Hawaiian geothermal fumaroles contain diverse and novel viruses.

UNLABELLED: Viral community structure is known to influence the evolution of microbes in diverse and complex environments. While the diversity of microbes and their viruses have been metagenomically explored in terrestrial hot springs and hydrothermal vent systems, other volcanic features remain remarkably understudied. Fumaroles (steam vents) are geothermal features that heat groundwater with magma, releasing heated water vapor and volcanic gases, such as CO2 and H2S. Fumaroles are physicochemically dynamic compared to terrestrial hot springs-temperatures and gas emissions fluctuate rapidly with volcanic activity. The viral community structures and diversity have never been systematically characterized or explored. We hypothesize that viruses facilitate microbial community adaptation to the harsh and dynamic fumarole environment. Using a sensitive profile-based approach for identification, we identify 383 viral operational taxonomic units (vOTUs) from 46 metagenomes of biofilms hosted near basaltic fumaroles. We estimate two previously undescribed order-level clades of Caudoviricetes (tailed phages), and find evidence of phylogenetic diversification within the fumarole systems. Read-mapping analysis of three sampled geothermal regions shows unexpected diversity and community structure within the geologic system: 99.7% of fumarole vOTUs are shared between distant fumaroles, and 40°C-60°C biofilms have high viral richness and evenness that do not correspond to biofilm microbial composition or diversity. Lastly, we provide the first description of a terrestrial environment dominated by Microviridae, which has only been described in viral communities of deep-ocean hydrothermal vents. Our study offers a unique geological system for the exploration of viral ecology in extreme environments.

IMPORTANCE: Geothermal environments serve as natural laboratories for studying adaptations to extreme conditions that challenge the limits of microbial life and offer insight into early life on Earth. Exploring microbial diversity in these systems reveals how ecological factors shape complex communities in extreme environments. Evidence increasingly shows that viruses influence microbial diversity in terrestrial hot springs and oceanic hydrothermal vents, yet the biogeography of viruses across these systems remains largely unexplored. We present the first metagenomic characterization of viral diversity and ecology in Hawaiian terrestrial volcanic fumaroles. Our results indicate extensive viral dispersal, in contrast to the typically more constrained dispersal observed in hot springs and hydrothermal vent systems. Furthermore, we observe a dominance of ssDNA viruses in fumarole viral communities, a pattern not previously reported in terrestrial systems. Our comprehensive analyses indicate that Hawaiian fumaroles are a valuable system for studying community patterns and the ecological determinants of viral biogeography.