Versatile methanotrophs form an active methane biofilter in the oxycline of a seasonally stratified coastal basin

Abstract

The potential and drivers of microbial methane removal in the water column of seasonally stratified coastal ecosystems and the importance of the methanotrophic community composition for ecosystem functioning are not well explored. Here, we combined depth profiles of oxygen and methane with 16S rRNA gene amplicon sequencing, metagenomics, and methane oxidation rates at discrete depths in a stratified coastal marine system (Lake Grevelingen, The Netherlands). Three amplicon sequence variants (ASVs) belonging to different genera of aerobic Methylomonadaceae and the corresponding three methanotrophic metagenome-assembled genomes (MOB-MAGs) were retrieved by 16S rRNA sequencing and metagenomic analysis respectively. The abundances of the different methanotrophic ASVs and MOB-MAGs peaked at different depths along the methane oxygen counter-gradient and the MOB-MAGs show a quite diverse genomic potential regarding oxygen metabolism, partial denitrification, and sulfur metabolism. Moreover, potential aerobic methane oxidation rates indicated high methanotrophic activity throughout the methane oxygen counter-gradient, even at depths with low in situ methane or oxygen concentration. This suggests that niche-partitioning with high genomic versatility of the present Methylomonadaceae might contribute to the functional resilience of the methanotrophic community and ultimately the efficiency of methane removal in the stratified water column of marine Lake Grevelingen.

Pathways of methane removal in the sediment and water column of a seasonally anoxic eutrophic marine basin

“…At and below the oxycline, however, 16S rRNA gene sequences of archaeal methanotrophs (Methanoperedenaceae) were identified (Figure 5B), indicating that in the anoxic waters, CH 4 removal might be coupled to reduction of NO À 3 or Fe and/or Mn oxides, although the contribution to total CH 4 removal is likely small. Some of the produced NO À 2 and/or NH + 4 might be used by anammox bacteria, although only a few 16S rRNA sequences of anammox were recovered in the amplicon set (Venetz et al, 2022). To our knowledge this is the first report of Methanoperedenaceae in marine waters in a zone of CH 4 oxidation.…”

“…Importantly, NH + 4 removal also occurred near the oxycline, presumably through nitrification. However, no accumulation of NO À 3 was observed near the oxycline, which is likely due to its immediate reduction via denitrification (Venetz et al, 2022). Nitrate removal could also potentially be linked to anaerobic CH 4 oxidation as the zone of decreasing CH 4 concentrations overlaps with the zone where NH + 4 is removed and, hence, where NO À 3 is produced and reduced.…”

“…DNA was extracted from the filters following the protocol of the DNeasy Power water DNA Isolation kit (Qiagen, Venlo, the Netherlands). For a further description of the data acquisition and analysis we refer to Venetz et al (2022).…”

Seasonal dynamics of the microbial methane filter in the water column of a eutrophic coastal basin

“…The efficiency of this so-called methane biofilter is one of the greatest uncertainties in methane-emission predictions (Dean et al ., 2018). In coastal basins, a consortium of anaerobic methane-oxidizing archaea with sulfate-reducing bacteria build the methane biofilter in the sediment (Wallenius et al ., 2021), and aerobic methane-oxidizing bacteria dominate the methane biofilter in the water column (Reeburgh, 2007; Steinle et al ., 2017; Steinsdóttir, et al ., 2022a; Venetz et al ., 2023). Deoxygenation and eutrophication can lead to increased methane production in the sediment, that can exceed the methane oxidation capacity, which can result in high benthic methane fluxes into the water column (Egger et al ., 2016; Zhang et al ., 2020; Lenstra et al ., 2023; Żygadłowska, et al ., 2023a).…”

“…During summer stratification, such a methane biofilter can counteract the high benthic methane fluxes (Mao et al ., 2022; Steinsdóttir, et al ., 2022b). Multiple potential metabolic pathways within the ambient methanotrophic community ensure the functionality of the methane biofilter along the vertical range of oxygen and methane concentrations (Hernandez et al ., 2015; Venetz et al ., 2023). Such niche partitioning over a range of oxygen concentrations likely aids the overall resilience of the methane biofilter towards regular changes in oxygen availability in the water column(Venetz et al ., 2023).…”