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

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.

Authors:
 [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
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); Sloan Foundation (United States); German Research Foundation (DFG); Natural Sciences and Engineering Research Council of Canada (NSERC)
OSTI Identifier:
1436345
Grant/Contract Number:  
AC02-05CH11231; SC0010566; G-2016-20166041; PR 1603/1-1
Resource Type:
Accepted Manuscript
Journal Name:
Nature Microbiology
Additional Journal Information:
Journal Volume: 3; Journal ID: ISSN 2058-5276
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biogeochemistry; environmental microbiology; metagenomics; symbiosis

Citation Formats

Probst, Alexander J., Ladd, Bethany, Jarett, Jessica K., Geller-McGrath, David E., Sieber, Christian M. K., Emerson, Joanne B., Anantharaman, Karthik, Thomas, Brian C., Malmstrom, Rex R., Stieglmeier, Michaela, Klingl, Andreas, Woyke, Tanja, Ryan, M. Cathryn, and Banfield, Jillian F. Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. United States: N. p., 2018. Web. doi:10.1038/s41564-017-0098-y.
Probst, Alexander J., Ladd, Bethany, Jarett, Jessica K., Geller-McGrath, David E., Sieber, Christian M. K., Emerson, Joanne B., Anantharaman, Karthik, Thomas, Brian C., Malmstrom, Rex R., Stieglmeier, Michaela, Klingl, Andreas, Woyke, Tanja, Ryan, M. Cathryn, & Banfield, Jillian F. Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. United States. doi:10.1038/s41564-017-0098-y.
Probst, Alexander J., Ladd, Bethany, Jarett, Jessica K., Geller-McGrath, David E., Sieber, Christian M. K., Emerson, Joanne B., Anantharaman, Karthik, Thomas, Brian C., Malmstrom, Rex R., Stieglmeier, Michaela, Klingl, Andreas, Woyke, Tanja, Ryan, M. Cathryn, and Banfield, Jillian F. Mon . "Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface". United States. doi:10.1038/s41564-017-0098-y. https://www.osti.gov/servlets/purl/1436345.
@article{osti_1436345,
title = {Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface},
author = {Probst, Alexander J. and Ladd, Bethany and Jarett, Jessica K. and Geller-McGrath, David E. and Sieber, Christian M. K. and Emerson, Joanne B. and Anantharaman, Karthik and Thomas, Brian C. and Malmstrom, Rex R. and Stieglmeier, Michaela and Klingl, Andreas and Woyke, Tanja and Ryan, M. Cathryn and Banfield, Jillian F.},
abstractNote = {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.},
doi = {10.1038/s41564-017-0098-y},
journal = {Nature Microbiology},
number = ,
volume = 3,
place = {United States},
year = {2018},
month = {1}
}

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