Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface

TLDR

An enormous diversity of previously unknown bacteria and archaea has been discovered recently, yet their functional capacities and distributions in the terrestrial subsurface remain uncertain. The study aimed to test whether stratified, sandstone‑hosted aquifers sampled over three phases of a CO₂‑driven geyser eruption cycle harbor microbial communities that differ in membership and function. Researchers continually sampled the geyser over its 5‑day eruption cycle, applying genome‑resolved metagenomics, single‑cell genomics, and geochemical analyses to link microorganisms to groundwater compositions from different depths. The analyses confirmed depth‑dependent community differences, with autotrophic Candidatus “Altiarchaeum sp.” and deep‑branching nanoarchaea dominating the deepest groundwater, a nanoarchaeon inferred as a potential symbiont, Candidate Phyla Radiation bacteria abundant at intermediate depths, microaerophilic Fe‑ and S‑oxidizers replicating rapidly during recovery, autotrophic Sulfurimonas dominating the shallow aquifer, and a total of 104 phylum‑level lineages partitioned between shallow and deep subsurface environments.

Abstract

Abstract An enormous diversity of previously unknown bacteria and archaea has been discovered recently, yet their functional capacities and distributions in the terrestrial subsurface remain uncertain. Here, we continually sampled a CO 2 -driven geyser (Colorado Plateau, Utah, USA) over its 5-day eruption cycle to test the hypothesis that stratified, sandstone-hosted aquifers sampled over three phases of the eruption cycle have microbial communities that differ both in membership and function. Genome-resolved metagenomics, single-cell genomics and geochemical analyses confirmed this hypothesis and linked microorganisms to groundwater compositions from different depths. Autotrophic Candidatus “Altiarchaeum sp.” and phylogenetically deep-branching nanoarchaea dominate the deepest groundwater. A nanoarchaeon with limited metabolic capacity is inferred to be a potential symbiont of the Ca . Altiarchaeum”. Candidate Phyla Radiation bacteria are also present in the deepest groundwater and they are relatively abundant in water from intermediate depths. During the recovery phase of the geyser, microaerophilic Fe- and S-oxidizers have high in situ genome replication rates. Autotrophic Sulfurimonas sustained by aerobic sulfide oxidation and with the capacity for N 2 fixation dominate the shallow aquifer. Overall, 104 different phylum-level lineages are present in water from these subsurface environments, with uncultivated archaea and bacteria partitioned to the deeper subsurface.