Insight into the evolution of microbial metabolism from the deep-branching bacterium, Thermovibrio ammonificans

  1. Donato Giovannelli  Is a corresponding author
  2. Stefan M Sievert
  3. Michael Hügler
  4. Stephanie Markert
  5. Dörte Becher
  6. Thomas Schweder
  7. Costantino Vetriani  Is a corresponding author
  1. Rutgers University, United States
  2. Woods Hole Oceanographic Institution, United States
  3. DVGW-Technologiezentrum Wasser, Germany
  4. Ernst-Moritz-Arndt-University Greifswald, Germany

Abstract

Anaerobic thermophiles inhabit relic environments that resemble the early Earth. However, the lineage of these modern organisms co-evolved with our planet. Hence, these organisms carry both ancestral and acquired genes and serve as models to reconstruct early metabolism. Based on comparative genomic and proteomic analyses, we identified two distinct groups of genes in Thermovibrio ammonificans: the first codes for enzymes that do not require oxygen and use substrates of geothermal origin; the second appears to be a more recent acquisition, and may reflect adaptations to cope with the rise of oxygen on Earth. We propose that the ancestor of the Aquificae was originally a hydrogen oxidizing, sulfur reducing bacterium that used a hybrid carbon fixation pathway for CO2 fixation. With the gradual rise of oxygen in the atmosphere, more efficient terminal electron acceptors became available and this lineage acquired genes that increased its metabolic flexibility while retaining ancestral metabolic traits.

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The following previously published data sets were used

Article and author information

Author details

  1. Donato Giovannelli

    Institute of Earth, Ocean and Atmospheric Sciences, Rutgers University, New Brunswick, United States
    For correspondence
    giovannelli@marine.rutgers.edu
    Competing interests
    The authors declare that no competing interests exist.
  2. Stefan M Sievert

    Biology Department, Woods Hole Oceanographic Institution, Woods Hole, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Michael Hügler

    DVGW-Technologiezentrum Wasser, Karlsruhe, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2820-0333
  4. Stephanie Markert

    Pharmaceutical Biotechnology, Institute of Pharmacy, Ernst-Moritz-Arndt-University Greifswald, Greifswald, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Dörte Becher

    Institute for Microbiology, Ernst-Moritz-Arndt-University Greifswald, Greifswald, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Thomas Schweder

    Institute for Microbiology, Ernst-Moritz-Arndt-University Greifswald, Greifswald, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Costantino Vetriani

    Institute of Earth, Ocean and Atmospheric Sciences, Rutgers University, New Brunswick, United States
    For correspondence
    vetriani@marine.rutgers.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8141-8438

Funding

National Science Foundation (MCB 04-56676)

  • Costantino Vetriani

National Aeronautics and Space Administration (NNX15AM18G)

  • Costantino Vetriani

National Science Foundation (OCE 03-27353)

  • Costantino Vetriani

National Science Foundation (MCB 08-43678)

  • Costantino Vetriani

National Science Foundation (OCE 09-37371)

  • Costantino Vetriani

National Science Foundation (OCE 11-24141)

  • Costantino Vetriani

National Science Foundation (MCB 15-17567)

  • Donato Giovannelli
  • Costantino Vetriani

National Science Foundation (OCE-1136727)

  • Stefan M Sievert

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Joerg Bohlmann, University of British Columbia, Canada

Publication history

  1. Received: June 21, 2016
  2. Accepted: April 23, 2017
  3. Accepted Manuscript published: April 24, 2017 (version 1)
  4. Version of Record published: May 23, 2017 (version 2)

Copyright

© 2017, Giovannelli et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Donato Giovannelli
  2. Stefan M Sievert
  3. Michael Hügler
  4. Stephanie Markert
  5. Dörte Becher
  6. Thomas Schweder
  7. Costantino Vetriani
(2017)
Insight into the evolution of microbial metabolism from the deep-branching bacterium, Thermovibrio ammonificans
eLife 6:e18990.
https://doi.org/10.7554/eLife.18990

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