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

Abstract

Marine sedimentation rate and bottom-water O2 concentration control organic carbon remineralization and sequestration across continental margins, but whether and how they shape microbiome architecture (the ultimate effector of all biogeochemical phenomena) across shelf and slope sediments is still unclear. Here we reveal distinct microbiome structures and functions, amidst comparable pore fluid chemistries, along 300 cm sediment horizons underlying the seasonal (shallow coastal; water depth: 31 m) and perennial (deep sea; water depths: 530 and 580 m) oxygen minimum zones (OMZs) of the Arabian Sea, situated across the western Indian margin. The sedimentary geomicrobiology was elucidated by analyzing metagenomes, metatranscriptomes, enrichment cultures, and depositional rates measured via radiocarbon and lead excess dating; the findings were then evaluated in light of the other geochemical data available for the cores. Along the perennial-OMZ sediment cores, microbial communities were dominated by Gammaproteobacteria and Alphaproteobacteria, but in the seasonal-OMZ core communities were dominated by Euryarchaeota and Firmicutes. 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 anaerobes requiring simple fatty acids (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 microbiome profile was completely reversed in the seasonal-OMZ sediment horizon. In the perennial-OMZ sediments, deposited organic carbon was higher in concentration and rich in marine components that degrade readily to simple fatty acids; simultaneously, lower sedimentation rate afforded higher O2 exposure time for organic matter degradation despite perennial hypoxia in the bottom water. The resultant abundance of reduced carbon substrates eventually sustained multiple inter-competing microbial processes in the upper sediment layers. The entire geomicrobial scenario was opposite in the sediments of the seasonal OMZ. These findings create a microbiological baseline for understanding carbon-sulfur cycling in distinct depositional settings and water column oxygenation regimes across the continental margins.