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 °C to 93.5 °C), pH (0.85 to 10.3), and tectonic setting, including convergent margins, divergent margins at mid-ocean ridges, and paleo-convergent intraplate plume systems. We identified 9,019 putative biosynthetic gene cluster families, mostly lacking similarity to known biosynthetic gene clusters. Volcanic arc systems consistently exhibited 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 synthetase and ribosomally synthesized and post-translationally modified peptide 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 future natural product discovery in geothermal environments. Competing Interest Statement The authors have declared no competing interest. Footnotes Comprehensive expansion of the Methods section to provide detailed descriptions of all analytical steps; Figures 2, 3, 6 and 7 revised; Supplemental figures updated. https://github.com/giovannellilab/antismash_BGC_geothermal_env