Complex subsurface hydrothermal fluid mixing at a submarine arc volcano supports distinct and highly diverse microbial communities

Abstract

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.

Degradation of biological macromolecules supports uncultured microbial populations in Guaymas Basin hydrothermal sediments

“…Then, Quant bins estimates the abundance of MAGs in each sample by computing a length-weighted average of the MAG’s contigs CPMs. We analyzed published metagenomes of hydrothermal ecosystems in Guaymas Basin [ 7 , 48 , 49 ] (16 datasets), of the Mid-Atlantic Ridge (4 datasets) [ 50 ], of Okinawa Trough (4 datasets) [ 51 ] and Brothers submarine volcano (6 datasets) [ 52 ], and of hadal sediments from the Yap Trench (3 datasets) [ 53 ] (Supplementary Data 4 ).…”

Metagenomic Data Assembly – The Way of Decoding Unknown Microorganisms

“…Another study (Reysenbach et al, 2020) led to discovery of numerous never seen before life-forms living in 1,800 metersdeep volcano's acid jets. Investigating metagenome-assembled genomes of the microbial communities inhabiting such extreme and dynamic systems 90 putative bacterial and archaeal genomic families and about 300 previously unknown genera, as well as a good number of potentially endemic to the submarine volcanic environment were identified.…”

“…Different studies use different assembly approaches by creating their own state-of-the-art assembly pipeline (Nayfach et al, 2020) or using different publicly available assembly tools (Castelle et al, 2015;Zaremba-Niedzwiedzka et al, 2017;Goltsman et al, 2018;Chiu and Miller, 2019;Reysenbach et al, 2020;Almeida et al, 2021) but all of them required metagenomic assembly.…”

Taphonomy of microorganisms and microbial microtextures at sulfidic hydrothermal vents: A case study from the Roman Ruins black smokers, Eastern Manus Basin

“…Detailed information now exists about the interactions between microbes and their dynamic fluid environment, and the physiologies and metabolisms of microspecies, which can be deduced from genomic or biomarker analyses (e.g. Huber et al, 2007; McCollom & Schock, 1997; Nakagawa et al, 2005; Nercessian et al, 2005; Reysenbach et al, 2020; Skennerton et al, 2015; Takai & Hirokoshi, 1999; Xie et al, 2011). Insights into these microbe–mineral systems can also be gained from fossil microorganisms and microbially induced mineral textures.…”