Microbial dark matter and their metabolic potential in terrestrial hot springs

Terrestrial hot springs have persisted throughout Earth’s history, offering valuable insights into the origin and evolution of life. Yet they are now undergoing irreversible biodiversity loss driven by climate change and human activities, underscoring the urgent need to preserve their unique microbial genomic heritage and decipher the life processes and ecological functions within them. By analyzing hot spring metagenomes worldwide, we constructed the Genomes from Hot Spring Microbiomes (GHM) catalog. The GHM catalog comprises 17,913 high-quality metagenome-assembled genomes (MAGs), revealing vast, previously unrecognized bacterial and archaeal diversity—including over 6,000 thermophilic lineages and numerous candidate phyla. We predicted over 20 million non-redundant protein-coding genes, delineating the metabolic blueprints that sustain biogeochemical cycling and adaptation to extreme physicochemical conditions. Additionally, we uncovered 37,258 putative biosynthetic gene clusters, nearly half of which show no similarity to known sequences in current databases. We recovered a substantial diversity of novel viral lineages (n = 14,606) and identified virus-host interactions, particularly through auxiliary metabolic genes that reprogram host metabolic networks and modulate key cellular processes in hot spring ecosystems. The GHM catalog serves as a vital resource for capturing microbial dark matter and understanding the ecology and evolution of terrestrial hot springs.