Abstract
Numerous studies on marine prokaryotic communities have postulated that a process of anaerobic oxidation of methane (AOM) coupled with sulfate reduction (SR) is the main methane sink in the world's oceans. AOM has also been reported in the deep biosphere. But the responses of the primary microbial players in eliciting changes in geochemical environments, specifically in methane and sulfate supplies, have yet to be fully elucidated. Marine mud volcanoes (MVs) expel a complex fluid mixture of which methane is the primary component, forming an environment in which AOM is a common phenomenon. In this context, we attempted to identify how the prokaryotic community would respond to changes in methane and sulfate intensities, which often occur in MV environments in the form of eruptions, diffusions or seepage. We applied an integrated approach, including (i) biochemical surveys of pore water originated from MV, (ii) in vitro incubation of mud breccia, and (iii) prokaryotic community structure analysis. Two distinct AOM regions were clearly detected. One is related to the sulfate methane transition zone (SMTZ) at depth of 30–55 cm below the sea floor (bsf); the second is at 165–205 cm bsf with ten times higher rates of AOM and SR. This finding contrasts with the sulfide concentrations in pore waters and supports the suggestion that potential AOM activity below the SMTZ might be an important methane sink that is largely ignored or underestimated in oceanic methane budget calculations. Moreover, the incubation conditions below the SMTZ favor the growth of methanotrophic archaeal group ANME-2 compared to ANME-1, and promote the rapid growth and high diversity of bacterial communities. These incubation conditions also promote the increase of richness in bacterial communities. Our results provide direct evidence of the mechanisms by which deep AOM processes can affect carbon cycling in the deep biosphere and global methane biochemistry.
Highlights
The existence of microbial life in the deep subsurface has been known since ZoBell’s studies in the 1930s [1] and was first proven in sediment cores during drilling in the 1980s [2]
Available reports demonstrate that the highest quantities of active prokaryotes are associated with diverse biogeochemical interfaces, e.g., highly organic rich sediments such as the Mediterranean sapropels [7]; the sulfate methane transition zone (SMTZ), where anaerobic methanotrophy is the driving force behind local microbial activities [4]; the deep hypersaline anoxic lakes, where the ecosystems are largely driven by sulfur cycling and methanogenesis [8]; an increase in microbial biomass was observed in sediments with gas hydrates [9]
After a long-term in vitro incubation, a deeply buried anaerobic oxidation of methane (AOM) active zone was discovered besides the SMTZ, where the AOM activity was one order of magnitude higher than that of SMTZ
Summary
The existence of microbial life in the deep subsurface has been known since ZoBell’s studies in the 1930s [1] and was first proven in sediment cores during drilling in the 1980s [2]. Whether the deep biosphere is the largest prokaryotic habitat on Earth is an enigma because the estimations of cell numbers and biomass differ dramatically among sampling sites and counting techniques [3,4,5]. The importance of these deeply buried communities for driving carbon and nutrient cycling and for catalyzing a multitude of reactions among rocks, sediment and fluids is widely accepted [6]. Longterm incubation under simulated conditions has not been frequently reported and has only been performed at shallow sediment depths near the SMTZ [10]
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