Carbon metabolic versatility underpins Bathyarchaeia ecological significance across the global deep subsurface

Abstract

Bathyarchaeia, among the most ancient and abundant microbial lineages on Earth, dominate diverse anoxic subsurface ecosystems and play a pivotal role in global carbon cycling. This review synthesizes current understanding of their physiological, metabolic, and evolutionary foundations underlying their ecological significance and environmental effects over geological timescales. Despite their global distribution in the deep biosphere, the phylogenetic diversity and total cellular abundance of Bathyarchaeia remain substantially underestimated. As uncultivated metabolic generalists, Bathyarchaeia exhibit remarkable metabolic versatility, including anaerobic organic degradation, dark carbon fixation, and putative methane and alkane metabolism. Specifically, genus Baizosediminiarchaeum has been demonstrated to adopt organomixotrophy by coupling anaerobic lignin degradation with inorganic carbon assimilation. These metabolic strategies likely enable them to thrive in energy-limited subsurface environments with dynamic geochemical fluctuations. The early evolutionary history of Bathyarchaeia appears closely linked to major geological events, including tectonic activity and plant evolution, whereas more recent lineage expansions reflect physiological adaptations to host-associated and anthropogenically influenced environments, highlighting their ongoing co-evolution with Earth’s modern environments. Overall, we propose carbon metabolic innovation as the central driver behind the ecological and evolutionary significance of Bathyarchaeia, putatively linking microbial ecological functions to planetary biogeochemical processes. Future efforts in isolation and cultivation remain essential for elucidating their unknown physiological and metabolic mechanisms. In parallel, advances in ecological modeling and the development of lineage-specific lipid biomarkers hold great promise for quantifying their contributions to global carbon budgets and reconstructing paleoenvironmental and paleoclimate conditions.