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.

Data availability

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

Version 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.

Metrics

  • 4,466
    views
  • 571
    downloads
  • 38
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.18990

Further reading

    1. Evolutionary Biology
    Case Vincent Miller, Jen A Bright ... Michael Pittman
    Research Article

    Enantiornithines were the dominant birds of the Mesozoic, but understanding of their diet is still tenuous. We introduce new data on the enantiornithine family Bohaiornithidae, famous for their large size and powerfully built teeth and claws. In tandem with previously published data, we comment on the breadth of enantiornithine ecology and potential patterns in which it evolved. Body mass, jaw mechanical advantage, finite element analysis of the jaw, and traditional morphometrics of the claws and skull are compared between bohaiornithids and living birds. We find bohaiornithids to be more ecologically diverse than any other enantiornithine family: Bohaiornis and Parabohaiornis are similar to living plant-eating birds; Longusunguis resembles raptorial carnivores; Zhouornis is similar to both fruit-eating birds and generalist feeders; and Shenqiornis and Sulcavis plausibly ate fish, plants, or a mix of both. We predict the ancestral enantiornithine bird to have been a generalist which ate a wide variety of foods. However, more quantitative data from across the enantiornithine tree is needed to refine this prediction. By the Early Cretaceous, enantiornithine birds had diversified into a variety of ecological niches like crown birds after the K-Pg extinction, adding to the evidence that traits unique to crown birds cannot completely explain their ecological success.

    1. Evolutionary Biology
    Mátyás Paczkó, Eörs Szathmáry, András Szilágyi
    Research Article

    The RNA world hypothesis proposes that during the early evolution of life, primordial genomes of the first self-propagating evolutionary units existed in the form of RNA-like polymers. Autonomous, non-enzymatic, and sustained replication of such information carriers presents a problem, because product formation and hybridization between template and copy strands reduces replication speed. Kinetics of growth is then parabolic with the benefit of entailing competitive coexistence, thereby maintaining diversity. Here, we test the information-maintaining ability of parabolic growth in stochastic multispecies population models under the constraints of constant total population size and chemostat conditions. We find that large population sizes and small differences in the replication rates favor the stable coexistence of the vast majority of replicator species (‘genes’), while the error threshold problem is alleviated relative to exponential amplification. In addition, sequence properties (GC content) and the strength of resource competition mediated by the rate of resource inflow determine the number of coexisting variants, suggesting that fluctuations in building block availability favored repeated cycles of exploration and exploitation. Stochastic parabolic growth could thus have played a pivotal role in preserving viable sequences generated by random abiotic synthesis and providing diverse genetic raw material to the early evolution of functional ribozymes.