Edited by Margaret J. McFall-Ngai, University of Hawaii at Manoa, Honolulu, HI, and approved July 15, 2015 (received for review January 19, 2015)
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.
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.
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.
