Global biogeography of chemosynthetic symbionts reveals both localized and globally distributed symbiont groups

Jay T Osvatic, Laetitia G E Wilkins, Lukas Leibrecht, Matthieu Leray, Sarah Zauner, Julia Polzin, Yolanda Camacho, Olivier Gros, Jan A van Gils, Jonathan A Eisen, Jillian M Petersen (Corresponding author), Benedict Yuen (Corresponding author)

Publications: Contribution to journalArticlePeer Reviewed

Abstract

In the ocean, most hosts acquire their symbionts from the environment. Due to the immense spatial scales involved, our understanding of the biogeography of hosts and symbionts in marine systems is patchy, although this knowledge is essential for understanding fundamental aspects of symbiosis such as host-symbiont specificity and evolution. Lucinidae is the most species-rich and widely distributed family of marine bivalves hosting autotrophic bacterial endosymbionts. Previous molecular surveys identified location-specific symbiont types that "promiscuously" form associations with multiple divergent cooccurring host species. This flexibility of host-microbe pairings is thought to underpin their global success, as it allows hosts to form associations with locally adapted symbionts. We used metagenomics to investigate the biodiversity, functional variability, and genetic exchange among the endosymbionts of 12 lucinid host species from across the globe. We report a cosmopolitan symbiont species, Candidatus Thiodiazotropha taylori, associated with multiple lucinid host species. Ca. T. taylori has achieved more success at dispersal and establishing symbioses with lucinids than any other symbiont described thus far. This discovery challenges our understanding of symbiont dispersal and location-specific colonization and suggests both symbiont and host flexibility underpin the ecological and evolutionary success of the lucinid symbiosis.
Original languageEnglish
Article numbere2104378118
Number of pages10
JournalProceedings of the National Academy of Sciences of the United States of America
Volume118
Issue number29
DOIs
Publication statusPublished - 20 Jul 2021

Funding

ACKNOWLEDGMENTS. We thank Gustav Paulay (FLMNH, Gainesville, FL), Amanda Bemis, and John Taylor (NHM, London) for providing preserved samples. John Taylor also provided high-resolution images of lucinid clams for Fig. 2. We thank Liz Hambleton (University of Vienna), Miriam Weber, Christian Lott, Boris Unger, Doroth\u00E9e Makarow, Natalie Elisabeth (University of California, Berkeley), Diana Chin, Tim Oortwijn, and Arthur Curry for providing fresh samples. We also thank Thalassa for 300 million y of sheltering lucinids. We are grateful to Stephanie Markert for providing access to the proteomics data, Ipek Yamin Meric and Nora Grossschmidt for helping with DNA extractions, Marina DeLe\u00F3n for help with fieldwork and travels in Costa Rica, Cassandra Ettinger for early discussions of the study, and Guillaume Jospin for support with the bio-informatic analyses. We thank Xavier Didelot for discussions on the recombination analysis. L.G.E.W. was supported by Grant GMBF5603 from the Gordon and Betty Moore Foundation (J.A.E. was Principal Investigator on the same grant). The work was also supported by the European Research Council Starting Grant EvoLucin and a Vienna Research Grant for Young Investigators from the Vienna Science and Technology Fund (WWTF, VRG14\u2013021) and the Austrian Academy of Sciences. Sequencing was carried out at the DNA Technologies and Expression Analysis Cores at the University of California, Davis Genome Center (supported by NIH Shared Instrumentation Grant 1S10OD010786-01), the Biomedical Sequencing Facility at CeMM (https://www.biomedical-sequencing. org/) in Vienna, Austria, and at the Joint Microbiome Facility (JMF) of the Medical University of Vienna and the University of Vienna (project ID 1911-1). Thanks to Petra Pjevac and Gudrun Kohl for sample processing at JMF. The gill embedding was performed by the Histopathology Facility at Vienna BioCenter Core Facilities, a member of the Vienna BioCenter, Austria.

Austrian Fields of Science 2012

  • 106026 Ecosystem research

Keywords

  • symbiosis
  • biogeography
  • recombination
  • RECOMBINATION
  • SPECIFICITY
  • RIFTIA-PACHYPTILA
  • FLEXIBILITY
  • METAGENOMES
  • GILL ENDOSYMBIONT
  • SEQUENCE
  • CODAKIA-ORBICULARIS BIVALVIA
  • DIVERSITY
  • TOOL

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