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

Abstract

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.

Extremely oligotrophic and complex carbon degrading microaerobic bacteria from Arabian Sea oxygen minimum zone sediments

“…Marine sediments constitute one of the largest microbiomes on Earth (Hoshino et al 2020), and act as the largest sink of organic carbon within the biosphere (Kallmeyer et al 2012; Jørgensen et al 2022; Ruben et al 2023). Particularly within the shelf/slope territories of the continental margins, productivity in the oceanic water column, rate of sedimentation, and the extent of organic matter delivery to the seafloor are all very high, consequent to which O 2 , followed by the less energy-efficient respiratory substrates such as nitrate, manganic, ferric, etc., get depleted within relatively shallow sediment depths (Canfield 1994; Seiter et al 2005; Burdige 2007; Komada et al 2016; Bhattacharya et al 2021; Sarkar et al 2022). This phenomenon is further accentuated in the mid-oceanic oxygen minimum zones (OMZs) that occur perennially along the western margins of the Earth’s continents, and are considered to be the crucial bellwethers of ocean warming, deoxygenation, and acidification caused by global climate change (Wright et al 2012; Long et al 2021).…”

“…The deposition and degradation dynamics, i.e. the concentration, chemical nature, and fate of the organic matter that is delivered to the seafloor, determine the microbiome structure and function in the sediment system across the continental margin (Bhattacharya et al 2021). With increasing water-depth (distance from the coast), lower sedimentation rate, so greater O 2 -exposure time (irrespective of the O 2 concentration of the bottom-water) for the breakdown of the buried organic matter into simpler compounds, is encountered in the sediment surface (Canfield 1994; Kristensen et al 1995; Burdige 2007; Middelburg 2019; Bhattacharya et al 2021); consequently, down the sediment depths there is a core-wide intensification of the simple-fatty-acids-requiring anaerobic metabolisms of the carbon-sulfur cycle (Fernandes et al 2018).…”

“…Whereas post-burial degradation of complex organic matter in the top-most strata of these sulfide-containing sediment systems is attributable to aerobic bacterial catabolism (Bhattacharya et al 2021), it is remarkable that obligately aerobic bacteria are present and active (Bhattacharya et al 2020), alongside sulfate-respiring anaerobes (Fernandes et al 2018), across a ∼3 meter sediment horizon of the Arabian Sea OMZ (ASOMZ), i.e. from the seafloor up to the depths where both organic carbon and sulfate are depleted and methane biogenesis begins (Fernandes et al 2018).…”

“…The deposition and degradation dynamics, i.e. the concentration, chemical nature, and fate of the organic matter that is delivered to the seafloor, determine the microbiome structure and function in the sediment system across the continental margins (Bhattacharya et al 2021). With increasing water-depth and distance from the coast, sedimentation rate decreases, and the organic matter delivered to the seafloor gets exposed to O 2 for longer periods of time.…”

“…With increasing water-depth and distance from the coast, sedimentation rate decreases, and the organic matter delivered to the seafloor gets exposed to O 2 for longer periods of time. As a consequence, irrespective of the O 2 concentration of the bottom-water, faster breakdown of complex organic matter into simpler compounds takes place in the sediment surface (Canfield 1994; Kristensen et al 1995; Burdige 2007; Middelburg 2019; Bhattacharya et al 2021). Across the sediment-depths, this leads to an overall intensification of the simple-fatty-acids-requiring anaerobic metabolisms such as sulfate reduction and methanogenesis (Fernandes et al 2018; Bhattacharya et al 2021).…”