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

Journal Article · · Nature Microbiology
 [1];  [2];  [3];  [1];  [4];  [1];  [1];  [1];  [3];  [5];  [5]; ORCiD logo [3]; ORCiD logo [2]; ORCiD logo [1]
  1. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
  2. Univ. of Calgary, AB (Canada). Dept. of Geoscience
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Ludwig Maximilian Univ., Munich (Germany). Plant Development and Electron Microscopy. Dept. of Biology

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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); Sloan Foundation (United States); German Research Foundation (DFG); Natural Sciences and Engineering Research Council of Canada (NSERC)
Grant/Contract Number:
AC02-05CH11231; SC0010566; G-2016-20166041; PR 1603/1-1
OSTI ID:
1436345
Journal Information:
Nature Microbiology, Vol. 3; ISSN 2058-5276
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 113 works
Citation information provided by
Web of Science

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Phylogenetic and structural diversity of aromatically dense pili from environmental metagenomes journal October 2019
Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria journal March 2020
A novel bacterial sulfur oxidation pathway provides a new link between the cycles of organic and inorganic sulfur compounds journal June 2018
Comparison of sulfide‐oxidizing Sulfurimonas strains reveals a new mode of thiosulfate formation in subsurface environments journal January 2020
Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria journal January 2019
Nano-Sized and Filterable Bacteria and Archaea: Biodiversity and Function journal August 2018
MetaCHIP: community-level horizontal gene transfer identification through the combination of best-match and phylogenetic approaches journal March 2019
Methane oxidation and methylotroph population dynamics in groundwater mesocosms journal April 2020
Consistent Metagenome-Derived Metrics Verify and Delineate Bacterial Species Boundaries journal January 2020
Small and mighty: adaptation of superphylum Patescibacteria to groundwater environment drives their genome simplicity journal April 2020
Structure and function of archaeal histones journal September 2018
Genome-reconstruction for eukaryotes from complex natural microbial communities journal March 2018
An archaeal symbiont-host association from the deep terrestrial subsurface journal May 2019
Statistical Analysis of Community RNA Transcripts between Organic Carbon and Geogas-Fed Continental Deep Biosphere Groundwaters journal August 2019
The rise of diversity in metabolic platforms across the Candidate Phyla Radiation journal June 2020
Genome analyses of uncultured TG2/ZB3 bacteria in ‘Margulisbacteria’ specifically attached to ectosymbiotic spirochetes of protists in the termite gut journal October 2018
Perspectives on Cultivation Strategies of Archaea journal August 2019
Niche differentiation is spatially and temporally regulated in the rhizosphere journal January 2020
Genomic diversity, lifestyles and evolutionary origins of DPANN archaea journal January 2019
Depth-discrete metagenomics reveals the roles of microbes in biogeochemical cycling in the tropical freshwater Lake Tanganyika journal February 2021
High-Level Abundances of Methanobacteriales and Syntrophobacterales May Help To Prevent Corrosion of Metal Sheet Piles journal August 2019
Genomic Description of ‘Candidatus Abyssubacteria,’ a Novel Subsurface Lineage Within the Candidate Phylum Hydrogenedentes journal August 2018
Microaerobic conditions caused the overwhelming dominance of Acinetobacter spp. and the marginalization of Rhodococcus spp. in diesel fuel/crude oil mixture-amended enrichment cultures journal October 2019
Unexpected host dependency of Antarctic Nanohaloarchaeota journal June 2019
Capability for arsenic mobilization in groundwater is distributed across broad phylogenetic lineages journal September 2019
Biosynthetic capacity, metabolic variety and unusual biology in the CPR and DPANN radiations journal September 2018
Genome‐inferred spatio‐temporal resolution of an uncultivated Roizmanbacterium reveals its ecological preferences in groundwater journal December 2019
The Fe(II)-oxidizing Zetaproteobacteria : historical, ecological and genomic perspectives journal January 2019
Time Series Genome-Centric Analysis Unveils Bacterial Response to Operational Disturbance in Activated Sludge journal July 2019
Accurate and complete genomes from metagenomes journal March 2020
Groundwater cable bacteria conserve energy by sulfur disproportionation journal November 2019
Homologous Recombination and Transposon Propagation Shape the Population Structure of an Organism from the Deep Subsurface with Minimal Metabolism journal March 2018
Genomic and in-situ Transcriptomic Characterization of the Candidate Phylum NPL-UPL2 From Highly Alkaline Highly Reducing Serpentinized Groundwater journal December 2018