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Research Article

Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population

Julia Klose, Martin F. Polz, Michael Wagner, Mario P. Schimak, Sabine Gollner, and Monika Bright
PNAS September 8, 2015 112 (36) 11300-11305; first published August 17, 2015; https://doi.org/10.1073/pnas.1501160112
Julia Klose
aDepartment of Limnology and Bio-Oceanography, University of Vienna, A-1090 Vienna, Austria;
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Martin F. Polz
bParsons Laboratory for Environmental Science and Engineering, Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139;
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Michael Wagner
cDepartment of Microbiology and Ecosystem Science, University of Vienna, A-1090 Vienna, Austria;
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Mario P. Schimak
aDepartment of Limnology and Bio-Oceanography, University of Vienna, A-1090 Vienna, Austria;
dMax Planck Institute for Marine Microbiology, 28359 Bremen, Germany;
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Sabine Gollner
aDepartment of Limnology and Bio-Oceanography, University of Vienna, A-1090 Vienna, Austria;
eDepartment of Ecosystem Studies, Royal Netherlands Institute for Sea Research (NIOZ), 4401 NT Yerseke, The Netherlands;
fGerman Center for Marine Biodiversity Research, Senckenberg am Meer, 26382 Wilhelmshaven, Germany
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Monika Bright
aDepartment of Limnology and Bio-Oceanography, University of Vienna, A-1090 Vienna, Austria;
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  • For correspondence: monika.bright@univie.ac.at
  1. Edited by Margaret J. McFall-Ngai, University of Hawaii at Manoa, Honolulu, HI, and approved July 15, 2015 (received for review January 19, 2015)

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Significance

For horizontally transmitted, facultative symbionts, cycles of infection and escape from the host are crucial for the persistence over host generations. The hydrothermal vent tubeworm Riftia pachyptila is entirely nourished by its thiotrophic endosymbiotic bacteria, which are acquired horizontally in settled larvae; however, release back into the environment has not been demonstrated. We show experimentally that viable symbionts are released upon host death. Moreover, observations of turnover of tubeworm clumps after a volcanic eruption provide evidence for rapid colonization, growth, and death. The observed connectivity of host-associated and free-living symbiont populations helps to explain the stability of this mutualism over ecological and evolutionary timescales.

Abstract

Theory predicts that horizontal acquisition of symbionts by plants and animals must be coupled to release and limited dispersal of symbionts for intergenerational persistence of mutualisms. For deep-sea hydrothermal vent tubeworms (Vestimentifera, Siboglinidae), it has been demonstrated that a few symbiotic bacteria infect aposymbiotic host larvae and grow in a newly formed organ, the trophosome. However, whether viable symbionts can be released to augment environmental populations has been doubtful, because (i) the adult worms lack obvious openings and (ii) the vast majority of symbionts has been regarded as terminally differentiated. Here we show experimentally that symbionts rapidly escape their hosts upon death and recruit to surfaces where they proliferate. Estimating symbiont release from our experiments taken together with well-known tubeworm density ranges, we suggest a few million to 1.5 billion symbionts seeding the environment upon death of a tubeworm clump. In situ observations show that such clumps have rapid turnover, suggesting that release of large numbers of symbionts may ensure effective dispersal to new sites followed by active larval colonization. Moreover, release of symbionts might enable adaptations that evolve within host individuals to spread within host populations and possibly to new environments.

  • symbiosis
  • mutualism stability
  • symbiont seeding
  • tubeworms
  • Vestimentifera

Footnotes

  • ↵1To whom correspondence should be addressed. Email: monika.bright{at}univie.ac.at.
  • Author contributions: M.B. designed research; J.K., M.P.S., S.G., and M.B. performed research; and J.K., M.F.P., M.W., and M.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1501160112/-/DCSupplemental.

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Endosymbionts escape dead tubeworms
Julia Klose, Martin F. Polz, Michael Wagner, Mario P. Schimak, Sabine Gollner, Monika Bright
Proceedings of the National Academy of Sciences Sep 2015, 112 (36) 11300-11305; DOI: 10.1073/pnas.1501160112

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Endosymbionts escape dead tubeworms
Julia Klose, Martin F. Polz, Michael Wagner, Mario P. Schimak, Sabine Gollner, Monika Bright
Proceedings of the National Academy of Sciences Sep 2015, 112 (36) 11300-11305; DOI: 10.1073/pnas.1501160112
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