Tectonic setting shapes microbial biosynthetic potential across global geothermal environments

Abstract

Microbial communities in geothermal environments constitute an underexplored reservoir of biosynthetic gene clusters with significant biotechnological potential. Here, we investigate the secondary metabolite potential of 219 microbial communities across marine and continental geothermal field sites, encompassing broad environmental gradients in temperature (4.7{degrees}C to 93.5{degrees}C), pH (0.85 to 10.3), and tectonic setting, including volcanic arcs, backarcs, divergent margins at on-axis mid-ocean ridges, post-subduction extensional arcs, and paleo-convergent intraplate plume systems. We identified 9,019 putative new biosynthetic gene cluster families, mostly lacking similarity to known biosynthetic gene clusters. Volcanic arc systems consistently exhibit the highest diversity of biosynthetic repertoires, whereas intraplate plume systems showed a greater representation of terpene-associated gene cluster families. In contrast, divergent margin systems were primarily characterized by nonribosomal peptide synthetases and ribosomally synthesized and post-translationally modified peptides pathways, together accounting for a large fraction of their predicted biosynthetic diversity. These findings suggest that tectonic context could be associated with large-scale patterns in microbial biosynthetic potential and provide a geobiological framework for guiding natural product discovery in geothermal ecosystems.