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Diversity of methanogenic archaeal communities in Japanese paddy field ecosystem, estimated by denaturing gradient gel electrophoresis

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An Erratum to this article was published on 07 April 2011

Abstract

Diversity of methanogenic archaeal communities in Japanese paddy field ecosystem was evaluated by the denaturing gradient gel electrophoresis (DGGE) after PCR amplification of the 16S rRNA genes (16S rDNAs), sequencing analysis and data evaluation by principal component analysis. Data were obtained from samples collected from the plowed soil layer, rice roots, rice straws incorporated in soil, plant residues (mixture of weeds, rice litters, rice roots, and rice stubbles) in soil, and composing rice straw. The number of bands of DGGE profiles ranged from 12 to 26 with the highest numbers in rice roots and rice straws incorporated in soil. However, the diversity indices based on both the numbers and intensity of bands indicated that the community of the plowed soil layer was the most diverse, even, and stable. Sequencing of the main DGGE bands showed the presence of Methanomicrobiales, Methanosarcinales, Methanobacteriaceae, and Methanocellales. The plowed soil layer included all phylogenetic groups of the methanogenic archaea of the other studied habitats, with prevalence of the members of Methanomicrobiales and Methanocellales. The phylogenetic diversity was compared with that of paddy soils collected in Italy, China, and the Philippines and that of 12 anaerobic environments (fen, waste, coast, permafrost, natural gas field, bovine rumen, riparian soil, termite, ciliate endosymboints, lake sediment, landfill, and seep rumen). The phylogenetic diversity was more similar among paddy soils than with the other anaerobic environments. Probably, the methanogenic archaeal communities of the paddy field soils were characterized by indigenous members and some of the members of the community of the plowed soil layer colonized rice roots, rice straws, and plant residues.

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References

  • Aoki S (1996) Black-box: data analysis on the www. <http://aoki2.si.gunma-u.ac.jp/BlackBox/BlackBox.html>

  • Asakawa S, 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. doi:10.1016/j.soilbio.2007.09.024

    Article  CAS  Google Scholar 

  • Cahyani VR, Watanabe A, Matsuya K, Asakawa S, Kimura M (2002) Succession of microbiota estimated by phospholipid fatty acid analysis and changes in organic constituents during the composting process of rice straw. Soil Sci Plant Nutr 48:735–743

    CAS  Google Scholar 

  • Cahyani VR, Matsuya K, Asakawa S, Kimura M (2003) Succession and phylogenetic composition of bacterial communities responsible for the composting process of rice straw estimated by PCR-DGGE analysis. Soil Sci Plant Nutr 49:619–630

    CAS  Google Scholar 

  • Cahyani VR, Matsuya K, Asakawa S, Kimura M (2004) Succession and phylogenetic profile of methanogenic archaeal communities during the composting process of rice straw estimated by PCR-DGGE analysis. Soil Sci Plant Nutr 50:555–563

    CAS  Google Scholar 

  • Conrad R (2007) Micorbial ecology of methanogens and methanotrophs. Adv Agron 96:1–63. doi:10.1016/S0065-2113(07)96005-8

    Article  CAS  Google Scholar 

  • Conrad R, Frenzel P (2002) Flooded soils. In: Bitton G (ed) Encyclopedia of Environmental Microbiology, vol 3. Wiley, New York, pp 1316–1333

    Google Scholar 

  • Conrad R, Erkel C, Liesack W (2006) Rice Cluster I methanogens, an important group of Archaea producing greenhouse gas in soil. Curr Opin Biotechnol 17:262–267. doi:10.1016/j.copbio.2006.04.002

    Article  PubMed  CAS  Google Scholar 

  • Conrad R, Klose M, Noll M, Kemnitz D, Bodelier PLE (2008) Soil type links microbial colonization of rice roots to methane emission. Global Change Biol 14:657–669. doi:10.1111/j.1365-2486.2007.01516.x

    Article  Google Scholar 

  • de Lipthay JR, Enzinger C, Johnsen K, Aamand J, Sørensen SJ (2004) Impact of DNA extraction method on bacterial community composition measured by denaturing gradient gel electrophoresis. Soil Biol Biochem 36:1607–1614. doi:10.1016/j.soilbio.2004.03.011

    Article  Google Scholar 

  • Fromin N, Hamelin J, Tarnawski S, Roesti D, Jourdain-Miserez K, Forestier N, Teyssier-Cuvelle S, Gillet F, Aragno M, Rossi P (2002) Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environ Microbiol 4:634–643

    Article  PubMed  CAS  Google Scholar 

  • Galand PE, Fritze H, Yrjälä K (2003) Microsite-dependent changes in methanogenic populations in a boreal oligotrophic fen. Environ Microbiol 5:1133–1143. doi:10.1046/j.1462-2920.2003.00520.x

    Article  PubMed  Google Scholar 

  • Ganzert L, Jurgens G, Münster U, Wagner D (2007) Methanogenic communities in permafrost-affected soils of the Laptev Sea coast, Siberian Arctic, characterized by 16S rRNA gene fingerprints. FEMS Microbiol Ecol 59:476–488. doi:10.1111/j.1574-6941.2006.00205.x

    Article  PubMed  CAS  Google Scholar 

  • Garrity GM, Bell JA, Lilburn T (2005) The revised road map to the manual. Bergey’s Manual of Systematic Bacteriology. In: Garrity GM (ed) The Proteobacteria, Part A, Introductory essays, vol 2, 2nd edn. Springer, New York, pp 159–206

    Google Scholar 

  • Glissmann K, Conrad R (2000) Fermentation pattern of methanogenic degradation of rice straw in anoxic paddy soil. FEMS Microbiol Ecol 31:117–126

    Article  PubMed  CAS  Google Scholar 

  • Großkopf R, Janssen PH, Liesack W (1998) Diversity and structure of the methanogenic community in anoxic rice paddy soil microcosm as examined by cultivation and direct 16 S rRNA gene sequence retrieval. Appl Environ Microbiol 64:960–969

    PubMed  Google Scholar 

  • Hashimoto-Yasuda T, Ikenaga M, Asakawa S, Kim H-Y, Okada M, Kobayashi K, Kimura M (2005) Effect of free-air CO2 enrichment (FACE) on methanogenic archaeal communities inhabiting rice roots in Japanese rice field. Soil Sci Plant Nutr 51:91–100

    Article  CAS  Google Scholar 

  • Hirota T (2001) Statistical macros for Excel. < http://sci.kj.yamagata-u.ac.jp/∼columbo/Stat/>

  • Ikenaga M, Muraoka Y, Toyota K, Kimura M (2002) Community structure of the microbiota associated with nodal roots of rice plants along with the growth stages: estimation by PCR-RFLP analysis. Biol Fertil Soils 36:397–404. doi:10.1007/s00374-002-0543-8

    Article  CAS  Google Scholar 

  • Ikenaga M, Asakawa S, Muraoka Y, Kimura M (2003) Bacterial communities associated with nodal roots of rice plant along with the growth stages: estimation by PCR-DGGE and sequence analyses. Soil Sci Plant Nutr 49:591–602

    CAS  Google Scholar 

  • Ikenaga M, Asakawa S, Muraoka Y, Kimura M (2004) Methanogenic archaeal communities in rice roots grown in flooded soil pots: estimation by PCR-DGGE and Sequencing analyses. Soil Sci Plant Nutr 50:701–711

    CAS  Google Scholar 

  • Jackson CR, Harper JP, Willoughby D, Roden EE, Churchill PF (1997) A simple, efficient method for the separation of humic substances and DNA from environmental samples. Appl Environ Microbiol 63:4993–4995

    PubMed  CAS  Google Scholar 

  • Kemnitz D, Chin K-J, Bodelier P, Conrad R (2004) Community analysis of methanogenic archaea within a riparian flooding gradient. Environ Microbiol 6:449–461. doi:10.1111/j.1462-2920.2004.00573.x

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (2000) Anaerobic microbiology in waterlogged rice fields. In: Bollag J-M, Stotzky G (eds) Soil Biochemistry, vol 10. Marcel Dekker, New York, pp 35–138

    Google Scholar 

  • Kimura M, Asakawa S (2006) Comparison of community structures of microbiota at main habitats in rice field ecosystems based on phospholipid fatty acid analysis. Biol Fertil Soils 43:20–29. doi:10.1007/s00374-005-0057-2

    Article  CAS  Google Scholar 

  • Kimura M, Wada H, Takai Y (1977) Study of rice rhizosphere IV—chemical property of rhizosphere soil. Jpn J Soil Sci Plant Nutr 48:540–545 (in Japanese)

    Google Scholar 

  • Kimura M, Murakami H, Wada H (1990) CO2, H2, and CH4 production in rice rhizosphere. Soil Sci Plant Nutr 37:55–60

    Google Scholar 

  • Kimura M, Murase J, Lu Y (2004) Carbon cycling in rice field ecosystems in the context of input, decomposition and translocation of organic materials and the fates of their end products (CO2 and CH4). Soil Biol Biochem 36:1399–1416. doi:10.1016/j.soilbio.2004.03.006

    Article  CAS  Google Scholar 

  • Koizumi Y, Takii S, Fukui M (2004) Depth-related change in archaeal community structure in a freshwater lake sediment as determined with denaturing gradient gel electrophoresis of amplified 16S rRNA genes and reversely transcribed rRNA fragments. FEMS Microbiol Ecol 48:285–292. doi:10.1016/j.femsec.2004.02.013

    Article  PubMed  CAS  Google Scholar 

  • Lehmann-Richter S, Großkopf R, Liesack W, Frenzel P, Conrad R (1999) Methanogenic archaea and CO2-dependent methanogenesis on washed rice roots. Environ Microbiol 1:159–166

    Article  PubMed  CAS  Google Scholar 

  • Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10

    Article  CAS  Google Scholar 

  • Magurran AE (1988) Ecological Diversity and its Measurement. Croom Helm, London

    Google Scholar 

  • Matsuyama T, Nakajima Y, Matsuya K, Ikenaga M, Asakawa S, Kimura M (2007) Bacterial community in plant residues in a Japanese paddy field estimated by RFLP and DGGE analyses. Soil Biol Biochem 39:463–472. doi:10.1016/j.soilbio.2006.08.016

    Article  CAS  Google Scholar 

  • Mochimaru H, Yoshioka H, Tamaki H, Nakamura K, Kaneko N, Sakata S, Imachi H, Sekiguchi Y, Uchiyama H, Kamagata Y (2007) Microbial diversity and methanogenic potential in a high temperature natural gas field in Japan. Extremophiles 11:453–461. doi:10.1007/s00792-006-0056-8

    Article  PubMed  CAS  Google Scholar 

  • Mori K, Sparling R, Hatsu M, Takamizawa K (2003) Quantification and diversity of the archaeal community in a landfill site. Can J Microbiol 49:28–36. doi:10.1139/W03-006

    Article  PubMed  CAS  Google Scholar 

  • Munson MA, Nedwell DB, Embley TM (1997) Phylogenetic diversity of Archaea in sediment samples from a coastal salt marsh. Appl Environ Microbiol 63:4729–4733

    PubMed  CAS  Google Scholar 

  • Murayama S (1984) Changes in the monosaccharide composition during the decomposition of straws under field conditions. Soil Sci Plant Nutr 30:367–381

    CAS  Google Scholar 

  • Ohkuma M, Noda S, Kudo T (1999) Phylogenetic relationships of symbiotic methanogens in diverse termites. FEMS Microbiol Lett 171:147–153

    Article  PubMed  CAS  Google Scholar 

  • Ramakrishnan B, Lueders T, Dunfield PF, Conrad R, Friedrich MW (2001) Archaeal community structures in rice soils from different geographical regions before and after initiation of methane production. FEMS Microbiol Ecol 37:175–186. doi:10.1111/j.1574-6941.2001.tb00865.x

    Article  CAS  Google Scholar 

  • Sakai S, Imachi H, Sekiguchi Y, Ohashi A, Harada H, Kamagata Y (2007) Isolation of key methanogens for global methane emission from rice paddy fields: a novel isolate affiliated with the clone cluster rice cluster I. Appl Environ Microbiol 73:4326–4331. doi:10.1128/AEM.03008-06

    Article  PubMed  CAS  Google Scholar 

  • Sekiguchi H, Tomioka N, Nakahara T, Uchiyama H (2001) A single band does not always represent single bacterial strains in denaturing gradient gel electrophoresis analysis. Biotechnol Lett 23:1205–1208

    Article  CAS  Google Scholar 

  • Skillman LC, Evans PN, Strömpl C, Joblin KN (2006) 16S rDNA directed PCR primers and detection of methanogens in the bovine rumen. Lett Appl Microbiol 42:222–228. doi:10.1111/j.1472-765X.2005.01833.x

    Article  PubMed  CAS  Google Scholar 

  • Suga Y, Hori K, Komori S, Fukunaga A, Ikeda J, Toyota K (2008) Simple and rapid DNA extraction method from plant roots for analysis of bacterial community structure. Soil Microorganisms 62:121–125 (in Japanese)

    Google Scholar 

  • Sugano A, Tsuchimoto H, Tun CC, Kimura M, Asakawa S (2005a) Succession of methanogenic archaea in rice straw incorporated into a Japanese rice field: estimation by PCR-DGGE and sequencing analyses. Archaea 1:391–397

    Article  PubMed  CAS  Google Scholar 

  • Sugano A, Tsuchimoto H, Tun CC, Asakawa S, Kimura M (2005b) Succession and phylogenetic profile of eubacterial communities in rice straw incorporated into a rice field: estimation by PCR-DGGE analysis. Soil Sci Plant Nutr 51:51–60

    Article  CAS  Google Scholar 

  • Tang Y-Q, Shigematsu T, Morimura S, Kida K (2007) Effect of dilution rate on the microbial structure of a mesophilic butyrate-degrading methanogenic community during continuous cultivation. Appl Microbiol Biotechnol 75:451–465. doi:10.1007/s00253-006-0819-2

    Article  PubMed  CAS  Google Scholar 

  • Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA (1982) Denitrification: ecological niches, competition and survival. Antonie Van Leeuwenhoek 48:569–583

    Article  PubMed  CAS  Google Scholar 

  • Tsutsuki K, Ponnamperuma FN (1987) Behavior of anaerobic decomposition products in submerged soils—effects of organic material amendment, soil properties, and temperature. Soil Sci Plant Nutr 33:13–33

    CAS  Google Scholar 

  • Tun CC, Ikenaga M, Asakawa S, Kimura M (2002) Community structure of bacteria and fungi responsible for rice straw decomposition in a paddy field estimated by PCR-RFLP analysis. Soil Sci Plant Nutr 48:805–813

    Google Scholar 

  • van Hoek AHAM, van Alen TA, Sprakel VSI, Leunissen JAM, Brigge T, Vogels GD, Hackstein JHP (2000) Multiple acquisition of methanogenic archaeal symboints by anaerobic ciliates. Mol Biol Evol 17:251–258

    PubMed  Google Scholar 

  • Watanabe A, Katoh K, Kimura M (1993) Effect of rice straw application on CH4 emission from paddy fields. II. Contribution of organic constituents in rice straw. Soil Sci Plant Nutr 39:707–712

    CAS  Google Scholar 

  • Watanabe T, Asakawa S, Nakamura A, Nagaoka K, Kimura M (2004) DGGE method for analyzing 16S rDNA of methanogenic archaeal community in paddy field soil. FEMS Microbiol Lett 232:153–163. doi:10.1016/S0378-1097(04)00045-X

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T, Kimura M, Asakawa S (2006) Community structure of methanogenic archaea in paddy field soil under double cropping (rice-wheat). Soil Biol Biochem 38:1264–1274. doi:10.1016/j.soilbio.2005.09.020

    Article  CAS  Google Scholar 

  • Watanabe T, Kimura M, Asakawa S (2007) Dynamics of methanogenic archaeal communities based on rRNA analysis and their relation to methanogenic activity in Japanese paddy field soils. Soil Biol Biochem 39:2877–2887. doi:10.1016/j.soilbio.2007.05.030

    Article  CAS  Google Scholar 

  • Wright A-DG, Toovey AF, Pimm CL (2006) Molecular identification of methanogenic archaea from sheep in Queensland, Australia reveal more uncultured novel archaea. Anaerobe 12:134–139. doi:10.1016/j.anaerobe.2006.02.002

    Article  PubMed  CAS  Google Scholar 

  • Yoo C-H, So J-D, Ida A, Tanaka F, Nishida M (1992) Effect of long-term organic matter application on the fine textured paddy soils of double cropping system in temperate area. J Korean Soc Soil Sci Fertil 25:325–333 (in Korean language, with English summary)

    CAS  Google Scholar 

  • Zinder SH (1993) Physiological ecology of methanogens. In: Ferry JG (ed) Methanogenesis. Ecology, Physiology, Biochemistry and Genetics. Chapman and Hall, New York, pp 128–206

    Google Scholar 

Download references

Acknowledgement

This work was partly supported by a Grant-in-Aid for Scientific Research and JSPS Fellows (19·6611) of the Japan Society for the Promotion of Science.

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  1. Laboratory of Soil Biology and Chemistry, Graduate School of Bioagricultural Sciences, Nagoya University, Chikusa, Nagoya, 464-8601, Japan

    Takeshi Watanabe, Makoto Kimura & Susumu Asakawa

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  1. Takeshi Watanabe
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  2. Makoto Kimura
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Correspondence to Takeshi Watanabe.

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An erratum to this article can be found online at http://dx.doi.org/10.1007/s00374-011-0560-6

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Watanabe, T., Kimura, M. & Asakawa, S. Diversity of methanogenic archaeal communities in Japanese paddy field ecosystem, estimated by denaturing gradient gel electrophoresis. Biol Fertil Soils 46, 343–353 (2010). https://doi.org/10.1007/s00374-009-0435-2

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