Microorganisms oxidize glucose through distinct pathways in permeable and cohesive sediments

In marine sediments, microbial degradation of organic matter under anoxic conditions is generally thought to proceed through fermentation to volatile fatty acids, which are then oxidized to CO2 coupled to the reduction of terminal electron acceptors (e.g. nitrate, iron, manganese, and sulfate). It has been suggested that, in environments with a highly variable oxygen regime, fermentation mediated by facultative anaerobic bacteria (uncoupled to external terminal electron acceptors) becomes the dominant process. Here, we present the first direct evidence for this fermentation using a novel differentially labeled glucose isotopologue assay that distinguishes between CO2 produced from respiration and fermentation. Using this approach, we measured the relative contribution of respiration and fermentation of glucose in a range of permeable (sandy) and cohesive (muddy) sediments, as well as four bacterial isolates. Under anoxia, microbial communities adapted to high-energy sandy or bioturbated sites mediate fermentation via the Embden-Meyerhof-Parnas pathway, in a manner uncoupled from anaerobic respiration. Prolonged anoxic incubation suggests that this uncoupling lasts up to 160 h. In contrast, microbial communities in anoxic muddy sediments (smaller median grain size) generally completely oxidized 13C glucose to 13CO2, consistent with the classical redox cascade model. We also unexpectedly observed that fermentation occurred under oxic conditions in permeable sediments. These observations were further confirmed using pure cultures of four bacteria isolated from permeable sediments. Our results suggest that microbial communities adapted to variable oxygen regimes metabolize glucose (and likely other organic molecules) through fermentation uncoupled to respiration during transient anoxic conditions.