Communal metabolism by Methylococcaceae and Methylophilaceae is driving rapid aerobic methane oxidation in sediments of a shallow seep near Elba, Italy

Abstract

Summary The release of abiotic methane from marine seeps into the atmosphere is a major source of this potent greenhouse gas. Methanotrophic microorganisms in methane seeps use methane as carbon and energy source, thus significantly mitigating global methane emissions. Here, we investigated microbial methane oxidation at the sediment–water interface of a shallow marine methane seep. Metagenomics and metaproteomics, combined with 13C‐methane stable isotope probing, demonstrated that various members of the gammaproteobacterial family Methylococcaceae were the key players for methane oxidation, catalysing the first reaction step to methanol. We observed a transfer of carbon to methanol‐oxidizing methylotrophs of the betaproteobacterial family Methylophilaceae, suggesting an interaction between methanotrophic and methylotrophic microorganisms that allowed for rapid methane oxidation. From our microcosms, we estimated methane oxidation rates of up to 871 nmol of methane per gram sediment per day. This implies that more than 50% of methane at the seep is removed by microbial oxidation at the sediment–water interface, based on previously reported in situ methane fluxes. The organic carbon produced was further assimilated by different heterotrophic microbes, demonstrating that the methane‐oxidizing community supported a complex trophic network. Our results provide valuable eco‐physiological insights into this specialized microbial community performing an ecosystem function of global relevance.

Lake mixing regime selects apparent methane oxidation kinetics of the methanotroph assemblage

“…3a, b). The shift of the MOB assemblage was accompanied by a drop in temperature and rise in oxygen, which are probable drivers of MOB succession in addition to methane availability (Hernandez et al, 2015;Oshkin et al, 2015;Trotsenko and Khmelenina, 2005). This did, however, not lead to much change in the methane affinity ( Fig.…”

“…The fact that both the affinity and maximum rate are higher would intrinsically suggests that the assemblage in the epilimnion has a competitive advantage over the assemblage in the hypolimnion. This implies that there were likely additional mechanisms or traits, like adaptation to oxygen concentration or temperature (Hernandez et al, 2015;Trotsenko and Khmelenina, 2005), that prevented the epilimnetic MOB assemblage from invading the assemblage in the hypolimnion. We already have strong indications from our previous work that these factors are indeed important (Mayr et al, 2020a, b).…”

Interpretations of Environmental Microbial Community Studies Are Biased by the Selected 16S rRNA (Gene) Amplicon Sequencing Pipeline

“…Recovering representative sequences such as OTUs or ASVs allows for further analysis like constructing phylogenetic trees or performing targeted analyses, such as searching for the same sequence or related sequences in other data sets, that is not possible when using direct read classification. However, direct taxonomic classification can be straight forward with functional gene sequences that do not have elaborate reference databases like the 16S rRNA gene (DeSantis et al, 2006;Quast et al, 2013), e.g., for methane monooxygenase genes (pmoA, mmoX) or methanol dehydrogenase genes (xoxF4, xoxF5, mxaF) (Taubert et al, 2019).…”

Low Abundance of Methanotrophs in Sediments of Shallow Boreal Coastal Zones With High Water Methane Concentrations

“…The importance of methanotrophs to limit CH 4 emission has previously been shown, e.g., Bornemann et al (2016) used pMMO primers (subunit A, pmoA) and clone-libraries to identify methanotrophs (taxonomic order Methylococcales) in the pelagic area of Lake Constance, and found that these bacteria contributed substantially to CH 4 removal in the bottom water directly above the sediment surface. Bacterial members belonging to the order Methylococcales are ubiquitous (Smith et al, 2018), and metagenome plus metatranscriptome analysis have shown that they dominate aerobic CH 4 oxidation in wetland soil (Smith et al, 2018), and are important in removing CH 4 escaping from benthic CH 4 seeps (Taubert et al, 2019). Methanotrophs are therefore essential key players in regulating CH 4 emission to the atmosphere from aquatic environments.…”