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 ~3 m 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). Along the perennial- and seasonal-OMZ sediment-cores microbial communities were predominated by Gammaproteobacteria/Alphaproteobacteria and Euryarchaeota/Firmicutes respectively. As a perennial-OMZ signature, a cryptic methane production-consumption cycle was found to operate near the sediment-surface; 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. We discerned that 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 metabolites 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-colum n oxygenation regimes.