Active methane processing microbes and the disproportionate role of NC10 phylum in methane mitigation in Amazonian floodplains

Abstract

Here we use a top-down and bottom-up approach in landscape ecology to analyze the active microbes processing methane fluxes (FCH4) in seasonally flooded-forest (FOR) andtraditional farming systems (TFS) in Amazonian floodplains flooded with black, white, and clear water. Our results revealed higher CH4 emissions from water-atmosphere interface in clear water floodplain, followed by black and white water floodplain, respectively. Active methanogenic and methanotrophic taxa were ubiquitous at 0-15 and 15-30 cm soil layer in FOR and TFS, with differences among the water types with respect to the richness, evenness and diversity of the methanogenic communities. These ecological results were not generalizable regarding to FOR and TFS sites, soil layers, and non-flooded and flooded periods. Despite the predominant oxidation of CH4 in the non-flooded period, higher richness and diversity of methanotrophs were revealed for FOR and TFS in the flooded period. In turn, the structure of the methanogenic and methanotrophic communities and their variation were influenced mainly by soil physicochemical factors, water type, soil depth and the presence of nitrifiers, as Nitrososphaera and Nitrospira. Our study reveals a signature across methanotrophic communities in soils from Amazon floodplain with different water types, with a putative disproportionate role of NC10 phylum in CH4 mitigation in natural and agricultural Amazonian floodplains. These findings open the possibilities to explore the role of NC10 phylum in the carbon cycling in Amazon.

Molecular evidence for stimulation of methane oxidation in Amazonian floodplains by ammonia-oxidizing communities

“…Both nitrate and sulfate reduction use H + ions, which can be related to the increase in pH that occurs during the flood season, indicating the use of both ions as electron acceptors. Bento et al (2021) also detected the presence of common nitrifiers, such as Nitrososphaera and Nitrospira , through amplicon sequencing analysis of the 16S rRNA gene, highlighting the importance of alternative electron acceptors for biogeochemical cycles during the flood season in the Amazonian floodplains. This chemical transformation can only occur in the absence of oxygen (O 2 ), which can be achieved by an increase in depth and by flooding, which explains the high proportion of the variability explained by the changes in season and depth ( Table 2 ).…”

“…Members of both the Methanoperedenaceae and Methylomirabilaceae families have been previously co-enriched ( Raghoebarsing et al, 2006 ), and in the absence of ammonia, which would inhibit anaerobic ammonia oxidation (anammox) activity and NO 2 – consumption, the dominant microbial consortium in an anaerobic bioreactor fed with CH 4 and NO 3 – was that of the archaeon Candidatus Methanoperdens nitroreducens and the bacterium Candidatus Methylomirabilis oxyfera ( Haroon et al, 2013 ), which were also detected in this floodplain ( Gabriel et al, 2020 ; Bento et al, 2021 ; Gontijo et al, 2021 ).…”

“…The model of interaction between Methanoperdens nitroreducens and Methylomirabilis oxyfera , described by Haroon et al (2013) , may also be applied to the Tocantins River floodplain soils where high CH 4 availability ( Bento et al, 2021 ) and highly acidic (pH < 4) soils with low ammonia availability could inhibit anammox activity ( Bai et al, 2015 ; Daverey et al, 2015 ) and allow for the cooperation between both methanotrophs. Methanoperdens nitroreducens can couple methane oxidation to reduce NO 3 – to NO 2 – ( Raghoebarsing et al, 2006 ), which would fuel Methylomirabilis oxyfera as it couples methane oxidation to NO 2 – reduction ( Ettwig et al, 2009 ).…”

“…A study in the Amazonian floodplains revealed a disproportionate role of the NC10 phylum in CH 4 mitigation across soil layers, forest, and agricultural sites, with seasonal flooding in the different water types of the floodplains and the presence of Candidatus M. nitroreducens in the clear water floodplain of the Tocantins River ( Bento et al, 2021 ). The nitrate-reducing archaeon Candidatus M. nitroreducens can not only reduce NO 3 – to NO 2 – but can also perform dissimilatory nitrate reduction to ammonium (DNRA) ( Ettwig et al, 2016 ).…”

Metagenomes from Eastern Brazilian Amazonian Floodplains in the Wet and Dry Seasons

“…Floodplains and wetlands constitute 14% of the total area of the Amazon basin ( 1 ) and are considered the largest natural geographic source of methane (CH 4 ) in the tropics ( 2 ). Therefore, several studies have investigated the CH 4 -producing and -consuming microbial communities in these sediments and their responses to a range of environmental factors using 16S rRNA amplicon sequencing ( 3 – 5 ). However, their overall microbial taxonomic and functional diversity remains little explored.…”