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166: 247-257.
25. Kaiser, O., Pühler, A., and Selbitschka, W. (2001) Phylogenetic analysis of microbial diversity in the rhizoplane of oilseed rape (Brassica napus cv. Westar) employing cultivation-dependent and cultivation-independent approaches. Microb Ecol 42: 136-149.
26. Kärenlampi, S., Schat, H., Vangronsveld, J., Verkleij, J.A.C., van der Lelie, D., Mergeay, M., and Tervahauta, A.I. (2000) Genetic engineering in the improvement of plants for phytoremediation of metal polluted soils. Environ Pollut 107: 225-231.
27. Khan, M.S., Zaidi, A., Wani, P.A., and Oves, M. (2009) Role of plant growth promoting rhizobacteria in the remediation of metal contaminated soils. Environ Chem Lett 7: 1-19.
28. Kobayashi, D.Y., and Palumbo, J.D. (2000) Bacterial endophytes and their effects on plants and uses in agriculture. In Microbial Endophytes. Bacon, C.W., and White, J.F., Jr (eds). New York, USA: Marcel Dekker, pp. 199-233.
29. Koopmans, G.F., Römkens, P.F.A.M., Fokkema, M.J., Song, J., Luo, Y.M., Japenga, J., and Zhao, F.J. (2008) Feasibility of phytoextraction to remediate cadmium and zinc contaminated soils. Environ Pollut 156: 905-914.
30. Larcher, M., Rapior, S., and Cleyet-Marel, J.C. (2008) Bacteria from the rhizosphere and roots of Brassica napus influence its root growth promotion by Phyllobacterium brassicacearum. Acta Bot Gallica 155: 355-366.
31. Lemanceau, P., Corberand, T., Gardan, L., Latour, X., Laguerre, G., Boeufgras, J.M., and Alabouvette, C. (1995) Effect of two plant species flax (Linum usitatissimum L.) and tomato (Lycopersicon esculentum Mill.), on the diversity of soilborne populations of fluorescent pseudomonads. Appl Environ Microbiol 61: 1004-1012.
32. Li, W.C., and Wong, M.H. (2010) Effects of bacteria on metal bioavailability, speciation, and mobility in different metal mine soils: a column study. J Soils Sediments 10: 313-325.
33. Lim, S.R., and Schoenung, J.M. (2010) Human health and ecological toxicity potentials due to heavy metal content in waste electronic devices with flat panel displays. J Hazard Mater 177: 251-259.
34. Lodewyckx, C., Taghavi, S., Mergeay, M., Vangronsveld, J., Clijsters, H., and van der Lelie, D. (2001) The effect of recombinant heavy metal resistant endophytic bacteria on heavy metal uptake by their host plant. Int J Phytoremediation 3: 173-187.
35. Lugtenberg, B., and Kamilova, F. (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63: 541-556.
36. Lugtenberg, B.J.J., and Dekkers, L.C. (1999) What makes Pseudomonas bacteria rhizosphere competent? Environ Microbiol 1: 9-13.
37. Lundberg, D.S., Lebeis, S.L., Paredes, S.H., Yourstone, S., Gehring, J., Malfatti, S., etal. (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488: 86-90.
38. Ma, Y., Rajkumar, M., and Freitas, H. (2009) Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp. Chemosphere 75: 719-725.
39. Ma, Y., Prasad, M.N.V., Rajkumar, M., and Freitas, H. (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29: 248-258.
40. McKenna, I.M., Chaney, R.L., and Williams, F.M. (1993) The effects of cadmium and zinc interactions on the accumulation and tissue distribution of zinc and cadmium in lettuce and spinach. Environ Pollut 79: 113-120.
41. Marchiol, L., Sacco, P., Assolari, S., and Zerbi, G. (2004) Reclamation of polluted soil: phytoremediation potential of crop-related Brassica species. Water Air Soil Pollut 158: 345-356.
42. Meers, E., Van Slycken, S., Adriaensen, K., Ruttens, A., Vangronsveld, J., Du Laing, G., etal. (2010) The use of bio-energy crops (Zea mays) for 'phytoattenuation' of heavy metals on moderately contaminated soils: a field experiment. Chemosphere 78: 35-41.
43. Mench, M., Vangronsveld, J., Didier, V., and Clijsters, H. (1994) Evaluation of metal mobility, plant availability and immobiliation by chemical agents in a limed silty soil. Environ Pollut 86: 279-286.
44. Mergeay, M., Nies, D., Schlegel, H.G., Gerits, J., Charles, P., and Van Gijsegem, F. (1985) Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 162: 328-334.
45. Nabti, E., Sahnoune, M., Adjrad, S., Van Dommelen, A., Ghoul, M., Schmid, M., and Hartmann, A. (2007) A halophilic and osmotolerant Azospirillum brasilense strain from Algerian soil restores wheat growth under saline conditions. Eng Life Sci 7: 354-360.
46. Nautiyal, C.S. (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170: 265-270.
47. Polle, A., and Schützendübel, A. (2003) Heavy metal signalling in plants: linking cellular and organismic responses. In Plant Responses to Abiotic Stress. Topics in Current Genetics, Vol. 4. Hirt, H., and Shinozaki, K. (eds). Berlin, Heidelberg, Germany: Springer, pp. 167-215.
48. Rajkumar, M., Ae, N., and Freitas, H. (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77: 53-160.
49. Rajkumar, M., Ae, N., Narasimha, M., Prasad, V., and Freitas, H. (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28: 142-149.
50. Romick, T.L., and Fleming, H.P. (1998) Acetoin production as an indicator of growth and metabolic inhibition of Listeria monocytogenes. J Appl Microbiol 84: 18-24.
51. Römkens, P.F.A.M., Zeilmaker, M.J., Rietra, R.P.J.J., Kan, C.A., van Eijkeren, J.C.H., van Raamsdonk, L.W.D., and Lijzen, J.P.A. (2007) Blootstelling en opname van cadmium door runderen in de Kempen: een modelstudie. Wageningen: Alterra-rapport 1438.
52. Rouatt, J.W., Katznelson, H., and Payne, T.M.B. (1960) Statistical evaluation of the rhizosphere effect. Soil Sci Soc Am J 24: 271-273.
53. Ruttens, A., Boulet, J., Weyens, N., Smeets, K., Adriaensen, K., Meers, E., etal. (2010) Short rotation coppice culture of willow and poplar as energy crops on metal contaminated agricultural soils. Int J Phytoremediation 13: 194-207.
54. Schwyn, B., and Neilands, J.B. (1987) Universal chemical-assay for the detection and determination of siderophores. Anal Biochem 160: 47-56.
55. Sessitsch, A., and Puschenreiter, M. (2008) Endophytes and rhizosphere bacteria of plants growing in heavy metal-containing soils. In Microbiology of Extreme Soils. Dion, P., and Nautiyal, C.S. (eds). Berlin, Heidelberg, Germany: Springer, pp. 317-332.
56. Sheng, X.F., and Xia, J.J. (2006) Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere 64: 1036-1042.
57. Sheng, X.F., Xia, J.J., Jiang, C.Y., He, L.Y., and Qian, M. (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156: 1164-1170.
58. Shrivastava, G.K., and Singh, V.P. (1989) Uptake, accumulation and translocation of cadmium and zinc in Abelmoschus esculentus L. Moench. Plant Physiol Biochem 16: 17-22.
59. Siciliano, S.D., and Germida, J.J. (1999) Taxonomic diversity of bacteria associated with the roots of field-grown transgenic Brassica napus cv. Quest, compared to the non-transgenic B. napus cv. Excel and B. rapa cv. Parkland. FEMS Microbiol Ecol 29: 263-272.
60. Soderberg, K.H., and Bååth, E. (1998) Bacterial activity along a young barley root measured by the thymidine and leucine incorporation techniques. Soil Biol Biochem 30: 1259-1268.
61. Song, Z.H., Ding, L.X., Ma, B.J., Li, W.Z., and Mei, R.H. (1999) Studies on the population and dynamic analysis of peanut endophytes. Acta Phytophysiol Sinica 26: 309-314.
62. Sonke, J.E., Hoogewerff, J.A., van der Laan, S.R., and Vangronsveld, J. (2002) A chemical and mineralogical reconstruction of Zn-smelter emissions in the Kempen region (Belgium), based on organic pool sediment cores. Sci Total Environ 292: 101-119.
63. Stephenson, A.L., Dennis, J.S., and Scott, S.A. (2008) Improving the sustainability of the production of biodiesel from oilseed rape in the UK. Process Saf Environ Prot 86: 427-440.
64. Ström, L., Owen, A.G., Godbold, D.L., and Jones, D.L. (2002) Organic acid mediated P mobilization in the rhizosphere and uptake by maize roots. Soil Biol Biochem 34: 703-710.
65. Van Ginneken, L., Meers, E., Guisson, R., Ruttens, A., Elst, K., Tack, F.M.G., etal. (2007) Phytoremediation for heavy metal-contaminated soils combined with bioenergy production. J Environ Eng Landsc Manag 15: 227-236.
66. Van Ranst, E., Verloo, M., Demeyer, A., and Pauwels, J.M. (1999) Manual for the Soil Chemistry and Fertility Laboratory. Ghent, Belgium: Ghent University, Faculty Agricultural and Applied Biological Sciences.
67. Vangronsveld, J., Herzig, R., Weyens, N., Boulet, J., Adriaensen, K., Ruttens, A., etal. (2009) Phytoremediation of contaminated soils and groundwater: lessons from the field. Environ Sci Pollut Res Int 16: 765-794.
68. Vassilev, A., Schwitzguébel, J.P., Thewys, T., van der Lelie, D., and Vangronsveld, J. (2004) The use of plants for remediation of metal-contaminated soils. Sci World J 4: 9-34.
69. Wajda, L., Kuternozinska, W., and Pilipowicz, M. (1989) Cadmium toxicity to plant callus-culture in vitro 1. Modulation by zinc and dependence on plant-species and callus line. Environ Exp Bot 29: 301-305.
70. Wang, Y., Brown, H.N., Crowley, D.E., and Szaniszlo, P.J. (1993) Evidence for direct utilization of a siderophore, ferroxamine B, in axenically grown cucumber. Plant Cell Environ 16: 579-585.
71. Weyens, N., van der Lelie, D., Taghavi, S., Newman, L., and Vangronsveld, J. (2009a) Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27: 591-598.
72. Weyens, N., van der Lelie, D., Taghavi, S., and Vangronsveld, J. (2009b) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Opin Biotechnol 20: 248-254.
73. Weyens, N., Taghavi, S., Barac, T., van der Lelie, D., Boulet, J., Artois, T., etal. (2009c) Bacteria associated with Oak and Ash on a TCE-contaminated site: characterization of isolates with potential to avoid evapotranspiration of TCE. Environ Sci Pollut Res Int 16: 830-843.
74. Weyens, N., Croes, S., Dupae, J., Newman, L., van der Lelie, D., Carleer, R., and Vangronsveld, J. (2010) Endophytic bacteria improve phytoremediation of Ni and TCE co-contamination. Environ Pollut 158: 2422-2427.
75. Weyens, N., Boulet, J., Adriaensen, D., Timmermans, J.P., Prinsen, E., Van Oevelen, S., etal. (2011) Contrasting colonization and plant growth promoting capacity between wild type and a gfp-derative of the endophyte Pseudomonas putida W619 in hybrid poplar. Plant Soil 356: 217-230.
76. Witters, N., Mendelsohn, R., Van Slycken, S., Weyens, N., Schreurs, E., Meers, E., etal. (2011) Phytoremediation, a sustainable remediation technology? Conclusions from a case study I: energy production and carbon dioxide abatement. Biomass Bioenergy 39: 454-469.
77. Xiao, Z., and Xu, P. (2007) Acetoin metabolism in bacteria. Crit Rev Microbiol 33: 127-140.
78. 2-fixing bacterial strains isolated from rice fields along the Yangtze River Plain. J Basic Microbiol 46: 56-63.
79. Zhuang, X., Chen, J., Shim, H., and Bai, Z. (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33: 406-413.