Microbial and Reactive Transport Modeling Evidence for Hyporheic Flux-Driven Cryptic Sulfur Cycling and Anaerobic Methane Oxidation in a Sulfate-Impacted Wetland-Stream System

This study reexamines the common expectations that in freshwater systems, sulfur plays a minor role in carbon cycling, and aerobic processes dominate methane oxidation. In anoxic sediments of a sulfate-impacted wetland-stream system in Minnesota (USA), a reactive transport model calibrated to geochemical observations predicted sulfate reduction to be the major terminal electron accepting process, and it showed that anaerobic oxidation of methane predominantly coupled with sulfate reduction attenuated methane concentrations near the sediment-water interface. Consistent with model results, 16S rRNA microbiome analysis revealed a high relative abundance of taxa capable of dissimilatory sulfate reduction. It further supported the conclusion that high simulated sulfate reduction rates could be maintained by a cryptic sulfur cycle coupled to iron and methane. Low relative abundance of known iron reducing bacteria raised the possibility of abiotic ferric iron (Fe) reduction driving sulfide reoxidation to intermediate-valence sulfur forms; widespread potential for microbially mediated disproportionation, oxidation, and reduction of sulfur intermediates provided mechanisms for completing redox cycles; and archaea comprising up to 25% of the microbial community could include consortia capable of anaerobic oxidation of methane. These biogeochemical processes were found to be controlled by hyporheic fluxes. Lower-magnitude fluxes in wetland compared to channel sediments created sharper geochemical gradients that generated greater heterogeneity in microbial distributions and reaction rates. Changes in upward flux caused fluctuations in sulfate concentrations that led to alternating simulations of methane production and transport. Our work supports the importance of hyporheic flux-driven iron-sulfur-methane cycling in sulfate-impacted wetlands and prompts further investigations under freshwater conditions. Key Points Reactive transport model and microbiome analysis quantify and describe hyporheic flux-driven Fe-S-CH 4 processes in sulfate-impacted wetlands Cryptic S cycling, coupled to Fe reduction and anaerobic CH 4 oxidation and involving S intermediates, may drive high sulfate reduction rates Dynamic hyporheic fluxes control spatial distributions of microbial compositions and spatiotemporal distributions of reaction rates