Deep-sea volcanoes are biological hotspots nurtured by diverse hydrothermal mineral formations that contribute important chemical fluxes to the deep ocean. Yet, they are still some of the least explored features on the sea floor. Two distinct hydrothermal systems co-occur in the caldera of Brothers volcano in the Kermadec arc northeast of New Zealand. Two resurgent volcanic cones inside the caldera discharge magmatically-influenced hydrothermal fluids while, just 3 km away, seawater-influenced hydrothermal fluids are expelled from Cu-Zn-Au rich chimneys. How changes in the hydrothermal regime during the evolution of the volcano have shaped the microbial communities, is unknown. We reconstructed over 800 genomes from 18 Brothers volcano hydrothermal vent sites and demonstrate that the complex hydrologic evolution and subsurface hydrology of the volcano drives the rich microbial genomic diversity. We discovered about 65 bacterial and 29 archaeal genomic new families that encompass nearly 300 new genera. Within the Archaea alone, in addition to new members of phyla like the Heimdalarchaeota and Hydrothermarchaeota, the first deep-sea non-ammonia oxidizing thaumarchaeote genome closely related to one from Yellowstone National Park was obtained. Half of the archaeal genomes from the lower cone site are members of the archaeal DPANN superphylum, that have small genomes and are likely symbiotic. Comparative amplicon data from Brothers volcano and deep-sea hydrothermal vents, revealed two distinct microbial communities associated with hydrothermal activity on the caldera wall that differ at very small spatial scales (i.e. between adjacent chimneys). Much like in the Yellowstone caldera, where acid hot springs can be directly adjacent to alkaline hot spings, it is the complexity of the hydrological environment in caldera walls that manifests itself as an underlying imprint on differences in the microbial community diversity. This points to the importance of considering the geological legacy and subsurface hydrologic fluid regime in understanding drivers of microbial community diversity, assembly and evolution. These more than 800 Brothers volcano genomes, may hold secrets to new enzymes and tecnologies. During the research expedition day to day operations were share on a public website Divediscover.org. Two undergraduate students were involved in the research. Last Modified: 10/06/2019 Submitted by: Anna-Louise Reysenbach