Abundant toxin-related genes in the genomes of beneficial symbionts from deep-sea hydrothermal vent mussels

  1. Lizbeth Sayavedra
  2. Manuel Kleiner
  3. Ruby Ponnudurai
  4. Silke Wetzel
  5. Eric Pelletier
  6. Valerie Barbe
  7. Nori Satoh
  8. Eiichi Shoguchi
  9. Dennis Fink
  10. Corinna Breusing
  11. Thorsten BH Reusch
  12. Philip Rosenstiel
  13. Markus B Schilhabel
  14. Dörte Becher
  15. Thomas Schweder
  16. Stephanie Markert
  17. Nicole Dubilier
  18. Jillian M Petersen  Is a corresponding author
  1. Max Planck Institute for Marine Microbiology, Germany
  2. Ernst-Moritz-Arndt-University, Germany
  3. Commissariat à l'énergie atomique et aux énergies alternatives, France
  4. Okinawa Institute of Science and Technology, Japan
  5. GEOMAR Helmholtz Centre for Ocean Research Kiel, Germany
  6. Institute of Clinical Molecular Biology, Germany
  7. Institute of Marine Biotechnology, Germany
  8. University of Vienna, Austria

Abstract

Bathymodiolus mussels live in symbiosis with intracellular sulfur-oxidizing (SOX) bacteria that provide them with nutrition. We sequenced the SOX symbiont genomes from two Bathymodiolus species. Comparison of these symbiont genomes with those of their closest relatives revealed that the symbionts have undergone genome rearrangements, and up to 35% of their genes may have been acquired by horizontal gene transfer. Many of the genes specific to the symbionts were homologs of virulence genes. We discovered an abundant and diverse array of genes similar to insecticidal toxins of nematode and aphid symbionts, and toxins of pathogens such as Yersinia and Vibrio. Transcriptomics and proteomics revealed that the SOX symbionts express the toxin-related genes (TRGs) in their hosts. We hypothesize that the symbionts use these TRGs in beneficial interactions with their host, including protection against parasites. This would explain why a mutualistic symbiont would contain such a remarkable 'arsenal' of TRGs.

Article and author information

Author details

  1. Lizbeth Sayavedra

    Max Planck Institute for Marine Microbiology, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Manuel Kleiner

    Max Planck Institute for Marine Microbiology, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Ruby Ponnudurai

    Institute of Pharmacy, Ernst-Moritz-Arndt-University, Greifswald, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Silke Wetzel

    Max Planck Institute for Marine Microbiology, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Eric Pelletier

    Genoscope - Centre National de Séquençage, Commissariat à l'énergie atomique et aux énergies alternatives, Evry, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Valerie Barbe

    Genoscope - Centre National de Séquençage, Commissariat à l'énergie atomique et aux énergies alternatives, Evry, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Nori Satoh

    Marine Genomics Unit, Okinawa Institute of Science and Technology, Onna, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Eiichi Shoguchi

    Marine Genomics Unit, Okinawa Institute of Science and Technology, Onna, Japan
    Competing interests
    The authors declare that no competing interests exist.
  9. Dennis Fink

    Max Planck Institute for Marine Microbiology, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Corinna Breusing

    Evolutionary Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
  11. Thorsten BH Reusch

    Evolutionary Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
  12. Philip Rosenstiel

    Institute of Clinical Molecular Biology, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
  13. Markus B Schilhabel

    Institute of Clinical Molecular Biology, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
  14. Dörte Becher

    Institute of Marine Biotechnology, Greifswald, Germany
    Competing interests
    The authors declare that no competing interests exist.
  15. Thomas Schweder

    Institute of Pharmacy, Ernst-Moritz-Arndt-University, Greifswald, Germany
    Competing interests
    The authors declare that no competing interests exist.
  16. Stephanie Markert

    Institute of Pharmacy, Ernst-Moritz-Arndt-University, Greifswald, Germany
    Competing interests
    The authors declare that no competing interests exist.
  17. Nicole Dubilier

    Max Planck Institute for Marine Microbiology, Bremen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  18. Jillian M Petersen

    Department of Microbiology and Ecosystem Science, Division of Microbial Ecology, Research Network Chemistry Meets Microbiology, University of Vienna, Vienna, Austria
    For correspondence
    petersen@microbial-ecology.net
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Axel A Brakhage, Friedrich Schiller University Jena and Hans-Knöll-Institut, Germany

Publication history

  1. Received: April 9, 2015
  2. Accepted: September 14, 2015
  3. Accepted Manuscript published: September 15, 2015 (version 1)
  4. Version of Record published: October 21, 2015 (version 2)

Copyright

© 2015, Sayavedra 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. Lizbeth Sayavedra
  2. Manuel Kleiner
  3. Ruby Ponnudurai
  4. Silke Wetzel
  5. Eric Pelletier
  6. Valerie Barbe
  7. Nori Satoh
  8. Eiichi Shoguchi
  9. Dennis Fink
  10. Corinna Breusing
  11. Thorsten BH Reusch
  12. Philip Rosenstiel
  13. Markus B Schilhabel
  14. Dörte Becher
  15. Thomas Schweder
  16. Stephanie Markert
  17. Nicole Dubilier
  18. Jillian M Petersen
(2015)
Abundant toxin-related genes in the genomes of beneficial symbionts from deep-sea hydrothermal vent mussels
eLife 4:e07966.
https://doi.org/10.7554/eLife.07966

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