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

Alexander J Probst,Rex R Malmstrom,M Cathryn Ryan,Karthik Anantharaman,Jillian F Banfield,Michaela Stieglmeier,David E Geller-Mcgrath,Christian M K Sieber,Jessica K Jarett,Joanne B Emerson,Tanja Woyke,Andreas Klingl,Brian C Thomas,Bethany Ladd

doi:10.1038/s41564-017-0098-y

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 CO2-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 N2 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.

Highlights

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
A survey of ribosomal proteins predicted from metagenome sequences from Crystal Geyser microbial communities revealed the existence of a large phylogenetic diversity of previously unknown bacteria and archaea in this system[8], and a genomic resolution study documented a high incidence of carbon-fixation pathways[9]
Our microbiological investigation clearly demonstrated a strong stratification of microbial community composition and microbial function with relative groundwater source depths

Summary

Introduction

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. Studies to date have anal ysed samples acquired by drilling[1,2,3], from deep mines[4,5], subsurface research laboratories[6,7] and sites of groundwater discharge[8,9,10,11] These investigations have shown that the terrestrial subsurface is popu lated by a vast array of previously undescribed archaea and bacteria. A survey of ribosomal proteins predicted from metagenome sequences from Crystal Geyser microbial communities revealed the existence of a large phylogenetic diversity of previously unknown bacteria and archaea in this system[8], and a genomic resolution study documented a high incidence of carbon-fixation pathways[9]

Methods

Results

Conclusion