Abstract
Subsurface microbial communities undertake many terminal electron-accepting processes, often simultaneously. Using a tritium-based assay, we measured the potential hydrogen oxidation catalyzed by hydrogenase enzymes in several subsurface sedimentary environments (Lake Van, Barents Sea, Equatorial Pacific, and Gulf of Mexico) with different predominant electron-acceptors. Hydrogenases constitute a diverse family of enzymes expressed by microorganisms that utilize molecular hydrogen as a metabolic substrate, product, or intermediate. The assay reveals the potential for utilizing molecular hydrogen and allows qualitative detection of microbial activity irrespective of the predominant electron-accepting process. Because the method only requires samples frozen immediately after recovery, the assay can be used for identifying microbial activity in subsurface ecosystems without the need to preserve live material. We measured potential hydrogen oxidation rates in all samples from multiple depths at several sites that collectively span a wide range of environmental conditions and biogeochemical zones. Potential activity normalized to total cell abundance ranges over five orders of magnitude and varies, dependent upon the predominant terminal electron acceptor. Lowest per-cell potential rates characterize the zone of nitrate reduction and highest per-cell potential rates occur in the methanogenic zone. Possible reasons for this relationship to predominant electron acceptor include (i) increasing importance of fermentation in successively deeper biogeochemical zones and (ii) adaptation of H2ases to successively higher concentrations of H2 in successively deeper zones.
Highlights
Microorganisms in subsurface environments compete for electron donors and acceptors as they do in most surface environments (D’Hondt et al, 2002)
The predominant terminal electron acceptor is typically inferred to change with sediment depth (e.g., Froelich et al, 1979), with reduction of dissolved O2, NO−3, Mn4+, Fe3+, and SO24− predominating at successively greater depths
Some of these studies show that methanogenesis occurs in zones where sulfate-reduction is the predominant terminal electron acceptor (Mitterer et al, 2001; D’Hondt et al, 2002, 2004, 2014; Wang et al, 2008), while others show that iron reduction occurs deep in the sulfate-reducing zone (Wang et al, 2008; D’Hondt et al, 2014) or that sulfate reduction occurs deep in the “methanogenic” zone (Holmkvist et al, 2011)
Summary
Microorganisms in subsurface environments compete for electron donors and acceptors as they do in most surface environments (D’Hondt et al, 2002). The predominant terminal electron acceptor is typically inferred to change with sediment depth (e.g., Froelich et al, 1979), with reduction of dissolved O2, NO−3 , Mn4+, Fe3+, and SO24− predominating at successively greater depths After these oxidants are largely exhausted, only fermentation and methanogenesis are left to degrade organic matter (Martens and Berner, 1974; Froelich et al, 1979). These deviations from the generally assumed order of electron acceptor utilization represent a significant challenge when trying to quantify microbial activity in subsurface sediment
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