Novel microbial communities of the Haakon Mosby mud volcano and their role as a methane sink

Submarine mud volcanoes may be major players in the emission of the greenhouse gas methane. A select group of microorganisms, called methanotrophs, can consume this gas, but their impact on methane emission in this environment is not well understood. A study of the waters around a mud volcano in the Barents Sea has identified three key methanotrophic communities: aerobic bacteria, anaerobic archaea living beneath tubeworms, and previously undescribed archaea associated with bacterial mats. A natural cap on the capacity of the microbial methane filter was also discovered: the upward flow of sulphate- and oxygen-free volcanic fluids restricts the efficiency of methane oxidation, allowing much of the methane to escape to the hydrosphere and potentially the atmosphere. Mud volcanism is an important natural source of the greenhouse gas methane to the hydrosphere and atmosphere1,2. Recent investigations show that the number of active submarine mud volcanoes might be much higher than anticipated (for example, see refs 3–5), and that gas emitted from deep-sea seeps might reach the upper mixed ocean6,7,8. Unfortunately, global methane emission from active submarine mud volcanoes cannot be quantified because their number and gas release are unknown9. It is also unclear how efficiently methane-oxidizing microorganisms remove methane. Here we investigate the methane-emitting Haakon Mosby Mud Volcano (HMMV, Barents Sea, 72° N, 14° 44′ E; 1,250 m water depth) to provide quantitative estimates of the in situ composition, distribution and activity of methanotrophs in relation to gas emission. The HMMV hosts three key communities: aerobic methanotrophic bacteria (Methylococcales), anaerobic methanotrophic archaea (ANME-2) thriving below siboglinid tubeworms, and a previously undescribed clade of archaea (ANME-3) associated with bacterial mats. We found that the upward flow of sulphate- and oxygen-free mud volcano fluids restricts the availability of these electron acceptors for methane oxidation, and hence the habitat range of methanotrophs. This mechanism limits the capacity of the microbial methane filter at active marine mud volcanoes to <40% of the total flux.