Dynamics of the Methanogenic Archaeal Community during Plant Residue Decomposition in an Anoxic Rice Field Soil

ABSTRACT Incorporation of plant residues strongly enhances the methane production and emission from flooded rice fields. Temperature and residue type are important factors that regulate residue decomposition and CH4 production. However, the response of the methanogenic archaeal community to these factors in rice field soil is not well understood. In the present experiment, the structure of the archaeal community was determined during the decomposition of rice root and straw residues in anoxic rice field soil incubated at three temperatures (15°C, 30°C, and 45°C). More CH4 was produced in the straw treatment than root treatment. Increasing the temperature from 15°C to 45°C enhanced CH4 production. Terminal restriction fragment length polymorphism analyses in combination with cloning and sequencing of 16S rRNA genes showed that Methanosarcinaceae developed early in the incubations, whereas Methanosaetaceae became more abundant in the later stages. Methanosarcinaceae and Methanosaetaceae seemed to be better adapted at 15°C and 30°C, respectively, while the thermophilic Methanobacteriales and rice cluster I methanogens were significantly enhanced at 45°C. Straw residues promoted the growth of Methanosarcinaceae, whereas the root residues favored Methanosaetaceae. In conclusion, our study revealed a highly dynamic structure of the methanogenic archaeal community during plant residue decomposition. The in situ concentration of acetate (and possibly of H2) seems to be the key factor that regulates the shift of methanogenic community.

[1]  M. Kimura,et al.  Contribution of rice straw carbon to CH4 emission from rice paddies using 13C‐enriched rice straw , 1998 .

[2]  W. Liesack,et al.  Novel Euryarchaeotal Lineages Detected on Rice Roots and in the Anoxic Bulk Soil of Flooded Rice Microcosms , 1998, Applied and Environmental Microbiology.

[3]  P. Puget,et al.  Short‐Term Dynamics of Root‐ and Shoot‐Derived Carbon from a Leguminous Green Manure , 2001 .

[4]  R. Reinhardt,et al.  Retrieval of first genome data for rice cluster I methanogens by a combination of cultivation and molecular techniques. , 2005, FEMS microbiology ecology.

[5]  R. Conrad,et al.  Effect of Temperature on Carbon and Electron Flow and on the Archaeal Community in Methanogenic Rice Field Soil , 2000, Applied and Environmental Microbiology.

[6]  C. Buenoa,et al.  Methanogenic responses to exogenous substrates in anaerobic rice soils , 2022 .

[7]  R. Conrad,et al.  Activity, structure and dynamics of the methanogenic archaeal community in a flooded Italian rice field. , 2005, FEMS microbiology ecology.

[8]  M. Kimura,et al.  DGGE method for analyzing 16S rDNA of methanogenic archaeal community in paddy field soil. , 2004, FEMS microbiology letters.

[9]  F. Ponnamperuma,et al.  Behavior of anaerobic decomposition products in submerged soils, effects of organic material amendment, soil properties, and temperature. , 1987 .

[10]  R. Conrad,et al.  Diversity and ubiquity of thermophilic methanogenic archaea in temperate anoxic soils. , 2006, Environmental microbiology.

[11]  R. Conrad,et al.  Functional patterns and temperature response of cellulose-fermenting microbial cultures containing different methanogenic communities , 2001, Applied Microbiology and Biotechnology.

[12]  M. Kimura,et al.  Microscopic observation of the decomposition process of leaf sheath of rice straw and colonizing microorganisms during the cultivation period of paddy rice , 1999 .

[13]  J. Wiegel.  Temperature spans for growth: Hypothesis and discussion , 1990 .

[14]  M. Winfrey,et al.  Temperature limitation of methanogenesis in aquatic sediments , 1976, Applied and environmental microbiology.

[15]  M. Kimura,et al.  Effect of Rice Straw Application on CH_4 Emission from Paddy Fields : II. Contribution of Organic Constituents in Rice Straw , 1993 .

[16]  R. Conrad.  Control of microbial methane production in wetland rice fields , 2002, Nutrient Cycling in Agroecosystems.

[17]  R. Conrad.  Contribution of hydrogen to methane production and control of hydrogen concentrations in methanogenic soils and sediments , 1999 .

[18]  Y. Kamagata,et al.  Isolation of Key Methanogens for Global Methane Emission from Rice Paddy Fields: a Novel Isolate Affiliated with the Clone Cluster Rice Cluster I , 2007, Applied and Environmental Microbiology.

[19]  M. Kimura,et al.  Carbon dynamics of rhizodeposits, root- and shoot-residues in a rice soil , 2003 .

[20]  H. Blume,et al.  Page, A. L., R. H. Miller and D. R. Keeney (Ed., 1982): Methods of soil analysis; 2. Chemical and microbiological properties, 2. Aufl. 1184 S., American Soc. of Agronomy (Publ.), Madison, Wisconsin, USA, gebunden 36 Dollar. , 1985 .

[21]  R. Conrad,et al.  Thermophilic methanogens in rice field soil. , 2001, Environmental microbiology.

[22]  R. Conrad,et al.  Archaeal Community Structure and Pathway of Methane Formation on Rice Roots , 2003, Microbial Ecology.

[23]  R. Conrad,et al.  Methanogenic Pathway and Archaeal Community Structure in the Sediment of Eutrophic Lake Dagow: Effect of Temperature , 2004, Microbial Ecology.

[24]  H. Neue,et al.  Influence of organic matter incorporation on the methane emission from a wetland rice field , 1995 .

[25]  P. Claus,et al.  Temporal change of 13C-isotope signatures and methanogenic pathways in rice field soil incubated anoxically at different temperatures , 2004 .

[26]  R. Conrad,et al.  Localization of processes involved in methanogenic degradation of rice straw in anoxic paddy soil. , 2001, Environmental microbiology.

[27]  R. Conrad,et al.  Dynamics of the methanogenic archaeal community in anoxic rice soil upon addition of straw , 2006 .

[28]  R. Conrad,et al.  Detecting active methanogenic populations on rice roots using stable isotope probing. , 2005, Environmental microbiology.

[29]  T. Lueders,et al.  Enhanced sensitivity of DNA- and rRNA-based stable isotope probing by fractionation and quantitative analysis of isopycnic centrifugation gradients. , 2003, Environmental microbiology.

[30]  Conrad,et al.  Fermentation pattern of methanogenic degradation of rice straw in anoxic paddy soil. , 2000, FEMS microbiology ecology.

[31]  Jurgens,et al.  Identification of novel Archaea in bacterioplankton of a boreal forest lake by phylogenetic analysis and fluorescent in situ hybridization(1). , 2000, FEMS microbiology ecology.

[32]  R. Conrad,et al.  Archaeal community structures in rice soils from different geographical regions before and after initiation of methane production , 2001 .

[33]  R. Conrad,et al.  Effect of Temperature on Structure and Function of the Methanogenic Archaeal Community in an Anoxic Rice Field Soil , 1999, Applied and Environmental Microbiology.

[34]  H. Akasaka,et al.  Phylogeny of numerically abundant culturable anaerobic bacteria associated with degradation of rice plant residue in Japanese paddy field soil. , 2003, FEMS microbiology ecology.

[35]  M. Kimura,et al.  Effect of rice straw application on CH4 emission from paddy fields , 1993 .

[36]  Stephan Stubner,et al.  Structure and function of the methanogenic archaeal community in stable cellulose-degrading enrichment cultures at two different temperatures (15 and 30°C) , 1999 .

[37]  W. Liesack,et al.  Diversity and Structure of the Methanogenic Community in Anoxic Rice Paddy Soil Microcosms as Examined by Cultivation and Direct 16S rRNA Gene Sequence Retrieval , 1998, Applied and Environmental Microbiology.

[38]  Alfons J. M. Stams,et al.  Acetate threshold values and acetate activating enzymes in methanogenic bacteria , 1990 .

[39]  R. A. Rasmussen,et al.  Factors affecting methane emissions from rice fields , 1998 .

[40]  K. Giller,et al.  Driven by Nature: Plant Litter Quality and Decomposition , 1996 .

[41]  M. Kimura,et al.  Evaluation of origins of CH4 carbon emitted from rice paddies , 1999 .

[42]  A. Page.  Methods of soil analysis. Part 2. Chemical and microbiological properties. , 1982 .

[43]  R. Conrad,et al.  Molecular analyses of methyl-coenzyme M reductase alpha-subunit (mcrA) genes in rice field soil and enrichment cultures reveal the methanogenic phenotype of a novel archaeal lineage. , 2001, Environmental microbiology.

[44]  J. Anderson,et al.  Plant litter quality and decomposition: an historical overview , 1997 .

[45]  A. Stams,et al.  Methanogenesis from acetate: a comparison of the acetate metabolism in Methanothrix soehngenii and Methanosarcina spp. , 1992 .

[46]  R. Conrad,et al.  In Situ Stable Isotope Probing of Methanogenic Archaea in the Rice Rhizosphere , 2005, Science.

[47]  T. Lueders,et al.  Archaeal Population Dynamics during Sequential Reduction Processes in Rice Field Soil , 2000, Applied and Environmental Microbiology.