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

Author:

Sayavedra Lizbeth1,Kleiner Manuel1,Ponnudurai Ruby2,Wetzel Silke1,Pelletier Eric345,Barbe Valerie3,Satoh Nori6,Shoguchi Eiichi6,Fink Dennis1,Breusing Corinna7,Reusch Thorsten BH7,Rosenstiel Philip8,Schilhabel Markus B8,Becher Dörte910,Schweder Thomas29,Markert Stephanie29,Dubilier Nicole111,Petersen Jillian M1

Affiliation:

1. Max Planck Institute for Marine Microbiology, Bremen, Germany

2. Institute of Pharmacy, Ernst-Moritz-Arndt-University, Greifswald, Germany

3. Genoscope - Centre National de Séquençage, Commissariat à l'énergie atomique et aux énergies alternatives, Evry, France

4. Metabolic Genomics Group, Commissariat à l'énergie atomique et aux énergies alternatives, Evry, France

5. University of Évry-Val d'Essonne, Evry, France

6. Marine Genomics Unit, Okinawa Institute of Science and Technology, Onna, Japan

7. Evolutionary Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Kiel, Germany

8. Institute of Clinical Molecular Biology, Kiel, Germany

9. Institute of Marine Biotechnology, Greifswald, Germany

10. Institute of Microbiology, Ernst-Moritz-Arndt-University, Greifswald, Germany

11. University of Bremen, Bremen, Germany

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.

Funder

Max-Planck-Gesellschaft (MPG)

Gordon and Betty Moore Foundation

European Research Council (ERC)

Deutsche Forschungsgemeinschaft (DFG)

German Academic Exchange Service (DAAD)

Okinawa Institute of Science and Technology Graduate University (OIST)

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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