Changes in microbial community structure by methane fluxes at arctic cold seeps

Cold seeps are areas of the seafloor where hydrocarbon-rich fluids, primarily composed of methane (CH₄), migrate from below reservoirs through the sediments to reach the seafloor surface. This CH₄ is an important energy source for biological communities at cold seeps and it is taken up by specialized archaeal and bacterial methane oxidizers in anaerobic and aerobic environments. Reaction products, such as sulphide, are thereafter cycled into the microbial food web, by other microbial functional groups, underlining the importance of microorganisms in supporting biological production at cold seeps. However, large gaps of knowledge on total microbial biodiversity at these methane seeps and their spatial distribution remain, especially at high latitudes. South of Svalbard, five geological mounds shaped by the formation of CH₄ gas hydrates (gas hydrate pingos GHPs), have been described recently. While one GHP was inactive, four of them showed CH₄ seeping activity with flares primarily concentrated at the summits. This suggest that the environmental conditions gradually change from the rim of the GHP toward the summit. We hypothesized that the microbial biodiversity varies along that gradient, where the summits would harbor the highest abundances of methane oxidizers. In order to test this hypothesis, we investigated the microbial community structure at two active GHPs, an inactive GHP and a reference site. Porewater chemistry and sequencing-based community analyses of Archaea, Bacteria and Eukaryotes were investigated at several depths of the sediment along a distance gradient from the summit to the rim of each GHP. We show that local environmental conditions, such as the presence of CH₄, do affect the microbial community structure and composition. The anaerobic methane oxidizing ANME-1 dominates the archaeal libraries and are detected various types of sulphate-reducing bacteria, although none demonstrated a clear co-occurrence with the predominance of ANME-1. Additional common taxa observed in these CH₄-rich sediments that likely benefited from the metabolites of CH₄ oxidation were sulphide oxidizing Epsilonproteobactaerota, as well as organic matter degraders, such as Bathyarchaeota, Woesearchaeota or thermoplasmatales MBG-D, and heterotrophic ciliates and Cercozoa. Beyond our expectations, the distribution of the different community types were not separated in concentric zones around the GHPs and similar methane oxidizing communities could be retrieved at different location over a GHP.