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Dynamics of bacterial communities in rice field soils as affected by different long-term fertilization practices

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Abstract

Fertilization and the response of the soil microbial community to the process significantly affect crop yield and the environment. In this study, the seasonal variation in the bacterial communities in rice field soil subjected to different fertilization treatments for more than 50 years was investigated using 16S rRNA sequencing. The simultaneous application of inorganic fertilizers and rice straw compost (CAPK) maintained the species richness of the bacterial communities at levels higher than that in the case of non-fertilization (NF) and application of inorganic fertilizers only (APK) in the initial period of rice growth. The seasonal variation in the bacterial community structure in the NF and APK plots showed cyclic behavior, suggesting that the effect of season was important; however, no such trend was observed in the CAPK plot. In the CAPK plot, the relative abundances of putative copiotrophs such as Bacteroidetes, Firmicutes, and Proteobacteria were higher and those of putative oligotrophs such as Acidobacteria and Plactomycetes were lower than those in the other plots. The relative abundances of organotrophs with respiratory metabolism, such as Actinobacteria, were lower and those of chemoautotrophs that oxidize reduced iron and sulfur compounds were higher in the CAPK plot, suggesting greater carbon storage in this plot. Increased methane emission and nitrogen deficiency, which were inferred from the higher abundances of Methylocystis and Bradyrhizobium in the CAPK plot, may be a negative effect of rice straw application; thus, a solution for these should be considered to increase the use of renewable resources in agricultural lands.

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References

  • Acosta-Martínez, V., Dowd, S., Sun, Y., and Allen, V. 2008. Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol. Biochem. 40, 2762–2770.

    Article  Google Scholar 

  • Ahn, J.H., Choi, M.Y., Kim, B.Y., Lee, J.S., Song, J., Kim, G.Y., and Weon, H.Y. 2014. Effects of water-saving irrigation on emissions of greenhouse gases and prokaryotic communities in rice paddy soil. Microb. Ecol. 68, 271–283.

    Article  CAS  PubMed  Google Scholar 

  • Ahn, J.H., Choi, M.Y., Lee, H.W., Kim, B.Y., Song, J., Kim, M.S., and Weon, H.Y. 2013. Analysis of community structure of metabolically active bacteria in a rice field subjected to long-term fertilization practices. Korean J. Soil Sci. Fert. 46, 585–592.

    Article  CAS  Google Scholar 

  • Ahn, J.H., Song, J., Kim, B.Y., Kim, M.S., Joa, J.H., and Weon, H.Y. 2012a. Characterization of the bacterial and archaeal communities in rice field soils subjected to long-term fertilization practices. J. Microbiol. 50, 754–765.

    Article  PubMed  Google Scholar 

  • Ahn, J.H., Hong, I.P., Bok, J.I., Kim, B.Y., Song, J., and Weon, H.Y. 2012b. Pyrosequencing analysis of the bacterial communities in the guts of honey bees Apis cerana and Apis mellifera in Korea. J. Microbiol. 50, 735–745.

    Article  PubMed  Google Scholar 

  • Albuquerque, L., França, L., Rainey, F.A., Schumann, P., Nobre, M.F., and da Costa, M.S. 2011. Gaiella occulta gen. nov., sp. nov., a novel representative of a deep branching phylogenetic lineage within the class Actinobacteria and proposal of Gaiellaceae fam. nov. and Gaiellales ord. nov. Syst. Appl. Microbiol. 34, 595–599.

    Article  PubMed  Google Scholar 

  • Bao, Z., Okubo, T., Kubota, K., Kasahara, Y., Tsurumaru, H., Anda, M., Ikeda, S., and Minamisawa, K. 2014a. Metaproteomic identification of diazotrophic methanotrophs and their localization in root tissues of field-grown rice plants. Appl. Environ. Microbiol. 80, 5043–5052.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bao, Z., Watanabe, A., Sasaki, K., Okubo, T., Tokida, T., Liu, D., Ikeda, S., Imaizumi-Anraku, H., Asakawa, S., Sato, T., et al. 2014b. A rice gene for microbial symbiosis, Oryza sativa CCaMK, reduces CH4 flux in a paddy field with low nitrogen input. Appl. Environ. Microbiol. 80, 1995–2003.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bossio, D.A., Horwath, W.R., Mutters, R.G., and van Kessel, C. 1999. Methane pool and flux dynamics in a rice field following straw incorporation. Soil Biol. Biochem. 31, 1313–1322.

    Article  CAS  Google Scholar 

  • Bossio, D.A. and Scow, K.M. 1995. Impact of carbon and flooding on the metabolic diversity of microbial communities in soils. Appl. Environ. Microbiol. 61, 4043–4050.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bowman, K.S., Nobre, M.F., da Costa, M.S., Rainey, F.A., and Moe, W.M. 2013. Dehalogenimonas alkenigignens sp. nov., a chlorinated- alkane-dehalogenating bacterium isolated from groundwater. Int. J. Syst. Evol. Microbiol. 63, 1492–1498.

    Article  CAS  PubMed  Google Scholar 

  • Brussaard, L., de Ruiter, P.C., and Brown, G.G. 2007. Soil biodiversity for agricultural sustainability. Agr. Ecosyst. Environ. 121, 233–244.

    Article  Google Scholar 

  • Collins, M.D., Lawson, P.A., Willems, A., Cordoba, J.J., Fernandez-Garayzabal, J., Garcia, P., Cai, J., Hippe, H., and Farrow, J.A. 1994. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int. J. Syst. Evol. Microbiol. 44, 812–826.

    CAS  Google Scholar 

  • Devêvre, O.C. and Horwáth, W.R. 2000. Decomposition of rice straw and microbial carbon use efficiency under different soil temperatures and moistures. Soil Biol. Biochem. 32, 1773–1785.

    Article  Google Scholar 

  • Dilly, O., Bloem, J., Vos, A., and Munch, J.C. 2004. Bacterial diversity in agricultural soils during litter decomposition. Appl. Environ. Microbiol. 70, 468–474.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edgar, R.C. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996–998.

    Article  CAS  PubMed  Google Scholar 

  • Emerson, D., Field, E., Chertkov, O., Davenport, K., Goodwin, L., Munk, C., Nolan, M., and Woyke, T. 2013. Comparative genomics of freshwater Fe-oxidizing bacteria: implications for physiology, ecology, and systematics. Front. Microbiol. 4, 254

    Article  PubMed  PubMed Central  Google Scholar 

  • Fierer, N., Bradford, M.A., and Jackson, R.B. 2007. Toward an ecological classification of soil bacteria. Ecology 88, 1354–1364.

    Article  PubMed  Google Scholar 

  • Gao, S., Tanji, K.K., and Scardaci, S.C. 2004. Impact of rice straw incorporation on soil redox status and sulfide toxicity. Agron. J. 96, 70–76.

    Article  CAS  Google Scholar 

  • Goodfellow, M. 2012. Volume 5: The Actinobacteria. In Whitman, W., Goodfellow, M., Kämpfer, P., Busse, H.J., Trujillo, M., Ludwig, W., Suzuki, K.I., and Parte, A. (eds.), Bergey’s manual of systematic bacteriology, Springer, New York, USA.

    Chapter  Google Scholar 

  • Hamady, M., Lozupone, C., and Knight, R. 2009. Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and Phylo-Chip data. ISME J. 4, 17–27.

    Article  PubMed  PubMed Central  Google Scholar 

  • He, J.Z., Liu, X.Z., Zheng, Y., Shen, J.P., and Zhang, L.M. 2010. Dynamics of sulfate reduction and sulfate-reducing prokaryotes in anaerobic paddy soil amended with rice straw. Biol. Fert. Soils 46, 283–291.

    Article  CAS  Google Scholar 

  • He, Q. and Sanford, R.A. 2003. Characterization of Fe(III) reduction by chlororespiring Anaeromxyobacter dehalogenans. Appl. Environ. Microbiol. 69, 2712–2718.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • İnce, İ.A., Demirbağ, Z., and Katı, H. 2014. Arthrobacter pityocampae sp. nov., isolated from Thaumetopoea pityocampa (Lep., Thaumetopoeidae). Int. J. Syst. Evol. Microbiol. 64, 3384–3389.

    Article  PubMed  Google Scholar 

  • Islam, M., Singh Chauhan, P., Kim, Y., Kim, M., and Sa, T. 2011. Community level functional diversity and enzyme activities in paddy soils under different long-term fertilizer management practices. Biol. Fert. Soils 47, 599–604.

    Article  Google Scholar 

  • Jones, R.T., Robeson, M.S., Lauber, C.L., Hamady, M., Knight, R., and Fierer, N. 2009. A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J. 3, 442–453.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly, D., Wood, A., and Stackebrandt, E. 2005. Genus II. Thiobacillus. In Brenner, D.J., Krieg, N.R., Garrity, G.M., Staley, J.T., Boone, D.R., Vos, P., Goodfellow, M., Rainey, F.A., and Schleifer, K.H. (eds.), Bergey’s manual of systematic bacteriology, pp. 764–769. Springer, USA.

    Chapter  Google Scholar 

  • Kodama, Y. and Watanabe, K. 2004. Sulfuricurvum kujiense gen. nov., sp. nov., a facultatively anaerobic, chemolithoautotrophic, sulfur-oxidizing bacterium isolated from an underground crudeoil storage cavity. Int. J. Syst. Evol. Microbiol. 54, 2297–2300.

    Article  CAS  PubMed  Google Scholar 

  • Lang, E. 2014. The Family Kofleriaceae. In Rosenberg, E., DeLong, E.F., Lory, S., Stackebrandt, E., and Thompson, F. (eds.), The Prokaryotes: Deltaproteobacteria and Epsilonproteobacteria, pp. 183–189. Springer Berlin Heidelberg, Berlin, Heidelberg, Germany.

    Chapter  Google Scholar 

  • Lu, F. 2015. How can straw incorporation management impact on soil carbon storage? a meta-analysis. Mitig. Adapt. Strateg. Glob. Change 20, 1545–1568.

    Article  Google Scholar 

  • Moe, W.M., Yan, J., Nobre, M.F., da Costa, M.S., and Rainey, F.A. 2009. Dehalogenimonas lykanthroporepellens gen. nov., sp. nov., a reductively dehalogenating bacterium isolated from chlorinated solvent-contaminated groundwater. Int. J. Syst. Evol. Microbiol. 59, 2692–2697.

    Article  CAS  PubMed  Google Scholar 

  • Mooshammer, M., Wanek, W., Hämmerle, I., Fuchslueger, L., Hofhansl, F., Knoltsch, A., Schnecker, J., Takriti, M., Watzka, M., Wild, B., et al. 2014. Adjustment of microbial nitrogen use efficiency to carbon: nitrogen imbalances regulates soil nitrogen cycling. Nat. Commun. 5, 3694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Odum, E.P. 1969. The strategy of ecosystem development. Science 164, 262–270.

    Article  CAS  PubMed  Google Scholar 

  • Padmanabhan, P., Padmanabhan, S., DeRito, C., Gray, A., Gannon, D., Snape, J.R., Tsai, C.S., Park, W., Jeon, C., and Madsen, E.L. 2003. Respiration of 13C-labeled substrates added to soil in the field and subsequent 16S rRNA gene analysis of 13C-labeled soil DNA. Appl. Environ. Microbiol. 69, 1614–1622.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Price, M.N., Dehal, P.S., and Arkin, A.P. 2009. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641–1650.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian, X., Shen, G., Wang, Z., Guo, C., Liu, Y., Lei, Z., and Zhang, Z. 2014. Co-composting of livestock manure with rice straw: characterization and establishment of maturity evaluation system. Waste Manag. 34, 530–535.

    Article  CAS  PubMed  Google Scholar 

  • Rui, J., Peng, J., and Lu, Y. 2009. Succession of bacterial populations during plant residue decomposition in rice field soil. Appl. Environ. Microbiol. 75, 4879–4886.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanford, R.A., Cole, J.R., and Tiedje, J.M. 2002. Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl-halorespiring facultative anaerobic Myxobacterium. Appl. Environ. Microbiol. 68, 893–900.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schlesner, H. 1994. The development of media suitable for the microorganisms morphologically resembling Planctomyces spp., Pirellula spp., and other planctomycetales from various aquatic habitats using dilute media. Syst. Appl. Microbiol. 17, 135–145.

    Article  Google Scholar 

  • Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., et al. 2009. Introducing mothur: open-source, platformindependent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537–7541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh, B.K., Bardgett, R.D., Smith, P., and Reay, D.S. 2010. Microorganisms and climate change: terrestrial feedbacks and mitigation options. Nat. Rev. Microbiol. 8, 779–790.

    Article  CAS  PubMed  Google Scholar 

  • Suh, J.S., Noh, H.J., and Kwon, J.S. 2009. Impact of amendments on microbial biomass, enzyme activity and bacterial diversity of soils in long-term rice field experiment. Korean J. Soil. Sci. Fert. 42, 257–265.

    Google Scholar 

  • Tardy, V., Spor, A., Mathieu, O., Lévèque, J., Terrat, S., Plassart, P., Regnier, T., Bardgett, R.D., van der Putten, W.H., Roggero, P.P., et al. 2015. Shifts in microbial diversity through land use intensity as drivers of carbon mineralization in soil. Soil Biol. Biochem. 90, 204–213.

    Article  CAS  Google Scholar 

  • The R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

    Google Scholar 

  • Tsiafouli, M.A., Thébault, E., Sgardelis, S.P., de Ruiter, P.C., van der Putten, W.H., Birkhofer, K., Hemerik, L., de Vries, F.T., Bardgett, R.D., Brady, M.V., et al. 2015. Intensive agriculture reduces soil biodiversity across Europe. Glob. Change Biol. 21, 973–985.

    Article  Google Scholar 

  • Wall, D.H., Nielsen, U.N., and Six, J. 2015. Soil biodiversity and human health. Nature 528, 69–76.

    CAS  PubMed  Google Scholar 

  • Ward, N.L., Challacombe, J.F., Janssen, P.H., Henrissat, B., Coutinho, P.M., Wu, M., Xie, G., Haft, D.H., Sait, M., Badger, J., et al. 2009. Three genomes from the phylum Acidobacteria provide insight into the life styles of these microorganisms in soils. Appl. Environ. Microbiol. 75, 2046–2056.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weiss, J.V., Rentz, J.A., Plaia, T., Neubauer, S.C., Merrill-Floyd, M., Lilburn, T., Bradburne, C., Megonigal, J.P., and Emerson, D. 2007. Characterization of neutrophilic Fe(II)-oxidizing bacteria isolated from the rhizosphere of wetland plants and description of Ferritrophicum radicicola gen. nov. sp. nov., and Sideroxydans paludicola sp. nov. Geomicrobiol. J. 24, 559–570.

    Article  CAS  Google Scholar 

  • Won, K., Kook, M., and Yi, T.H. 2014. Terrabacter koreensis sp. nov., isolated from soil of a flowerbed. Int. J. Syst. Evol. Microbiol. 64, 3335–3340.

    Article  PubMed  Google Scholar 

  • Wu, M., Qin, H., Chen, Z., Wu, J., and Wei, W. 2011. Effect of longterm fertilization on bacterial composition in rice paddy soil. Biol. Fert. Soils 47, 397–405.

    Article  Google Scholar 

  • Ye, R., Doane, T.A., Morris, J., and Horwath, W.R. 2015. The effect of rice straw on the priming of soil organic matter and methane production in peat soils. Soil Biol. Biochem. 81, 98–107.

    Article  CAS  Google Scholar 

  • Yuan, H., Ge, T., Wu, X., Liu, S., Tong, C., Qin, H., Wu, M., Wei, W., and Wu, J. 2012. Long-term field fertilization alters the diversity of autotrophic bacteria based on the ribulose-1,5-biphosphate carboxylase/oxygenase (RubisCO) large-subunit genes in paddy soil. Appl. Microbiol. Biotechnol. 95, 1061–1071.

    Article  CAS  PubMed  Google Scholar 

  • Yuan, H., Ge, T., Zhou, P., Liu, S., Roberts, P., Zhu, H., Zou, Z., Tong, C., and Wu, J. 2013. Soil microbial biomass and bacterial and fungal community structures responses to long-term fertilization in paddy soils. J. Soils Sediments 13, 877–886.

    Article  Google Scholar 

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Correspondence to Hang-Yeon Weon.

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12275_2016_6463_MOESM2_ESM.xlsx

Supplementary data Table S1. Seasonal variability of the taxonomic distribution (indicated in percentage) of the bacterial 16S rRNAs obtained from the rice field soils fertilized differentially

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Ahn, JH., Lee, S.A., Kim, J.M. et al. Dynamics of bacterial communities in rice field soils as affected by different long-term fertilization practices. J Microbiol. 54, 724–731 (2016). https://doi.org/10.1007/s12275-016-6463-3

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