A global metagenomic atlas uncovers ubiquitous biosynthetic potential linked to adaptation in extreme environments

Abstract

Extreme environments impose severe physicochemical stresses that drive microorganisms to evolve specialized survival strategies. Microbial secondary metabolites determined by biosynthetic gene clusters (BGCs) are recognized as important mediators of microbial adaptation to environmental stress. However, their ecological roles, particularly habitat-dependent preferences across different environments, remain poorly understood. Although extreme environments provide opportunities to mine microbiomes for unique adaptations, such research is hampered by a lack of systematic overview of its genomic diversity, BGC diversity, and the relationships between them. Here, we constructed a standardized extremophilic genomic catalogue (SEGC) from 1,462 metagenomic samples spanning seven representative extreme habitats. The catalogue comprised 54,661 metagenome-assembled genomes representing 21,805 species, 66.1% of which were previously uncharacterized. With this catalogue, we identified 162,855 BGCs distributed across 81.5% of MAGs. Gene cluster family analysis showed the strong habitat dependence largely explained by species-level habitat specificity. Terpene biosynthetic pathways illustrated habitat-linked adaptive strategies, with hopan-22-ol biosynthesis enriched in acid mine, deep sea and hydrothermal plume environments, while retinal-based phototrophy predominated in cryosphere and saline-alkaline habitats. Metatranscriptomic analyses supported in situ activity of these pathways. In conclusion, we presented a global atlas of biosynthetic potential across extreme-environment microbiota and revealed habitat-dependent patterns of secondary metabolism linked to microbial survival.