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

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 s...

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Main Authors: Klose, Julia, Wagner, Michael, Schimak, Mario P., Gollner, Sabine, Bright, Monika, Polz, Martin F
Other Authors: Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Format: Article
Language:en_US
Published: National Academy of Sciences (U.S.) 2016
Online Access:http://hdl.handle.net/1721.1/102104
https://orcid.org/0000-0001-9296-3733
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author Klose, Julia
Wagner, Michael
Schimak, Mario P.
Gollner, Sabine
Bright, Monika
Polz, Martin F
author2 Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
author_facet Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
Klose, Julia
Wagner, Michael
Schimak, Mario P.
Gollner, Sabine
Bright, Monika
Polz, Martin F
author_sort Klose, Julia
collection MIT
description 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.
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spelling mit-1721.1/1021042022-10-02T00:39:06Z Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population Klose, Julia Wagner, Michael Schimak, Mario P. Gollner, Sabine Bright, Monika Polz, Martin F Massachusetts Institute of Technology. Department of Civil and Environmental Engineering Parsons Laboratory for Environmental Science and Engineering (Massachusetts Institute of Technology) Polz, Martin F. 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. 2016-04-04T16:04:54Z 2016-04-04T16:04:54Z 2015-09 2015-01 Article http://purl.org/eprint/type/JournalArticle 0027-8424 1091-6490 http://hdl.handle.net/1721.1/102104 Klose, Julia, Martin F. Polz, Michael Wagner, Mario P. Schimak, Sabine Gollner, and Monika Bright. “Endosymbionts Escape Dead Hydrothermal Vent Tubeworms to Enrich the Free-Living Population.” Proc Natl Acad Sci USA 112, no. 36 (August 17, 2015): 11300–11305. https://orcid.org/0000-0001-9296-3733 en_US http://dx.doi.org/10.1073/pnas.1501160112 Proceedings of the National Academy of Sciences Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf National Academy of Sciences (U.S.) National Academy of Sciences (U.S.)
spellingShingle Klose, Julia
Wagner, Michael
Schimak, Mario P.
Gollner, Sabine
Bright, Monika
Polz, Martin F
Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population
title Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population
title_full Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population
title_fullStr Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population
title_full_unstemmed Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population
title_short Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population
title_sort endosymbionts escape dead hydrothermal vent tubeworms to enrich the free living population
url http://hdl.handle.net/1721.1/102104
https://orcid.org/0000-0001-9296-3733
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