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Anaerobic oxidation of methane (AOM) is hypothesized to occur through reverse hydrogenotrophic methanogenesis in marine sediments because sulfate reducers pull hydrogen concentrations so low that reverse hydrogenotrophic methanogenesis is exergonic. If true, hydrogenotrophic methanogenesis can theoretically co-occur with sulfate reduction if the organic matter is so labile that fermenters produce more hydrogen than sulfate reducers can consume, causing hydrogen concentrations to rise. Finding accumulation of biologically-produced methane in sulfate-containing organic-rich sediments would therefore support the theory that AOM occurs through reverse hydrogenotrophic methanogenesis since it would signal the absence of net AOM in the presence of sulfate. Methods16S rRNA gene libraries were compared to geochemistry and incubations in high depth-resolution sediment cores collected from organic-rich Cape Lookout Bight, North Carolina. ResultsWe found that methane began to accumulate while sulfate is still abundant (6–8 mM). Methane-cycling archaeaANME-1,Methanosarciniales, andMethanomicrobialesalso increased at these depths. Incubations showed that methane production in the upper 16 cm in sulfate-rich sediments was biotic since it could be inhibited by 2-bromoethanosulfonoic acid (BES). DiscussionWe conclude that methanogens mediate biological methane production in these organic-rich sediments at sulfate concentrations that inhibit methanogenesis in sediments with less labile organic matter, and that methane accumulation and growth of methanogens can occur under these conditions as well. Our data supports the theory that H2concentrations, rather than the co-occurrence of sulfate and methane, control whether methanogenesis or AOM via reverse hydrogenotrophic methanogenesis occurs. We hypothesize that the high amount of labile organic matter at this site prevents AOM, allowing methane accumulation when sulfate is low but still present in mM concentrations.
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Organohalide-Respiring Bacteria at the Heart of Anaerobic Metabolism in Arctic Wet Tundra Soils
ABSTRACT Recent work revealed an active biological chlorine cycle in coastal Arctic tundra of northern Alaska. This raised the question of whether chlorine cycling was restricted to coastal areas or if these processes extended to inland tundra. The anaerobic process of organohalide respiration, carried out by specialized bacteria like Dehalococcoides , consumes hydrogen gas and acetate using halogenated organic compounds as terminal electron acceptors, potentially competing with methanogens that produce the greenhouse gas methane. We measured microbial community composition and soil chemistry along an ∼262-km coastal-inland transect to test for the potential of organohalide respiration across the Arctic Coastal Plain and studied the microbial community associated with Dehalococcoides to explore the ecology of this group and its potential to impact C cycling in the Arctic. Concentrations of brominated organic compounds declined sharply with distance from the coast, but the decrease in organic chlorine pools was more subtle. The relative abundances of Dehalococcoides were similar across the transect, except for being lower at the most inland site. Dehalococcoides correlated with other strictly anaerobic genera, plus some facultative ones, that had the genetic potential to provide essential resources (hydrogen, acetate, corrinoids, or organic chlorine). This community included iron reducers, sulfate reducers, syntrophic bacteria, acetogens, and methanogens, some of which might also compete with Dehalococcoides for hydrogen and acetate. Throughout the Arctic Coastal Plain, Dehalococcoides is associated with the dominant anaerobes that control fluxes of hydrogen, acetate, methane, and carbon dioxide. Depending on seasonal electron acceptor availability, organohalide-respiring bacteria could impact carbon cycling in Arctic wet tundra soils. IMPORTANCE Once considered relevant only in contaminated sites, it is now recognized that biological chlorine cycling is widespread in natural environments. However, linkages between chlorine cycling and other ecosystem processes are not well established. Species in the genus Dehalococcoides are highly specialized, using hydrogen, acetate, vitamin B 12 -like compounds, and organic chlorine produced by the surrounding community. We studied which neighbors might produce these essential resources for Dehalococcoides species. We found that Dehalococcoides species are ubiquitous across the Arctic Coastal Plain and are closely associated with a network of microbes that produce or consume hydrogen or acetate, including the most abundant anaerobic bacteria and methanogenic archaea. We also found organic chlorine and microbes that can produce these compounds throughout the study area. Therefore, Dehalococcoides could control the balance between carbon dioxide and methane (a more potent greenhouse gas) when suitable organic chlorine compounds are available to drive hydrogen and acetate uptake.
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- Award ID(s):
- 1712774
- PAR ID:
- 10281613
- Editor(s):
- Rudi, Knut
- Date Published:
- Journal Name:
- Applied and Environmental Microbiology
- Volume:
- 87
- Issue:
- 3
- ISSN:
- 0099-2240
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/AEM.01643-20
