Response of Methanogenic Microbial Communities to Desiccation Stress in Flooded and Rain-Fed Paddy Soil from Thailand

Abstract

Rice paddies in central Thailand are flooded either by irrigation (irrigated rice) or by rain (rain-fed rice). The paddy soils and their microbial communities thus experience permanent or arbitrary submergence, respectively. Since methane production depends on anaerobic conditions, we hypothesized that structure and function of the methanogenic microbial communities are different in irrigated and rain-fed paddies and react differently upon desiccation stress. We determined rates and relative proportions of hydrogenotrophic and aceticlastic methanogenesis before and after short-term drying of soil samples from replicate fields. The methanogenic pathway was determined by analyzing concentrations and δ13C of organic carbon and of CH4 and CO2 produced in the presence and absence of methyl fluoride, an inhibitor of aceticlastic methanogenesis. We also determined the abundance (qPCR) of genes and transcripts of bacterial 16S rRNA, archaeal 16S rRNA and methanogenic mcrA (coding for a subunit of the methyl coenzyme M reductase) and the composition of these microbial communities by T-RFLP fingerprinting and/or Illumina deep sequencing. The abundances of genes and transcripts were similar in irrigated and rain-fed paddy soil. They also did not change much upon desiccation and rewetting, except the transcripts of mcrA, which increased by more than two orders of magnitude. In parallel, rates of CH4 production also increased, in rain-fed soil more than in irrigated soil. The contribution of hydrogenotrophic methanogenesis increased in rain-fed soil and became similar to that in irrigated soil. However, the relative microbial community composition on higher taxonomic levels was similar between irrigated and rain-fed soil. On the other hand, desiccation and subsequent anaerobic reincubation resulted in systematic changes in the composition of microbial communities for both Archaea and Bacteria. It is noteworthy that differences in the community composition were mostly detected on the level of operational taxonomic units (OTUs; 97% sequence similarity). The treatments resulted in change of the relative abundance of several archaeal OTUs. Some OTUs of Methanobacterium, Methanosaeta, Methanosarcina, Methanocella and Methanomassiliicoccus increased, while some of Methanolinea and Methanosaeta decreased. Bacterial OTUs within Firmicutes, Cyanobacteria, Planctomycetes and Deltaproteobacteria increased, while OTUs within other proteobacterial classes decreased.

Structure, function and resilience to desiccation of methanogenic microbial communities in temporarily inundated soils of the Amazon rainforest (Cunia Reserve, Rondonia)

“…Soils dominated by Firmicutes, Methanocellales and Methanosarcinaceae were apparently able to operate similarly (similar rate and pathway of methanogenesis) as when the soils contained a balanced mixture of various bacterial and archaeal taxa. Similar observations have been made before testing a variety of different soils and sediments (Angel et al, ; Conrad et al, ; Ji et al, ; Hernandez et al, ; Reim et al, ). It was expected that desiccation resulted in a loss of sensitive microbial species and thus in a decrease of diversity.…”

“…Rewetting and second incubation manifested this situation resulting in dominance of mainly Methanocellales and Methanosarcinaceae . Such dominance seems to be a general feature when flooded soils or sediments are artificially desiccated and rewetted (Conrad et al, ; Ji et al, ; Hernandez et al, ; Reim et al, ). It may be due to the antioxidant features of these methanogenic taxa (Erkel et al, ; Lyu and Lu, ).…”

“…Hence, CH 4 production in soils is probably the main driving force for CH 4 emission from tropical wetlands. It is well known that CH 4 production in flooded soils is achieved by methanogenic microbial communities, as shown by numerous studies in wetland soils, rice field soils in particular (Lueders and Friedrich, 2000;Conrad, 2007;Asakawa and Kimura, 2008;Rui et al, 2009;Kim and Liesack, 2015;Reim et al, 2017). In tropical wetlands, however, knowledge is comparatively poor.…”

“…Probably it is mainly this plasticity, which allows for the potential of methanogenic functioning in a large variety of different environments, including desert soils (Peters and Conrad, 1996;Angel et al, 2011). Nevertheless, the abundance and composition of the various methanogenic communities can be quite different, for example when comparing methanogenic communities in permanently flooded lake sediments (Ji et al, 2016), seasonally flooded rice field soils (Fernandez Scavino et al, 2013;Reim et al, 2017) or rarely flooded soils (Angel et al, 2012;Hernandez et al, 2017).…”

Rewetting of Three Drained Peatlands Drives Congruent Compositional Changes in Pro- and Eukaryotic Soil Microbiomes through Environmental Filtering

“…Wet peatlands are known to contribute a large share of the global CH4 emissions [1,52]. The higher mcrA abundance after rewetting ( Figure 5) could lead to increased CH4 emissions from peatlands, as is the case in rice paddy fields [16,53]. Interestingly, their abundance was high in the rewetted top soils, at least in Alderwet and Percowet, and not in the subsoils.…”