Redox effects on the microbial degradation of refractory organic matter in marine sediments

Abstract Microbially mediated reduction–oxidation (redox) reactions are often invoked as being the mechanisms by which redox state influences the degradation of sedimentary organic matter (OM) in the marine environment. To evaluate the effects of elevated, oscillating and reduced redox potentials on the fate of primarily aged, mineral-adsorbed OM contained in continental shelf sediments, we used microbial fuel cells to control redox state within and around marine sediments, without amending the sediments with reducing or oxidizing substances. We subsequently followed electron fluxes in the redox elevated and redox oscillating treatments, and related sediment chemical, isotopic and bacterial community changes to redox conditions over a 748-day experimental period. The electron fluxes of the elevated and oscillating redox cells were consistent with models of organic carbon (OC) oxidation with time-dependent first-order rate constants declining from 0.023 to 0.005 y −1 , in agreement with rate constants derived from typical OC profiles and down core ages of offshore sediments, or from sulfate reduction rate measurements in similar sediments. Moreover, although cumulative electron fluxes were higher in the continuously elevated redox treatment, incremental rates of electron harvesting in the two treatments converged over the 2 year experiment. These similar rates were reflected in chemical indicators of OM metabolism such as dissolved OC and ammonia, and particulate OC concentrations, which were not significantly different among all treatments and controls over the experimental time-scale. In contrast, products of carbonate and opal dissolution and metal mobilization showed greater enrichments in sediments with elevated and oscillating redox states. Microbial community composition in anode biofilms and surrounding sediments was assessed via high-throughput 16S rRNA gene sequencing, and these analyses revealed that the elevated and oscillatory redox treatments led to the enrichment of Deltaproteobacteria on the sediment-hosted anodes over time. Many Deltaproteobacteria are capable of using electrodes as terminal electron acceptors to completely oxidize organic substrates. Notably, Deltaproteobacteria were not measurably enriched in the sediments adjacent to anodes, suggesting that – in these experiments – electron-shuttling bacterial networks did not radiate out away from the electrodes, affecting millimeters or centimeters of sediment. Rather, microbial phylotypes allied to the Clostridia appeared to dominate in the sediment amongst all treatments, and likely played essential roles in converting complex dissolved and particulate sources of OM to simple fermentation products. Thus, we advance that the rate at which fermentation products are generated and migrate to oxidation fronts is what limits the remineralization of OM in many subsurface sediments removed from molecular oxygen. This is a diagenetic scenario that is consistent with the discharging behavior of redox oscillating sediment MFCs. It is also compatible with hypotheses that molecular O 2 – and not just the resulting elevated redox potential – may be required to effectively catalyze the degradation of refractory OM. Such decomposition reactions have been suggested to depend on substrate interactions with highly reactive oxygen-containing radicals and/or with specialized extracellular enzymes produced by aerobic prokaryotic or eukaryotic cells.