Vertical distribution and metabolic diversity of autotrophic microbes in the deep sediment of the challenger deep

Carbon fixation in marine ecosystems is a vital process that contributes to climate regulation, with ocean sediments playing a critical role in carbon sequestration. This process is driven by chemolithoautotrophy in marine sediments, fueled by reduced compounds, such as those containing nitrogen and sulfur. However, the vertical distribution of microbial autotrophs and their energy coupling systems remain poorly understood in many sediments. In this study, we investigated a 750 cm sediment core from the Challenger Deep, the deepest point on Earth, which harbors abundant and diverse microbes under extreme conditions.

To explore the autotrophic characteristics across redox conditions in this core, we characterized the microbial community, metagenome, and metagenome-assembled genomes (MAGs), and their potential for carbon fixation processes and associated energy metabolism. The Wood-Ljungdahl (WL) pathway, primarily driven by Planctomycetota and Aerophobota, and the reverse oxidative TCA (roTCA) cycle, primarily driven by Bacteroidota and Gemmatimonadota, were the dominant predicted carbon fixation pathways, with hydrogen as the primary energy source, coupled to nitrogen and sulfur metabolism. Notably, the 3-hydroxypropionate/4-hydroxybutyrate (3HP/4HB) cycle, mediated by Nitrososphaeria, showed the highest abundance in the oxidized environment (15-27 cm below the seafloor), where ammonia oxidation likely served as the primary energy source. Gammaproteobacteria were predicted to utilise sulfur oxidation, whereas Alphaproteobacteria and Chloroflexota used hydrogen to drive the Calvin-Benson-Bassham (CBB), reductive glycine pathway (rGly) in Alphaproteobacteria and the dicarboxylate/4-hydroxybutyrate cycle (DC/4HB) in Chloroflexota, respectively. The abundance of carbon fixation, and nitrogen, sulfur and hydrogen cycling functional genes were significantly correlated with environmental factors (NH₄⁺ and SiO₃^2-) based on Pearson's correlation analysis.

This study reveals the vertical distribution of microbial carbon fixation potential and diversity in sediments driven by redox conditions, highlights the crucial role of hydrogen as an energy source, and provides new insights for optimizing global deep-sea carbon cycle models. Collectively, these findings extend the redox tower theory by revealing a hadal-sediment specific distribution of autotrophic genes, characterized by persistent enrichment of energetically efficient pathways and dominant hydrogen-based energy coupling across deep sediment layers.