Characterization of the bacterial and archaeal communities in rice field soils subjected to long-term fertilization practices

Journal of Microbiology

Volumn 50, Issue 5, 2012, Pages 754-765

  Ahn, Jae Hyung ^a   Song, Jaekyeong ^a   Kim, Byung Yong ^a   Kim, Myung Sook ^a   Joa, Jae Ho ^b   Weon, Hang Yeon ^a  

^a National Institute of Animal Science   (South Korea)

^b Rural Development Administration   (South Korea)

Author keywords

archaea; bacteria; community; long term fertilization; pyrosequencing; rice field

Indexed keywords

EID: 84868541991     PISSN: 12258873     EISSN: 19763794     Source Type: Journal    
DOI: 10.1007/s12275-012-2409-6     Document Type: Article

References (83)

1. Ahamadou, B., Huang, Q., Chen, W., Wen, S., Zhang, J., Mohamed, I., Cai, P., and Liang, W. 2009. Microcalorimetric assessment of microbial activity in long-term fertilization experimental soils of Southern China. FEMS Microbiol. Ecol. 70, 186-195.
2. Allison, L. E. 1965. Organic carbon, pp. 1367-1376. In B. C. A. (ed.), Methods of soil analysis. Part II, Am. Soc. Agron. Inc. Publ., Madison, Wisconsin, USA.
3. Asakawa, S. and Kimura, M. 2008. Comparison of bacterial community structures at main habitats in paddy field ecosystem based on DGGE analysis. Soil Biol. Biochem. 40, 1322-1329.
4. Bannert, A., Kleineidam, K., Wissing, L., Mueller-Niggemann, C., Vogelsang, V., Welzl, G., Cao, Z., and Schloter, M. 2011. Changes in diversity and functional gene abundances of microbial communities involved in nitrogen fixation, nitrification, and denitrification in a tidal wetland versus paddy soils cultivated for different time periods. Appl. Environ. Microbiol. 77, 6109-6116.
5. Bartram, A. K., Lynch, M. D. J., Stearns, J. C., Moreno-Hagelsieb, G., and Neufeld, J. D. 2011. Generation of multimillion-sequence 16S rRNA gene libraries from complex microbial communities by assembling paired-end illumina reads. Appl. Environ. Microbiol. 77, 3846-3852.
6. Bittman, S., Forge, T. A., and Kowalenko, C. G. 2005. Responses of the bacterial and fungal biomass in a grassland soil to multiyear applications of dairy manure slurry and fertilizer. Soil Biol. Biochem. 37, 613-623.
7. 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.
8. Brochier-Armanet, C., Boussau, B., Gribaldo, S., and Forterre, P. 2008. Mesophilic crenarchaeota: Proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245-252.
9. Brochier-Armanet, C., Gribaldo, S., and Forterre, P. 2012. Spotlight on the Thaumarchaeota. ISME J. 6, 227-230.
10. Casida, L. E., Jr., Klein, D. A., and Santoro, T. 1964. Soil dehydrogenase activity. Soil Sci. 98, 371-376.
11. Chen, Z., Liu, J., Wu, M., Xie, X., Wu, J., and Wei, W. 2012. Differentiated response of denitrifying communities to fertilization regime in paddy soil. Microb. Ecol. 63, 446-459.
12. Chu, H., Lin, X., Fujii, T., Morimoto, S., Yagi, K., Hu, J., and Zhang, J. 2007. Soil microbial biomass, dehydrogenase activity, bacterial community structure in response to long-term fertilizer management. Soil Biol. Biochem. 39, 2971-2976.
13. Chun, J., Kim, K., Lee, J. H., and Choi, Y. 2010. The analysis of oral microbial communities of wild-type and toll-like receptor 2-deficient mice using a 454 GS FLX titanium pyrosequencer. BMC Microbiol. 10, 101.
14. Conrad, R. 2007. Microbial ecology of methanogens and methanotrophs. Adv. Agron. 96, 1-63.
15. Conrad, R., Erkel, C., and Liesack, W. 2006. Rice cluster I methanogens, an important group of Archaea producing greenhouse gas in soil. Curr. Opin. Biotech. 17, 262-267.
16. Conrad, R., Klose, M., and Noll, M. 2009. Functional and structural response of the methanogenic microbial community in rice field soil to temperature change. Environ. Microbiol. 11, 1844-1853.
17. Cui, J., Meng, H., Nie, M., Chen, X., Li, Z., Bu, N., Li, B., Chen, J., Quan, Z., and Fang, C. 2012. Bacterial succession during 500 years of soil development under agricultural use. Ecol. Res. 27, 793-807.
18. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C., and Knight, R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics27, 2194-2200.
19. Einen, J., Thorseth, I. H., and Øreås, L. 2008. Enumeration of Archaea and Bacteria in seafloor basalt using real-time quantitative PCR and fluorescence microscopy. FEMS Microbiol. Lett. 282, 182-187.
20. Enwall, K., Philippot, L., and Hallin, S. 2005. Activity and composition of the denitrifying bacterial community respond differently to long-term fertilization. Appl. Environ. Microbiol. 71, 8335-8343.
21. Golyshina, O. V., Yakimov, M. M., Lünsdorf, H., Ferrer, M., Nimtz, M., Timmis, K. N., Wray, V., Tindall, B. J., and Golyshin, P. N. 2009. Acidiplasma aeolicum gen. nov., sp. nov., a euryarchaeon of the family Ferroplasmaceae isolated from a hydrothermal pool, and transfer of Ferroplasma cupricumulans to Acidiplasma cupricumulans comb. nov. Int. J. Syst. Evol. Microbiol. 59, 2815-2823.
22. Grégoire, P., Bohli, M., Cayol, J.-L., Joseph, M., Guasco, S., Dubourg, K., Cambar, J., Michotey, V., Bonin, P., Fardeau, M.-L., andet al. 2011. Caldilinea tarbellica sp. nov., a filamentous, thermophilic, anaerobic bacterium isolated from a deep hot aquifer in the Aquitaine Basin. Int. J. Syst. Evol. Microbiol. 61, 1436-1441.
23. Großkopf, R., Stubner, S., and Liesack, W. 1998. Novel euryarchaeotal lineages detected on rice roots and in the anoxic bulk soil of flooded rice microcosms. Appl. Environ. Microbiol. 64, 4983-4989.
24. Gubry-Rangin, C., Nicol, G. W., and Prosser, J. I. 2010. Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol. Ecol. 74, 566-574.
25. Hahn, M. W. and Schauer, M. 2007. 'Candidatus Aquirestis calciphila' and 'Candidatus Haliscomenobacter calcifugiens', filamentous, planktonic bacteria inhabiting natural lakes. Int. J. Syst. Evol. Microbiol. 57, 936-940.
26. 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.
27. Hur, M., Kim, Y., Song, H. R., Kim, J. M., Choi, Y. I., and Yi, H. 2011. Effect of genetically modified poplars on soil microbial communities during the phytoremediation of waste mine tailings. Appl. Environ. Microbiol. 77, 7611-7619.
28. IPCC. 2007. IPCC fourth assessment report: climate change 2007 synthesis report. Geneva, Switzerland.
29. 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. Soils47, 599-604.
30. Jones, D. and Keddie, R. 2006. The Genus Arthrobacter, pp. 945-960. In Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K. H., and Stackebrandt, E. (eds.), The prokaryotes, Springer, New York, N. Y., USA.
31. Kämpfer, P. 2010. Genus III. Haliscomenobacter, pp. 25-469. In Krieg, N. R., Staley, J. T., Brown, D. R., Hedlund, B. P., Paster, B. J., Ward, N. L., Ludwig, W., and Whitman, W. B. (eds.), Bergey's manual of systematic bacteriology, Springer, New York, N. Y., USA.
32. Kendall, M. M., Wardlaw, G. D., Tang, C. F., Bonin, A. S., Liu, Y., and Valentine, D. L. 2007. Diversity of Archaea in marine sediments from Skan Bay, Alaska, including cultivated methanogens, and description of Methanogenium boonei sp. nov. Appl. Environ. Microbiol. 73, 407-414.
33. Kikuchi, H., Watanabe, T., Jia, Z., Kimura, M., and Asakawa, S. 2007. Molecular analyses reveal stability of bacterial communities in bulk soil of a Japanese paddy field: Estimation by denaturing gradient gel electrophoresis of 16S rRNA genes amplified from DNA accompanied with RNA. Soil Sci. Plant Nutr. 53, 448-458.
34. Kim, M. S., Ahn, J. H., Jung, M. K., Yu, J. H., Joo, D., Kim, M. C., Shin, H. Y., Kim, T., Ryu, T. H., Kweon, S. J., andet al. 2005. Molecular and cultivation-based characterization of bacterial community structure in rice field soil. J. Microbiol. Biotechnol. 15, 1087-1093.
35. Kim, J. G., Jung, M. Y., Park, S. J., Rijpstra, W. I. C., Sinninghe Damsté, J. S., Madsen, E. L., Min, D., Kim, J. S., Kim, G. J., and Rhee, S. K. 2012. Cultivation of a highly enriched ammonia-oxidizing archaeon of thaumarchaeotal group I. 1b from an agricultural soil. Environ. Microbiol. 14, 1528-1543.
36. Kögel-Knabner, I., Amelung, W., Cao, Z., Fiedler, S., Frenzel, P., Jahn, R., Kalbitz, K., Kölbl, A., and Schloter, M. 2010. Biogeochemistry of paddy soils. Geoderma. 157, 1-14.
37. Kolganova, T. V., Kuznetsov, B. B., and Turova, T. P. 2002. Designing and testing oligonucleotide primers for amplification and sequencing of archaeal 16S rRNA genes. Mikrobiologiia71, 283-286.
38. Lauber, C. L., Hamady, M., Knight, R., and Fierer, N. 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 75, 5111-5120.
39. Lee, S. H., Kim, C. G., and Kang, H. 2011. Temporal dynamics of bacterial and fungal communities in a genetically modified (GM) rice ecosystem. Microb. Ecol. 61, 646-659.
40. Letunic, I. and Bork, P. 2011. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 39, W475-W478.
41. Liesack, W., Schnell, S., and Revsbech, N. P. 2000. Microbiology of flooded rice paddies. FEMS Microbiol. Rev. 24, 625-645.
42. Lozupone, C. A. and Knight, R. 2008. Species divergence and the measurement of microbial diversity. FEMS Microbiol. Rev. 32, 557-578.
43. Lu, Y., Rosencrantz, D., Liesack, W., and Conrad, R. 2006. Structure and activity of bacterial community inhabiting rice roots and the rhizosphere. Environ. Microbiol. 8, 1351-1360.
44. Lüdemann, H., Arth, I., and Liesack, W. 2000. Spatial changes in the bacterial community structure along a vertical oxygen gradient in flooded paddy soil cores. Appl. Environ. Microbiol. 66, 754-762.
45. Ludwig, W., Strunk, O., Klugbauer, S., Klugbauer, N., Weizenegger, M., Neumaier, J., Bachleitner, M., and Schleifer, K. H. 1998. Bacterial phylogeny based on comparative sequence analysis. Electrophoresis19, 554-568.
46. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner, A., Lai, T., Steppi, S., Jobb, G., andet al. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371.
47. Lueders, T. and Friedrich, M. 2000. Archaeal population dynamics during sequential reduction processes in rice field soil. Appl. Environ. Microbiol. 66, 2732-2742.
48. Marschner, P., Kandeler, E., and Marschner, B. 2003. Structure and function of the soil microbial community in a long-term fertilizer experiment. Soil Biol. Biochem. 35, 453-461.
49. McDonald, D., Price, M. N., Goodrich, J., Nawrocki, E. P., DeSantis, T. Z., Probst, A., Andersen, G. L., Knight, R., and Hugenholtz, P. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 6, 610-618.
50. Muyzer, G., de Waal, E. C., and Uitterlinden, A. G. 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59, 695-700.
51. Nemergut, D. R., Townsend, A. R., Sattin, S. R., Freeman, K. R., Fierer, N., Neff, J. C., Bowman, W. D., Schadt, C. W., Weintraub, M. N., and Schmidt, S. K. 2008. The effects of chronic nitrogen fertilization on alpine tundra soil microbial communities: implications for carbon and nitrogen cycling. Environ. Microbiol. 10, 3093-3105.
52. NIAST (National Institute of Agricultural Science and Technology). 2000. Methods of analysis of soil and plant. NIAST, Suwon, Korea (in Korean).
53. Nicol, G. W., Leininger, S., Schleper, C., and Prosser, J. I. 2008. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ. Microbiol. 10, 2966-2978.
54. Noll, M., Matthies, D., Frenzel, P., Derakshani, M., and Liesack, W. 2005. Succession of bacterial community structure and diversity in a paddy soil oxygen gradient. Environ. Microbiol. 7, 382-395.
55. Pedrazzini, F. R. and McKee, K. L. 1984. Effect of flooding on activities of soil dehydrogenases and alcohol dehydrogenase in rice (Oryza Sativa L.) roots. Soil Sci. Plant Nutr. 30, 359-366.
56. Pester, M., Schleper, C., and Wagner, M. 2011. The Thaumarchaeota: An emerging view of their phylogeny and ecophysiology. Curr. Opin. Microbiol. 14, 300-306.
57. Podosokorskaya, O. A., Bonch-Osmolovskaya, E. A., Novikov, A. A., Kolganova, T. V., and Kublanov, I. V. 2012. Ornatilinea apprima gen. nov., sp. nov., a novel cellulolytic representative of class Anaerolineae. Int. J. Syst. Evol. Microbiol. Article in press.
58. 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.
59. Pruesse, E., Peplies, J., and Glöckner, F. O. 2012. SINA: accurate high throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics Article in press.
60. Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J., and Glöckner, F. O. 2007. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188-7196.
61. Quince, C., Lanzen, A., Davenport, R., and Turnbaugh, P. 2011. Removing noise from pyrosequenced amplicons. BMC Bioinformatics12, 38.
62. Ramakrishnan, B., Lueders, T., Dunfield, P. F., Conrad, R., and Friedrich, M. W. 2001. Archaeal community structures in rice soils from different geographical regions before and after initiation of methane production. FEMS Microbiol. Ecol. 37, 175-186.
63. Reysenbach, A. 2001. Class IV. Thermoplasmata class. nov., pp. 335-340. In. Boone, D. R and Castenholz, R. W. (eds.), Bergey's manual of systematic bacteriology, Springer, New York, N. Y., USA.
64. Roesch, L. F. W., Fulthorpe, R. R., Riva, A., Casella, G., Hadwin, A. K. M., Kent, A. D., Daroub, S. H., Camargo, F. A. O., Farmerie, W. G., and Triplett, E. W. 2007. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1, 283-290.
65. Ross, D. J. 1971. Some factors influencing the estimation of dehydrogenase activities of some soils under pasture. Soil Biol. Biochem. 3, 97-110.
66. Rousk, J., Baath, E., Brookes, P. C., Lauber, C. L., Lozupone, C., Caporaso, J. G., Knight, R., and Fierer, N. 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 4, 1340-1351.
67. Sakai, S., Conrad, R., Liesack, W., and Imachi, H. 2010. Methanocella arvoryzae sp. nov., a hydrogenotrophic methanogen isolated from rice field soil. Int. J. Syst. Evol. Microbiol. 60, 2918-2923.
68. Sakai, S., Imachi, H., Hanada, S., Ohashi, A., Harada, H., and Kamagata, Y. 2008. Methanocella paludicola gen. nov., sp. nov., a methane-producing archaeon, the first isolate of the lineage 'Rice Cluster I', and proposal of the new archaeal order Methanocellales ord. nov. Int. J. Syst. Evol. Microbiol. 58, 929-936.
69. 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., andet al. 2009. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541.
70. Shen, J. P., Zhang, L. M., Guo, J. F., Ray, J. L., and He, J. Z. 2010. Impact of long-term fertilization practices on the abundance and composition of soil bacterial communities in Northeast China. Appl. Soil Ecol. 46, 119-124.
71. Šimek, M. and Hopkins, D. W. 1999. Regulation of potential denitrification by soil pH in long-term fertilized arable soils. Biol. Fert. Soils30, 41-47.
72. Subhani, A., Changyong, H., Zhengmiao, X., Min, L., and EI-gharmry, A. M. 2001. Impact of soil environment and agronomic practices on microbial/dehydrogenase enzyme activity in soil. A review. Pak. J. Biol. Sci. 4, 333-338.
73. 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.
74. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739.
75. van Breemen, N., Burrough, P. A., Velthorst, E. J., van Dobben, H. F., de Wit, T., Ridder, T. B., and Reijnders, H. F. R. 1982. Soil acidification from atmospheric ammonium sulphate in forest canopy throughfall. Nature299, 548-550.
76. Wang, Y., Ke, X., Wu, L., and Lu, Y. 2009. Community composition of ammonia-oxidizing bacteria and archaea in rice field soil as affected by nitrogen fertilization. Syst. Appl. Microbiol. 32, 27-36.
77. Wang, G., Watanabe, T., Jin, J., Liu, X., Kimura, M., and Asakawa, S. 2010. Methanogenic archaeal communities in paddy field soils in north-east China as evaluated by PCR-DGGE, sequencing and real-time PCR analyses. Soil Sci. Plant Nutr. 56, 831-838.
78. Watanabe, T., Wang, G., Taki, K., Ohashi, Y., Kimura, M., and Asakawa, S. 2010. Vertical changes in bacterial and archaeal communities with soil depth in Japanese paddy fields. Soil Sci. Plant Nutr. 56, 705-715.
79. Wright, E. S., Yilmaz, L. S., and Noguera, D. R. 2012. DECIPHER, a search-based approach to chimera identification for 16S rRNA sequences. Appl. Environ. Microbiol. 78, 717-725.
80. Wu, M., Qin, H., Chen, Z., Wu, J., and Wei, W. 2011. Effect of long-term fertilization on bacterial composition in rice paddy soil. Biol. Fert. Soils47, 397-405.
81. Yao, H., Gao, Y., Nicol, G. W., Campbell, C. D., Prosser, J. I., Zhang, L., Han, W., and Singh, B. K. 2011. Links between ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Appl. Environ. Microbiol. 77, 4618-4625.
82. Yeon, B. Y., Kwak, H. K., Huh, B. L., Hong, C. W., and Lee, J. H. 1997. Influence of long term application of compost, lime and silicate fertilizer on some properites of paddy soil. RDA. J. Agro-Envir. Sci. 39, 9-15 (in Korean).
83. Yeon, B. Y., Kwak, H. K., Song, Y. S., Jun, H. J., Cho, H. J., and Kim, C. H. 2007. Changes in rice yield and soil organic matter content under continued application of rice straw compost for 50 years in paddy soil. Korean J. Soil. Sci. Fert. 40, 454-459 (in Korean).