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.陆地热泉在地球演化历程中持续存在，为生命起源与演化研究提供了宝贵视角。然而如今它们正遭受由气候变化与人类活动引发的不可逆生物多样性丧失，这凸显出保护其独特微生物基因组遗产、解析其内生命过程与生态功能的迫切性。通过对全球热泉宏基因组的分析，我们构建了热泉微生物组基因组（Genomes from Hot Spring Microbiomes, GHM）目录。该目录包含17913个高质量宏基因组组装基因组（metagenome-assembled genomes, MAGs），揭示了大量此前未被认知的细菌与古菌多样性——涵盖超过6000个嗜热类群以及诸多候选门级类群。我们预测了超过2000万个非冗余蛋白编码基因，勾勒出支撑生物地球化学循环以及极端理化条件适应性的代谢蓝图。此外，我们还发现了37258个潜在生物合成基因簇，其中近半数与当前数据库中的已知序列无同源性。我们获取了大量新型病毒类群（共计14606个），并解析了病毒-宿主互作关系，尤其是通过辅助代谢基因重编程宿主代谢网络、调控热泉生态系统关键细胞过程这一途径。GHM目录可作为捕获微生物暗物质、解析陆地热泉生态与演化的重要资源。