Dataset Information

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 CH(4) 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 degrees C, 30 degrees C, and 45 degrees C). More CH(4) was produced in the straw treatment than root treatment. Increasing the temperature from 15 degrees C to 45 degrees C enhanced CH(4) 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 degrees C and 30 degrees C, respectively, while the thermophilic Methanobacteriales and rice cluster I methanogens were significantly enhanced at 45 degrees 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 H(2)) seems to be the key factor that regulates the shift of methanogenic community.

SUBMITTER: Peng J

PROVIDER: S-EPMC2394899 | biostudies-literature | 2008 May

REPOSITORIES: biostudies-literature

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Dynamics of the methanogenic archaeal community during plant residue decomposition in an anoxic rice field soil.

Peng Jingjing J Lü Zhe Z Rui Junpeng J Lu Yahai Y

Applied and environmental microbiology 20080314 9

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 CH(4) 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 fiel ...[more]

PMID: 18344350

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Project description:Soil temperatures in Italian rice fields typically range between about 15 and 30 degrees C. A change in the incubation temperature of anoxic methanogenic soil slurry from 30 degrees C to 15 degrees C typically resulted in a decrease in the CH4 production rate, a decrease in the steady-state H2 partial pressure, and a transient accumulation of acetate. Previous experiments have shown that these changes were due to an alteration of the carbon and electron flow in the methanogenic degradation pathway of organic matter caused by the temperature shift (K. J. Chin and R. Conrad, FEMS Microbiol. Ecol. 18:85-102, 1995). To investigate how temperature affects the structure of the methanogenic archaeal community, total DNA was extracted from soil slurries incubated at 30 and 15 degrees C. The archaeal small-subunit (SSU) rRNA-encoding genes (rDNA) of these environmental DNA samples were amplified by PCR with an archaeal-specific primer system and used for the generation of clone libraries. Representative rDNA clones (n = 90) were characterized by terminal restriction fragment length polymorphism (T-RFLP) and sequence analysis. T-RFLP analysis produced for the clones terminally labeled fragments with a characteristic length of mostly 185, 284, or 392 bp. Sequence analysis allowed determination of the phylogenetic affiliation of the individual clones with their characteristic T-RFLP fragment lengths and showed that the archaeal community of the anoxic rice soil slurry was dominated by members of the families Methanosarcinaceae (185 bp) and Methanosaetaceae (284 bp), the kingdom Crenarchaeota (185 or 284 bp), and a novel, deeply branching lineage of the (probably methanogenic) kingdom Euryarchaeota (392 bp) that has recently been detected on rice roots (R. Grosskopf, S. Stubner, and W. Liesack, Appl. Environ. Microbiol. 64:4983-4989, 1998). The structure of the archaeal community changed when the temperature was shifted from 30 degrees C to 15 degrees C. Before the temperature shift, the clones (n = 30) retrieved from the community were dominated by Crenarchaeota (70%), "novel Euryarchaeota" (23%), and Methanosarcinacaeae (7%). Further incubation at 30 degrees C (n = 30 clones) resulted in a relative increase in members of the Methanosarcinaceae (77%), whereas further incubation at 15 degrees C (n = 30 clones) resulted in a much more diverse community consisting of 33% Methanosarcinaceae, 23% Crenarchaeota, 20% Methanosaetaceae, and 17% novel Euryarchaeota. The appearance of Methanosaetaceae at 15 degrees C was conspicuous. These results demonstrate that the structure of the archaeal community in anoxic rice field soil changed with time and incubation temperature.

Project description:Addition of straw is common practice in rice agriculture, but its effect on the path of microbial CH(4) production and the microbial community involved is not well known. Since straw from rice (C3 plant) and maize plants (C4 plant) exhibit different ?(13)C values, we compared the effect of these straw types using anoxic rice field soils from Italy and China, and also a soil from Thailand that had previously not been flooded. The temporal patterns of production of CH(4) and its major substrates H(2) and acetate, were slightly different between rice straw and maize straw. Addition of methyl fluoride, an inhibitor of acetoclastic methanogenesis, resulted in partial inhibition of acetate consumption and CH(4) production. The ?(13)C of the accumulated CH(4) and acetate reflected the different ?(13)C values of rice straw versus maize straw. However, the relative contribution of hydrogenotrophic methanogenesis to total CH(4) production exhibited a similar temporal change when scaled to CH(4) production irrespectively of whether rice straw or maize straw was applied. The composition of the methanogenic archaeal communities was characterized by terminal restriction fragment length polymorphism (T-RFLP) analysis and was quantified by quantitative PCR targeting archaeal 16S rRNA genes or methanogenic mcrA genes. The size of the methanogenic communities generally increased during incubation with straw, but the straw type had little effect. Instead, differences were found between the soils, with Methanosarcinaceae and Methanobacteriales dominating straw decomposition in Italian soil, Methanosarcinaceae, Methanocellales, and Methanobacteriale in China soil, and Methanosarcinaceae and Methanocellales in Thailand soil. The experiments showed that methanogenic degradation in different soils involved different methanogenic population dynamics. However, the path of CH(4) production was hardly different between degradation of rice straw versus maize straw and was also similar for the different soil types.

Project description:Physical protection of soil carbon (C) is one of the important components of C storage. However, its exact mechanisms are still not sufficiently lucid. The goal of this study was to explore the influence of soil structure, that is, soil pore spatial arrangements, with and without presence of plant residue on (i) decomposition of added plant residue, (ii) CO2 emission from soil, and (iii) structure of soil bacterial communities. The study consisted of several soil incubation experiments with samples of contrasting pore characteristics with/without plant residue, accompanied by X-ray micro-tomographic analyses of soil pores and by microbial community analysis of amplified 16S-18S rRNA genes via pyrosequencing. We observed that in the samples with substantial presence of air-filled well-connected large (>30 µm) pores, 75-80% of the added plant residue was decomposed, cumulative CO2 emission constituted 1,200 µm C g(-1) soil, and movement of C from decomposing plant residue into adjacent soil was insignificant. In the samples with greater abundance of water-filled small pores, 60% of the added plant residue was decomposed, cumulative CO2 emission constituted 2,000 µm C g(-1) soil, and the movement of residue C into adjacent soil was substantial. In the absence of plant residue the influence of pore characteristics on CO2 emission, that is on decomposition of the native soil organic C, was negligible. The microbial communities on the plant residue in the samples with large pores had more microbial groups known to be cellulose decomposers, that is, Bacteroidetes, Proteobacteria, Actinobacteria, and Firmicutes, while a number of oligotrophic Acidobacteria groups were more abundant on the plant residue from the samples with small pores. This study provides the first experimental evidence that characteristics of soil pores and their air/water flow status determine the phylogenetic composition of the local microbial community and directions and magnitudes of soil C decomposition processes.

Project description:The population dynamics of Archaea after flooding of an Italian rice field soil were studied over 17 days. Anoxically incubated rice field soil slurries exhibited a typical sequence of reduction processes characterized by reduction of nitrate, Fe(3+), and sulfate prior to the initiation of methane production. Archaeal population dynamics were followed using a dual approach involving molecular sequence retrieval and fingerprinting of small-subunit (SSU) rRNA genes. We retrieved archaeal sequences from four clone libraries (30 each) constructed for different time points (days 0, 1, 8, and 17) after flooding of the soil. The clones could be assigned to known methanogens (i.e., Methanosarcinaceae, Methanosaetaceae, Methanomicrobiaceae, and Methanobacteriaceae) and to novel euryarchaeotal (rice clusters I, II, and III) and crenarchaeotal (rice clusters IV and VI) lineages previously detected in anoxic rice field soil and on rice roots (R. Grosskopf, S. Stubner, and W. Liesack, Appl. Environ. Microbiol. 64:4983-4989, 1998). During the initiation of methanogenesis (days 0 to 17), we detected significant changes in the frequency of individual clones, especially of those affiliated with the Methanosaetaceae and Methanobacteriaceae. However, these findings could not be confirmed by terminal restriction fragment length polymorphism (T-RFLP) analysis of SSU rDNA amplicons. Most likely, the fluctuations in sequence composition of clone libraries resulted from cloning bias. Clonal SSU rRNA gene sequences were used to define operational taxonomic units (OTUs) for T-RFLP analysis, which were distinguished by group-specific TaqI restriction sites. Sequence analysis showed a high degree of conservation of TaqI restriction sites within the different archaeal lineages present in Italian rice field soil. Direct T-RFLP analysis of archaeal populations in rice field soil slurries revealed the presence of all archaeal lineages detected by cloning with a predominance of terminal restriction fragments characteristic of rice cluster I (389 bp), Methanosaetaceae (280 bp), and Methanosarcinaceae/rice cluster VI (182 bp). In general, the relative gene frequency of most detected OTUs remained rather constant over time during the first 17 days after flooding of the soil. Most minor OTUs (e.g., Methanomicrobiaceae and rice cluster III) and Methanosaetaceae did not change in relative frequency. Rice cluster I (37 to 30%) and to a lesser extent rice cluster IV as well as Methanobacteriaceae decreased over time. Only the relative abundance of Methanosarcinaceae (182 bp) increased, roughly doubling from 15 to 29% of total archaeal gene frequency within the first 11 days, which was positively correlated to the dynamics of acetate and formate concentrations. Our results indicate that a functionally dynamic ecosystem, a rice field soil after flooding, was linked to a relatively stable archaeal community structure.

Dataset Information

Dynamics of the methanogenic archaeal community during plant residue decomposition in an anoxic rice field soil.

Publications

Dynamics of the methanogenic archaeal community during plant residue decomposition in an anoxic rice field soil.

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