Comparison of bacterial diversity, root exudates and soil enzymatic activities in the rhizosphere of AVP1-transgenic and nontransgenic wheat (Triticum aestivum L.).
bacterial diversity
risk assessment
soil enzymes
transgenic plants
wheat
Journal
Journal of applied microbiology
ISSN: 1365-2672
Titre abrégé: J Appl Microbiol
Pays: England
ID NLM: 9706280
Informations de publication
Date de publication:
Nov 2022
Nov 2022
Historique:
revised:
30
06
2022
received:
08
05
2022
accepted:
07
07
2022
pubmed:
1
8
2022
medline:
22
10
2022
entrez:
31
7
2022
Statut:
ppublish
Résumé
Soil microbial communities are among the most diverse communities that might be affected due to transgenic crops. Therefore, risk assessment studies on transgenes are essentially required as any adverse effects may depend not only on the specific gene and crop involved but also on soil conditions. The present study deals with the comparison of bacterial populations, root exudates and activities of soil enzymes in nontransgenic and AVP1-transgenic wheat rhizosphere, overexpressing vacuolar H + pyrophosphatase for salinity and drought stress tolerance. Amounts of organic acids and sugars produced as root exudates and activities of dehydrogenase, phosphatase and protease enzymes in soil solution showed no significant differences in AVP1-transgenic and nontransgenic wheat rhizosphere, except for urease and phenol oxidase activities. The higher copy number of nifH gene showed the abundance of nitrogen-fixing bacteria in the rhizosphere of AVP1-transgenic wheat compared with nontransgenic wheat. nifH gene sequence analysis indicated the common diazotrophic genera Azospirillum, Bradyrhizobium, Rhizobium and Pseudomonas in AVP1-transgenic and nontransgenic wheat except for Zoogloea detected only in nontransgenic wheat. Using 454-pyrosequencing of 16S rRNA gene from soil DNA, a total of 156, 282 sequences of 18 phyla were obtained, which represented bacterial (128,006), Archeal (7928) and unclassified (21,568) sequences. Proteobacteria, Crenarchaeota and Firmicutes were the most abundant phyla in the transgenic and nontransgenic wheat rhizosphere. Further comparison of different taxonomic units at the genus level showed similar distribution in transgenic and nontransgenic wheat rhizospheres. We conclude that the AVP1 gene in transgenic wheat has no apparent adverse effects on the soil environment and different bacterial communities. However, the bacterial community depends on several other factors, not only genetic composition of the host plants. The present research supports introduction and cultivation of transgenic plants in agricultural systems without any adverse effects on indigenous bacterial communities and soil ecosystems.
Substances chimiques
Soil
0
RNA, Ribosomal, 16S
0
Urease
EC 3.5.1.5
Monophenol Monooxygenase
EC 1.14.18.1
Sugars
0
Phosphoric Monoester Hydrolases
EC 3.1.3.2
Peptide Hydrolases
EC 3.4.-
Pyrophosphatases
EC 3.6.1.-
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3094-3112Informations de copyright
© 2022 Society for Applied Microbiology.
Références
Alexandrino, M., Costa, R., Canário, A.V. & Costa, M.C. (2014) Clostridia initiate heavy metal bioremoval in mixed sulfidogenic cultures. Environmental Science & Technology, 48, 3378-3385.
Andersen, C.P. (2003) Source-sink balance and carbon allocation below ground in plants exposed to ozone. The New Phytologist, 157, 213-228.
Badri, D.V. & Vivanco, J.M. (2009) Regulation and function of root exudates. Plant, Cell & Environment, 32, 666-681.
Baldrian, P., Větrovský, T., Cajthaml, T., Dobiášová, P., Petránková, M., Šnajdr, J. et al. (2013) Estimation of fungal biomass in forest litter and soil. Fungal Ecology, 6, 1-11.
Barriuso, J., Valverde, J.R. & Mellado, R.P. (2012) Effect of Cry1Ab protein on rhizobacterial communities of Bt-maize over a four-year cultivation period. PLoS One, 7, e35481.
Bashan, Y. & de-Bashan, L.E. (2010) How the plant growth-promoting bacterium Azospirillum promote plant growth-A critical assessment. Advances in Agronomy, 108, 77-136.
Baumgarte, S. & Tebbe, C.C. (2005) Field studies on the environmental fate of the Cry1Ab Bt-toxin produced by transgenic maize (MON810) and its effect on bacterial communities in the maize rhizosphere. Molecular Ecology, 14, 2539-2551.
Bhandari, V. & Gupta, R.S. (2014) Molecular signatures for the phylum (class) Thermotogae and a proposal for its division into three orders (Thermotogales, Kosmotogales ord. nov. and Petrotogales ord. nov.) containing four families (Thermotogaceae, Fervidobacteriaceae fam. nov., Kosmotogaceae fam. nov. and Petrotogaceae fam. nov.) and a new genus Pseudothermotoga gen. nov. with five new combinations. Antonie Leeuwenhoek, 105, 143-168.
Brimecombe, M.J., De Leij, F.A. & Lynch, J.M. (2000) The effect of root exudates on rhizosphere microbial populations. Biochemistry and Organic substances at the soil-plant interface. The Rhizosphere. New York, NY: Marcel Dekker, Inc, pp. 95-140.
Buchanan, B.B., Gruissem, W. & Jones, R.L. (2015) Biochemistry and molecular biology of plants. Hoboken, NJ: John Wiley & Sons.
Bukhat, S., Imran, A., Javaid, S., Shahid, M., Majeed, A. & Naqqash, T. (2020) Communication of plants with microbial world: Exploring the regulatory networks for PGPR mediated defense signaling. Microbiological Research, 238, 126486.
Bulgarelli, D., Rott, M., Schlaeppi, K., van Themaat, E.V.L., Ahmadinejad, N., Assenza, F. et al. (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature, 488, 91-95.
Castaldini, M., Turrini, A., Sbrana, C., Benedetti, A., Marchionni, M., Mocali, S. et al. (2005) Impact of Bt corn on rhizospheric and soil eubacterial communities and on beneficial mycorrhizal symbiosis in experimental microcosms. Applied and Environmental Microbiology, 71, 6719-6729.
Chelius, M.K. & Triplett, E.W. (2001) The diversity of archaea and bacteria in association with the roots of Zea mays L. Microbial Ecology, 41, 252-515.
Coba de la Peña, T., Redondo, F.J., Manrique, E., Lucas, M.M. & Pueyo, J.J. (2010) Nitrogen fixation persists under conditions of salt stress in transgenic Medicago truncatula plants expressing a cyanobacterial flavodoxin. Plant Biotechnology Journal, 8, 954-965.
Collavino, M.M., Tripp, H.J., Frank, I.E., Vidoz, M.L., Calderoli, P.A., Donato, M. et al. (2014) nifH pyrosequencing reveals the potential for location-specific soil chemistry to influence N2-fixing community dynamics. Environmental Microbiology, 16, 3211-3223.
Davey, M., Holmes, G. & Johnstone, R. (2008) High rates of nitrogen fixation (acetylene reduction) on coral skeletons following bleaching mortality. Coral Reef, 27, 227-236.
Drury, B., Rosi-Marshall, E. & Kelly, J.J. (2013) Wastewater treatment effluent reduces the abundance and diversity of benthic bacterial communities in urban and suburban rivers. Applied and Environmental Microbiology, 79, 1897-1905.
Duc, L., Neuenschwander, S., Rehrauer, H. & Zeyer, J. (2011) Application of a nifH microarray to assess the impact of environmental factors on free-living diazotrophs in a glacier forefield. Canadian Journal of Microbiology, 57, 105-114.
Dunfield, K.E. & Germida, J.J. (2003) Seasonal changes in the rhizosphere microbial communities associated with field-grown genetically modified canola (Brassica napus). Applied and Environmental Microbiology, 69, 7310-7318.
Dunfield, K.E. & Germida, J.J. (2004) Impact of genetically modified crops on soil-and plant-associated microbial communities. Journal of Environmental Quality, 33, 806-815.
Fang, M., Kremer, R. & Motavalli, P. (2005) Bacterial diversity in rhizospheres of nontransgenic and transgenic corn. Applied and Environmental Microbiology, 7, 4132-4136.
Fierer, N., Jackson, J.A., Vilgalys, R. & Jackson, R.B. (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Applied and Environmental Microbiology, 71, 4117-4120.
Fierer, N., Lauber, C.L., Ramirez, K.S., Zaneveld, J., Bradford, M.A. & Knight, R. (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. The ISME Journal, 6, 1007-1017.
Fischer, D., Uksa, M., Tischler, W., Kautz, T., Köpke, U. & Schloter, M. (2013) Abundance of ammonia oxidizing microbes and denitrifiers in different soil horizons of an agricultural soil in relation to the cultivated crops. Biology and Fertility of Soils, 49, 1-4.
Flores, S., Saxena, D. & Stotzky, G. (2005) Transgenic Bt plants decompose less in soil than non-Bt plants. Soil Biology and Biochemistry, 37, 1073-1082.
Fudou, R., Jojima, Y., Iizuka, T. & Yamanaka, S. (2002) Haliangium ochraceum gen. nov., sp. nov. and Haliangium tepidum sp. nov.: novel moderately halophilic myxobacteria isolated from coastal saline environments. The Journal of General and Applied Microbiology, 48, 109-116.
Gans, J., Wolinsky, M. & Dunbar, J. (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science, 309, 1387-1390.
García-Salamanca, A., Molina-Henares, M.A., Dillewijn, P., Solano, J., Pizarro-Tobías, P., Roca, A. et al. (2013) Bacterial diversity in the rhizosphere of maize and the surrounding carbonate-rich bulk soil. Microbial Biotechnology, 6, 36-44.
Gaxiola, R.A., Fink, G.R. & Hirschi, K.D. (2002) Genetic manipulation of vacuolar proton pumps and transporters. Plant Physiology, 129, 967-973.
Gaxiola, R.A., Li, J., Undurraga, S., Dang, L.M., Allen, G.J., Alper, S.L. et al. (2001) Drought-and salt-tolerant plants result from overexpression of the AVP1 H+-pump. PNAS, 98, 11444-11449.
Gianfreda, L., Sannino, F., Ortega, N. & Nannipieri, P. (1994) Activity of free and immobilized urease in soil: effects of pesticides. Soil Biology and Biochemistry, 26(6), 777-784.
Gianfreda, L., Sannino, F. & Violante, A. (1995) Pesticide effects on the activity of free, immobilized and soil invertase. Soil Biology and Biochemistry, 27(9), 1201-1208.
Glick, B.R. (1995) The enhancement of plant growth by free-living bacteria. Canadian Journal of Microbiology, 41, 109-117.
Gong, Z.-L., Zhang, C.-F., Jin, R. & Zhang, Y.-Q. (2016) Steroidobacter flavus sp. nov., a microcystin-degrading Gammaproteobacterium isolated from soil. Antonie Leeuwenhoek, 109, 1-7.
Gopal, N., Hill, C., Ross, P., Beresford, T., Fenelon, M. & Cotter, P. (2015) The prevalence and control of Bacillus and related spore-forming bacteria in the dairy industry. Frontiers in Microbiology, 6, 1418.
Govaerts, B., Mezzalama, M., Unno, Y., Sayre, K.D., Luna-Guido, M., Vanherck, K. et al. (2007) Influence of tillage, residue management, and crop rotation on soil microbial biomass and catabolic diversity. Applied Soil Ecology, 37, 18-30.
Griffiths, B., Geoghegan, I. & Robertson, W. (2000) Testing genetically engineered potato, producing the lectins GNA and Con A, on non-target soil organisms and processes. Journal of Applied Ecology, 37, 159-170.
Griffiths, B., Hallett, P., Kuan, H., Pitkin, Y. & Aitken, M. (2005) Biological and physical resilience of soil amended with heavy metal-contaminated sewage sludge. European Journal of Soil Science, 56, 197-206.
Griffiths, R.I., Bailey, M.J., McNamara, N.P. & Whiteley, A.S. (2006) The functions and components of the Sourhope soil microbiota. Applied Soil Ecology, 33, 114-126.
Guan, Z.-J., Lu, S.-B., Huo, Y.-l., Guan, Z.-P., Liu, B. & Wei, W. (2016) Do genetically modified plants affect adversely on soil microbial communities? Agriculture, Ecosystems & Environment, 235, 289-305.
Gupta, S. & Gajbhiye, V.T. (2004) Adsorption-desorption, persistence and leaching behavior of thifluzamide in alluvial soil. Chemosphere, 57, 471-480.
Handelsman, J. (2004) Metagenomics: application of genomics to uncultured microorganisms. Microbiology and Molecular Biology Reviews: MMBR, 68, 669-754.
Heuer, H., Kroppenstedt, R.M., Lottmann, J., Berg, G. & Smalla, K. (2002) Effects of T4 lysozyme release from transgenic potato roots on bacterial rhizosphere communities are negligible relative to natural factors. Applied and Environmental Microbiology, 68(3), 1325-1335.
Icoz, I. & Stotzky, G. (2008) Fate and effects of insect-resistant Bt crops in soil ecosystems. Soil Biology and Biochemistry, 40, 559-586.
İnceoğlu, Ö., Al-Soud, W.A., Salles, J.F., Semenov, A.V. & van Elsas, J.D. (2011) Comparative analysis of bacterial communities in a potato field as determined by pyrosequencing. PLoS One, 6, e23321.
Kahnert, A., Mirleau, P., Wait, R. & Kertesz, M.A. (2002) The LysR-type regulator SftR is involved in soil survival and sulphate ester metabolism in Pseudomonas putida. Environmental Microbiology, 4, 225-237.
Kaštovská, E., Edwards, K. & Šantrůčková, H. (2016) Rhizodeposition flux of competitive versus conservative graminoid: contribution of exudates and root lysates as affected by N loading. Plant and Soil, 412, 1-14.
Kennedy, A. (2004) Non-symbiotic bacterial diazotrophs in crop-farming systems: can their potential for plant growth promotion be better exploited? Soil Biology and Biochemistry, 36, 1229-1244.
Kent, A.D. & Triplett, E.W. (2002) Microbial communities and their interactions in soil and rhizosphere ecosystems. Annual Reviews in Microbiology, 56, 211-236.
Kertesz, M.A. & Mirleau, P. (2004) The role of soil microbes in plant sulphur nutrition. Journal of Experimental Botany, 55, 1939-1945.
Kinross, J.M., Darzi, A.W. & Nicholson, J.K. (2011) Gut microbiome-host interactions in health and disease. Genome Medicine, 3, 14.
Kloepper, J. & Schroth, M. (1978) Association of in vitro antibiosis with inducibility of increased plant growth by Pseudomonas spp. Phytopathology News, 12, 136.
Kulichevskaya, I.S., Suzina, N.E., Liesack, W. & Dedysh, S.N. (2010) Bryobacter aggregatus gen. nov., sp. nov., a peat-inhabiting, aerobic chemo-organotroph from subdivision 3 of the Acidobacteria. International Journal of Systematic and Evolutionary Microbiology, 60, 301-306.
Lapage, S., Shelton, J.E. & Mitchell, T. (1970) Chapter I media for the maintenance and preservation of bacteria. Methods in Microbiology, 3, 1-133.
Liu, B., Liu, G.-H., Sengonca, C., Schumann, P., Tang, J.-Y., Chen, M.-C. et al. (2014) Bacillus wuyishanensis sp. nov., isolated from rhizosphere soil of a medical plant, Prunella vulgaris, in Wuyi mountain of China. International Journal of Systematic and Evolutionary Microbiology, 65, 2030-2035.
Liu, W. (2010) Do genetically modified plants impact arbuscular mycorrhizal fungi? Ecotoxicology, 19, 229-238.
Lonergan, M.C., Severin, E.J., Doleman, B.J., Beaber, S.A., Grubbs, R.H. & Lewis, N.S. (1996) Array-based vapor sensing using chemically sensitive, carbon black-polymer resistors. Chemistry of Materials, 8, 2298-2312.
Lovely, R.H. (1987) Recent studies in the behavioral toxicology of ELF electric and magnetic fields. Progress in Clinical and Biological Research, 257, 327-347.
Lücker, S., Wagner, M., Maixner, F., Pelletier, E., Koch, H., Vacherie, B. et al. (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. PNAS, 107, 13479-13484.
Lugtenberg, B. & Kamilova, F. (2009) Plant-growth-promoting rhizobacteria. Annual Review of Microbiology, 63, 541-556.
Martínez-Viveros, O., Jorquera, M., Crowley, D., Gajardo, G. & Mora, M. (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. Journal of Soil Science and Plant Nutrition, 10, 293-319.
McLean, E. (1982) Soil pH and lime requirement. In: Methods of soil, second ed. Chemical and microbiological properties. Madison, WI: Crop Science Society of America, pp. 199-224.
Mimura, M., Lelmen, K.E., Shimazaki, T., Kikuchi, A. & Watanabe, K.N. (2008) Impact of environmental stress-tolerant transgenic potato on genotypic diversity of microbial communities and soil enzyme activities under stress conditions. Microbes and Environments, 23, 221-228.
Mina, U., Chaudhary, A. & Kamra, A. (2011) Effect of Bt cotton on enzymes activity and microorganisms in rhizosphere. The Journal of Agricultural Science, 3, 96.
Mirza, M.S., Ahmad, W., Latif, F. & Haurat, J. (2001) Isolation, partial characterization, and the effect of plant growth-promoting bacteria (PGPB) on micro-propagated sugarcane in vitro. Plant and Soil, 23, 47-54.
Muangchinda, C., Chavanich, S., Viyakarn, V., Watanabe, K., Imura, S., Vangnai, A. et al. (2014) Abundance and diversity of functional genes involved in the degradation of aromatic hydrocarbons in Antarctic soils and sediments around Syowa Station. Environmental Science and Pollution Research, 22, 1-11.
Nannipieri, P., Ascher, J., Ceccherini, M., Landi, L., Pietramellara, G., Renella, G. et al. (2008) Effects of root exudates in microbial diversity and activity in rhizosphere soils. In: Molecular Mechanisms of Plant and Microbe Coexistence. Berlin: Springer, pp. 339-365.
Naqqash, T., Hameed, S., Imran, A., Hanif, M.K., Majeed, A. & van Elsas, J.D. (2016) Differential response of potato toward inoculation with taxonomically diverse plant growth promoting rhizobacteria. Frontiers in Plant Science, 7, 144.
Naqqash, T., Imran, A., Hameed, S., Shahid, M., Majeed, A., Iqbal, J. et al. (2020) First Report of diazotrophic Brevundimonas spp. as growth enhancer and root colonizer of potato. Scientific Reports, 10, 1-14.
Nazaries, L., Pan, Y., Bodrossy, L., Baggs, E.M., Millard, P., Murrell, J.C. et al. (2013) Evidence of microbial regulation of biogeochemical cycles from a study on methane flux and land use change. Applied and Environmental Microbiology, 79, 4031-4040.
Patrick, D.S. & Jo, H. (2005) Metagenomics for studying unculturable microorganisms: cutting the Gordian knot. Genome Biology, 6(6), 229.
Pinton, R., Varanini, Z. & Nannipieri, P. (2001) The rhizosphere as a site of biochemical interactions among soil components, plants, and microorganisms. In: The rhizosphere. Boca Raton, FL: CRC Press, pp. 17-34.
Poly, F., Ranjard, L., Nazaret, S., Gourbière, F. & Monrozier, L. (2001) Comparison of nifH gene pools in soils and soil microenvironments with contrasting properties. Applied and Environmental Microbiology, 67, 2255-2317.
Porcel, R., Zamarreno, A., Garcia-Mina, J. & Aroca, R. (2014) Involvement of plant endogenous ABA in Bacillus megaterium PGPR activity in tomato plants. BMC Plant Biology, 14, 36.
Qaisrani, M.M., Mirza, M.S., Zaheer, A. & Malik, K.A. (2014) Isolation and identification by 16s RRNA sequence analysis of achromobacter, azospirillum and rhodococcus strains from the rhizosphere of maize and screening for the beneficial effect on plant growth. Pakistan Journal of Agricultural Sciences, 51, 91-99.
Rastogi, G., Sbodio, A., Tech, J.J., Suslow, T.V., Coaker, G.L. & Leveau, J.H.J. (2012) Leaf microbiota in an agroecosystem: spatiotemporal variation in bacterial community composition on field-grown lettuce. The ISME Journal, 6, 1812-1822.
Rastogi, G., Tech, J.J., Coaker, G.L. & Leveau, J.H. (2010) A PCR-based toolbox for the culture-independent quantification of total bacterial abundances in plant environments. Journal of Microbiological Methods, 83, 127-132.
Rosch, C., Mergel, A. & Bothe, H. (2002) Biodiversity of denitrifying and dinitrogen-fixing bacteria in an acid forest soil. Applied and Environmental Microbiology, 68, 3818-3829.
Rosenbaum, K.K., Miller, G.L., Kremer, R.J. & Bradley, K.W. (2014) Interactions between glyphosate, Fusarium infection of common waterhemp (Amaranthus rudis), and soil microbial abundance and diversity in soil collections from Missouri. Weed Science, 62, 71-82.
Rückert, G. (1980) Myxobacteria (Myxobacteriales) on leaf surfaces. Zeitschrift für Allgemeine Mikrobiologie, 21, 761-763.
Sachdev, D., Agarwal, V., Verma, P., Shouche, Y., Dhakephalkar, P. & Chopade, B. (2009) Assessment of microbial biota associated with rhizosphere of wheat (Triticum aestivum) during flowering stage and their plant growth promoting traits. Internet Journal of Microbiology, 7, 627-638.
Sahoo, R.K. & Tuteja, N. (2013) Effect of salinity tolerant PDH45 transgenic rice on physicochemical properties, enzymatic activities and microbial communities of rhizosphere soils. Plant Signaling & Behavior, 8, e24950.
Sakai, M., Hosoda, A., Ogura, K. & Ikenaga, M. (2014) The growth of Steroidobacter agariperforans sp. nov., a novel agar-degrading bacterium isolated from soil, is enhanced by the diffusible metabolites produced by bacteria belonging to rhizobiales. Microbes and Environments, 29, 89-95.
Scheffknecht, S., Mammerler, R., Steinkellner, S. & Vierheilig, H. (2006) Root exudates of mycorrhizal tomato plants exhibit a different effect on microconidia germination of Fusarium oxysporum f. sp. lycopersici than root exudates from non-mycorrhizal tomato plants. Mycorrhiza, 16, 365-370.
Shen, R.F., Cai, H. & Gong, W.H. (2006) Transgenic Bt cotton has no apparent effect on enzymatic activities or functional diversity of microbial communities in rhizosphere soil. Plant and Soil, 285(1), 149-159.
Siciliano, S. & Germida, 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 Microbiology Ecology, 29, 263-272.
Silva, E.M.C.P., Semenov, A.V., van Elsas, J.D. & Salles, J.F. (2011) Seasonal variations in the diversity and abundance of diazotrophic communities across soils. FEMS Microbiology Ecology, 77, 57-68.
Smith, D.L., Subramanian, S., Lamont, J.R. & Bywater-Ekegärd, M. (2015) Signaling in the phytomicrobiome: breadth and potential. Frontiers in Plant Science, 6, 709.
Sogin, M.L., Morrison, H.G., Huber, J.A., Welch, D.M., Huse, S.M., Neal, P.R. et al. (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. PNAS, 103, 12115-12120.
Song, W., Yuan, L.N., Xiao, L., Zhan, Z., Yang, L.Y. & Jiang, L.J. (2007) ALPase activity and the distribution of phosphate solubilizing bacteria and the relationship between them in sediments of Lake Taihu. Huan Jing Ke Xue, 28, 2355-2360.
Suarez, C., Ratering, S., Kramer, I. & Schnell, S. (2014) Cellvibrio diazotrophicus sp. nov., a nitrogen-fixing bacteria isolated from the rhizosphere of salt meadow plants and emended description of the genus Cellvibrio. International Journal of Systematic and Evolutionary Microbiology, 64, 481-486.
Sullivan, T.S., McBride, M.B. & Thies, J.E. (2013) Soil bacterial and archaeal community composition reflects high spatial heterogeneity of pH, bioavailable Zn, and Cu in a metalliferous peat soil. Soil Biology and Biochemistry, 66, 102-109.
Sungthong, R. & Nakaew, N. (2014) The genus Nonomuraea: a review of a rare actinomycete taxon for novel metabolites. Journal of Basic Microbiology, 55, 554-565.
Tabatabai, M. & Bremner, J. (1969) Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biology and Biochemistry, 1, 301-307.
Tahir, M., Mirza, M.S., Hameed, S., Dimitrov, M.R. & Smidt, H. (2015) Cultivation-based and molecular assessment of bacterial diversity in the rhizosheath of wheat under different crop rotations. PLoS One, 10, e0130030.
Tahir, M., Mirza, M.S., Zaheer, A., Dimitrov, M.R., Smidt, H. & Hameed, S. (2013) Isolation and identification of phosphate solubilizer ‘Azospirillum, Bacillus’ and ‘Enterobacter’ strains by 16SrRNA sequence analysis and their effect on growth of wheat (‘Triticum aestivum’ L.). Australian Journal of Crop Science, 7, 1284.
Tan, G.Y. & Tan, W.K. (1986) Interaction between Alfalfa Cultivars and Rhizobium strains for nitrogen-fixation. Theoretical and Applied Genetics, 71, 724-729.
Thaweenut, N., Hachisuka, Y., Ando, S., Yanagisawa, S. & Yoneyama, T. (2011) Two seasons' study on nifH gene expression and nitrogen fixation by diazotrophic endophytes in sugarcane (Saccharum spp. hybrids): expression of nifH genes similar to those of rhizobia. Plant and Soil, 338, 435-449.
Topp, E., Mulbry, W.M., Zhu, H., Nour, S.M. & Cuppels, D. (2000) Characterization of s-triazine herbicide metabolism by a Nocardioides sp. isolated from agricultural soils. Applied and Environmental Microbiology, 66, 3134-3141.
Tuteja, N., Verma, S., Sahoo, R.K., Raveendar, S. & Reddy, I.B.L. (2012) Recent advances in development of marker-free transgenic plants: regulation and biosafety concern. Journal of Biosciences, 37, 167-197.
Verbruggen, E., Kuramae, E.E., Hillekens, R., de Hollander, M., Kiers, E.T., Röling, W.F. et al. (2012) Testing potential effects of maize expressing the Bacillus thuringiensis Cry1Ab endotoxin (Bt maize) on mycorrhizal fungal communities via DNA-and RNA-based pyrosequencing and molecular fingerprinting. Applied and Environmental Microbiology, 78, 7384-7392.
Veres, Z., Kotroczó, Z., Magyaros, K., Tóth, J.A. & Tóthmérész, B. (2013) Dehydrogenase activity in a litter manipulation experiment in temperate forest soil. Acta Silvatica et Lignaria Hungarica, 9, 25-33.
Wang, C., Wang, P.F. & Hu, X. (2007) Removal of COD(Cr) and nitrogen in severely polluted river water by bank filtration. Environmental Technology, 28, 649-657.
Wang, L., Zheng, Z., Luo, X. & Zhang, J. (2011) Performance and mechanisms of a microbial-earthworm ecofilter for removing organic matter and nitrogen from synthetic domestic wastewater. Journal of Hazardous Materials, 195, 245-253.
Wei, X.-D., Zou, H.-L., Chu, L.-M., Liao, B., Ye, C.-M. & Lan, C.-Y. (2006) Field released transgenic papaya affects microbial communities and enzyme activities in soil. Plant and Soil, 285, 347-358.
Winding, A., Hund-Rinke, K. & Rutgers, M. (2005) The use of microorganisms in ecological soil classification and assessment concepts. Ecotoxicology and Environmental Safety, 62, 230-248.
Xie, X.S., Choi, P.J., Li, G.-W., Lee, N.K. & Lia, G. (2008) Single-molecule approach to molecular biology in living bacterial cells. Annual Review of Biophysics, 37, 417-444.
Zehr, J.P., Jenkins, B.D., Short, S.M. & Steward, G.F. (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environmental Microbiology, 5, 539-554.
Zhao, C., Deng, Y., Wang, X., Li, Q., Huang, Y. & Liu, B. (2014) Identification and characterization of an anaerobic ethanol-producing cellulolytic bacterial consortium in Great Basin hot spring with agricultural residues and energy crops. Journal of Microbiology and Biotechnology, 24, 1280-1290.
Zhou, J., He, Z., Yang, Y., Deng, Y., Tringe, S.G. & Alvarez-Cohen, L. (2015) High-throughput metagenomic technologies for complex microbial community analysis: open and closed formats. mBio, 6, e02288-02214.