Hydrothermally active submarine volcanoes are mineral-rich biological oases contributing significantly to chemical fluxes in the deep sea, yet little is known about the microbial communities inhabiting these systems. Here we investigate the diversity of microbial life in hydrothermal deposits and their metagenomics-inferred physiology in light of the geological history and resulting hydrothermal fluid paths in the subsurface of Brothers submarine volcano north of New Zealand on the southern Kermadec arc. From metagenome-assembled genomes we identified over 90 putative bacterial and archaeal genomic families and nearly 300 previously unknown genera, many potentially endemic to this submarine volcanic environment. While magmatically influenced hydrothermal systems on the volcanic resurgent cones of Brothers volcano harbor communities of thermoacidophiles and diverse members of the superphylum “DPANN,” two distinct communities are associated with the caldera wall, likely shaped by two different types of hydrothermal circulation. The communities whose phylogenetic diversity primarily aligns with that of the cone sites and magmatically influenced hydrothermal systems elsewhere are characterized predominately by anaerobic metabolisms. These populations are probably maintained by fluids with greater magmatic inputs that have interacted with different (deeper) previously altered mineral assemblages. However, proximal (a few meters distant) communities with gene-inferred aerobic, microaerophilic, and anaerobic metabolisms are likely supported by shallower seawater-dominated circulation. Furthermore, mixing of fluids from these two distinct hydrothermal circulation systems may have an underlying imprint on the high microbial phylogenomic diversity. Collectively our results highlight the importance of considering geologic evolution and history of subsurface processes in studying microbial colonization and community dynamics in volcanic environments.

热液活跃的海底火山是富含矿物质的生物绿洲，对深海的化学通量做出了重大贡献，但对居住在这些系统中的微生物群落知之甚少。在这里，我们根据地质历史和新西兰北部克马德克弧南部兄弟海底火山地下的热液流体路径，研究热液矿床中微生物生命的多样性及其宏基因组学推断的生理学。从宏基因组组装的基因组中，我们确定了 90 多个推定的细菌和古细菌基因组家族以及近 300 个以前未知的属，其中许多可能是这种海底火山环境的特有种。虽然受岩浆影响的热液系统对兄弟火山的火山复活锥体有嗜热嗜酸菌群落和超门“DPANN”的不同成员，但两个不同的群落与火山口壁相关，可能由两种不同类型的热液循环形成。其系统发育多样性主要与其他地方的锥体和受岩浆影响的热液系统一致的群落主要以厌氧代谢为特征。这些种群可能由具有更大岩浆输入的流体维持，这些流体与先前改变的不同（更深）矿物组合相互作用。然而，近端（几米远）群落具有基因推断的需氧、微需氧、较浅的海水占主导地位的循环可能支持厌氧代谢。此外，来自这两个不同的热液循环系统的流体的混合可能对高微生物系统发育多样性有潜在的影响。总的来说，我们的研究结果强调了在研究火山环境中的微生物定植和群落动态时考虑地质演化和地下过程历史的重要性。