Sedimentation rate and organic matter dynamics shape microbiomes across a continental margin

Abstract. Marine sedimentation rate and bottom-water O2 concentration control the remineralization/sequestration of organic carbon across continental margins; but whether/how they shape microbiome architecture (the ultimate effector of all biogeochemical phenomena), across shelf/slope sediments, is unknown. Here we reveal distinct microbiome structures and functions, amidst comparable pore fluid chemistries, along 300 cm sediment horizons underlying the seasonal (shallow coastal) and perennial (deep sea) oxygen minimum zones (OMZs) of the Arabian Sea, situated across the western-Indian margin (water-depths: 31 m and, 530 and 580 m, respectively). The sedimentary geomicrobiology was elucidated by analyzing metagenomes, metatranscriptomes, and enrichment cultures, and also sedimentation rates measured by radiocarbon and lead excess (210Pbxs); the findings were then evaluated in the light of the other geochemical data available for the cores investigated. Along the perennial- and seasonal-OMZ sediment cores, microbial communities were dominated by Gammaproteobacteria and Alphaproteobacteria, and Euryarchaeota and Firmicutes, respectively. As a perennial-OMZ signature, a cryptic methane production-consumption cycle was found to operate near the sediment-surface (within the sulfate reduction zone); overall diversity, as well as the relative abundances of simple-fatty-acids-requiring anaerobes (methanogens, anaerobic methane-oxidizers, sulfate-reducers and acetogens), peaked in the topmost sediment-layer and then declined via synchronized fluctuations until the sulfate-methane transition zone was reached. The entire microbiome profile was reverse in the seasonal-OMZ sediment horizon. In the perennial-OMZ sediments organic carbon deposited was higher in concentration and marine components-rich, so it potentially degraded readily to simple fatty acids; lower sedimentation rate afforded higher O2 exposure time for organic matter degradation despite perennial hypoxia in the bottom-water; thus, the resultant abundance of reduced carbon substrates sustained multiple inter-competing microbial processes in the upper sediment-layers. Remarkably, the whole geomicrobial scenario was opposite in the sediments of the seasonal/shallow-water OMZ. Our findings create a microbiological baseline for understanding carbon-sulfur cycling across distinct marine depositional settings and water-column oxygenation regimes.