Uniform selective pressures within redox zones drive gradual changes in microbial community composition in hadal sediments

Abstract

Microbial communities in marine sediments are highly diverse, yet the processes that give rise to this complexity are unclear. It has been proposed that benthic microbial communities must be continuously re‐seeded from the water column because dispersal within the sediment is severely limited. Previous studies consistently report that the composition of the microbial community gradually changes with sediment depth. However, the relative contributions of the processes that underlie these compositional gradients have not been determined, and it is unknown whether microbial dispersal is indeed too slow to outpace burial. Here, we applied ecological statistical frameworks to 16S rRNA gene amplicon‐based community composition data from Atacama Trench sediments to investigate the links between biogeochemistry, burial, and microbial community assembly processes. We confirm that dispersal limitation affects microbial communities and find that gradual changes in community composition are driven by selective pressures that change abruptly across the discrete boundaries between redox zones rather than along continuous biogeochemical gradients, while selective pressures are uniform within each zone. The gradual changes in community composition over centimetres of depth within a zone hence reflects a decades‐long response to the abruptly changing selective pressures.

Strong linkage between benthic oxygen uptake and bacterial tetraether lipids in deep-sea trench regions

“…The empirical relationships between brGDGTs and environmental parameters, whether driven by the direct physiological adaptations of source bacteria to changing environments, and/or the indirect restructuring of bacterial communities, remain an open question 52 . Several biogeochemical and microbial studies have investigated the sites examined in this study 38 , 53 – 55 . Our trench core sediments display redox stratification into oxic, nitrogenous, and ferruginous zones 53 , 54 .…”

“…Several biogeochemical and microbial studies have investigated the sites examined in this study 38 , 53 – 55 . Our trench core sediments display redox stratification into oxic, nitrogenous, and ferruginous zones 53 , 54 . Despite bathymetric and depositional heterogeneity, microbial communities exhibit high similarities among sediments sharing similar redox stratifications within each trench, while vary strongly with sediment depth following redox gradients 55 .…”

Particulate Organic Matter in the Atacama Trench: Tracing Sources and Possible Transport Mechanisms to the Hadal Seafloor

“…For example, this could be driven by bacterial processes such as anammox leading to rapid nitrogen loss within a shallow layer of the sediment surface (Thamdrup et al., 2021). Other recent studies have also highlighted potential physiological adaptations of the benthic microbial community to the high‐pressure and low‐temperature present in the hadal realm though cell membrane lipid composition (Flores et al., 2022; Tamby et al., 2023), whereas long‐term selective forces, where co‐existing taxa are more dissimilar and the phylogenetic turnover is greater than expected over the redox zone, lead to large community shifts over time (Schauberger et al., 2023). Together, changes in the chemical composition of benthic microbes as well as their metabolisms could alter the overall elemental and stable isotope composition of sedimentary OM.…”

Metagenome-assembled genomes of deep-sea sediments: changes in microbial functional potential lag behind redox transitions

“…In continental sediments where a similar redox zonation is found, sediment mixing by bioturbation blurs relationships between community composition and redox gradients [ 21 ]. By contrast, hadal trench sediments are hardly affected by bioturbation due to the lack of burrowing macroinfauna [ 14 , 22 ], which makes them great model systems to explore the succession of microbial communities and their functions alongside biogeochemical gradients [ 23 ].…”