Dry/Wet Cycles Change the Activity and Population Dynamics of Methanotrophs in Rice Field Soil

Abstract

bThe methanotrophs in rice field soil are crucial in regulating the emission of methane. Drainage substantially reduces methane emission from rice fields. However, it is poorly understood how drainage affects microbial methane oxidation. Therefore, we analyzed the dynamics of methane oxidation rates, composition (using terminal restriction fragment length polymorphism [T-RFLP]), and abundance (using quantitative PCR [qPCR]) of methanotroph pmoA genes (encoding a subunit of particulate methane monooxygenase) and their transcripts over the season and in response to alternate dry/wet cycles in planted paddy field microcosms. In situ methane oxidation accounted for less than 15% of total methane production but was enhanced by intermittent drainage. The dry/wet alternations resulted in distinct effects on the methanotrophic communities in different soil compartments (bulk soil, rhizosphere soil, surface soil). The methanotrophic communities of the different soil compartments also showed distinct seasonal dynamics. In bulk soil, potential methanotrophic activity and transcription of pmoA were relatively low but were significantly stimulated by drainage. In contrast, however, in the rhizosphere and surface soils, potential methanotrophic activity and pmoA transcription were relatively high but decreased after drainage events and resumed after reflooding. While type II methanotrophs dominated the communities in the bulk soil and rhizosphere soil compartments (and to a lesser extent also in the surface soil), it was the pmoA of type I methanotrophs that was mainly transcribed under flooded conditions. Drainage affected the composition of the methanotrophic community only minimally but strongly affected metabolically active methanotrophs. Our study revealed dramatic dynamics in the abundance, composition, and activity of the various type I and type II methanotrophs on both a seasonal and a spatial scale and showed strong effects of dry/wet alternation cycles, which enhanced the attenuation of methane flux into the atmosphere. Methanotrophs utilize methane as the sole carbon and energy source. Methane is a potent greenhouse gas in the atmosphere. The activity of methanotrophs is crucial for attenuation of methane emission from the biosphere into the atmosphere. They consume about 0.6 Gt methane annually, roughly equivalent to the total amount of methane emitted into the atmosphere (1). Although anaerobic oxidation of methane has been discovered in many anoxic sediments, it is the aerobic oxidation that is important for methane emission from rice field soil, oxidizing up to 90% of methane produced (2-5). Among the aerobic methanotrophs, proteobacterial methanotrophs play the dominant role, while verrucomicrobial methanotrophs are restricted to extreme environments (6). The aerobic oxidation of methane depends on methane monooxygenase (MMO) in the initial enzymatic reaction. This enzyme has two forms, a soluble type (sMMO) and a membraneassociated type (pMMO). All known bacterial methanotrophs except Methylocella and Methylo...

Effects of copper on methane emission, methanogens and methanotrophs in the rhizosphere and bulk soil of rice paddy

“…The oxygen would lead to significantly higher diversity and abundance of methanotrophs in the rhizosphere than bulk soil (Wu et al, 2009). A previous study also showed that the copy number of pmoA gene was approximately one order of magnitude higher, while the transcript number was more than two orders of magnitude higher in rhizosphere than in bulk soil (Ma et al, 2013).…”

Methylotrophs in natural habitats: current insights through metagenomics

“…Typically, both type I and type II methanotrophs are detected via PCR. However, transcript analysis, along with methane-oxidizing potential measurements, indicated that type I methanotrophs are likely responsible for much of the activity, at least in some of the sampled sites (Reim et al 2012;Ma et al 2013). A metaproteogenomic approach has also been applied to rice rhizosphere environments .…”

The differential effects of ammonium and nitrate on methanotrophs in rice field soil

“…The proteobacterial methanotrophs are conventionally classified into type I (Gammaproteobacteria) and type II (Alphaproteobacteria) groups based on their cellular morphology, chemistry and physiology (Hanson and Hanson, 1996;Luke and Frenzel, 2011). The pmoA gene that encodes the subunit of membrane-bound methane monooxygenase (MMO) is present in all known bacterial methanotrophs except Methylocella and Methyloferula (Dedysh et al, 2000;Vorobev et al, 2011) and can be used as a phylogenetic marker for the ecological studies of methanotrophs (McDonald et al, 2008;Ma et al, 2013).…”

“…The activity and growth of methanotrophs in soils are crucial in balancing the atmospheric CH 4 concentration. Various environmental and agricultural factors like soil type, water management, and fertilization can affect CH 4 oxidation (Bodelier et al, 2000;Ma et al, 2010Ma et al, , 2013Ma and Lu, 2011). In Asian rice field soils, nitrogen is a yield-limiting factor of rice production (Cassman et al, 1998) and the application of nitrogenous fertilizers is expected to increase in the next decades due to the food demand of the increasing population (Glibert et al, 2006).…”