Abstract
Emission of the greenhouse gas methane from the seabed is globally controlled by marine aerobic and anaerobic methanotrophs gaining energy via methane oxidation. However, the processes involved in the assembly and dynamics of methanotrophic populations in complex natural microbial communities remain unclear. Here we investigated the development of a methanotrophic microbiome following subsurface mud eruptions at Håkon Mosby mud volcano (1250 m water depth). Freshly erupted muds hosted deep-subsurface communities that were dominated by Bathyarchaeota, Atribacteria and Chloroflexi. Methanotrophy was initially limited to a thin surface layer of Methylococcales populations consuming methane aerobically. With increasing distance to the eruptive center, anaerobic methanotrophic archaea, sulfate-reducing Desulfobacterales and thiotrophic Beggiatoaceae developed, and their respective metabolic capabilities dominated the biogeochemical functions of the community. Microbial richness, evenness, and cell numbers of the entire microbial community increased up to tenfold within a few years downstream of the mud flow from the eruptive center. The increasing diversity was accompanied by an up to fourfold increase in sequence abundance of relevant metabolic genes of the anaerobic methanotrophic and thiotrophic guilds. The communities fundamentally changed in their structure and functions as reflected in the metagenome turnover with distance from the eruptive center, and this was reflected in the biogeochemical zonation across the mud volcano caldera. The observed functional succession provides a framework for the response time and recovery of complex methanotrophic communities after disturbances of the deep-sea bed.
Highlights
Electronic supplementary material The online version of this article contains supplementary material, which is available to authorized users.Research, Bremerhaven, Germany 4 Present address: Department of Geoscience, University of Calgary, Calgary, AB, Canada 5 Present address: Institute for Infectious Diseases, University ofBern, Bern, SwitzerlandThe ocean seabed is the largest methane reservoir on Earth, comprising this climate-relevant gas in the form of semistable methane hydrates, as gas bubbles or dissolved in porewater
We studied the development of a deep-sea methanotrophic microbiome on mud flows of a methane-emitting mud volcano in situ
Changes in biogeochemical rates with increasing distance to the eruptive center of the mud volcano were mirrored by changes in the corresponding metabolic genes and cell counts of the respective clades
Summary
Most of the methane rising from deeper subsurface layers is oxidized by methanotrophic microbial communities before it can reach the hydrosphere [1]. Anoxic subsurface layers, where methane and sulfate overlap, are inhabited by consortia of anaerobic methanotrophic archaea (ANME) and their partner bacteria of the sulfate-reducing Desulfobacterales [6,7,8,9]. These methanotrophic communities, referred to as the microbial methane filter, remove >90% of the methane in undisturbed continental margin sediments [1]. Understanding the causes for these different efficiencies, as well as the time scales needed for the establishment of an efficient methane filter, is crucial in order to assess the consequences of natural and man-made seafloor disturbances, such as rapidly dissociating hydrates [16, 17], mud slides, eruptive mud volcanoes [14] or large oil spills [18,19,20]
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