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...
Gespeichert in:
Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2015-09, Vol.112 (36), p.11300-11305 |
---|---|
Hauptverfasser: | , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | 11305 |
---|---|
container_issue | 36 |
container_start_page | 11300 |
container_title | Proceedings of the National Academy of Sciences - PNAS |
container_volume | 112 |
creator | Klose, Julia Polz, Martin F. Wagner, Michael Schimak, Mario P. Gollner, Sabine Bright, Monika |
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 surfaceswhere they proliferate. Estimating symbiont release from our experiments taken together with wellknown 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. |
doi_str_mv | 10.1073/pnas.1501160112 |
format | Article |
fullrecord | <record><control><sourceid>jstor_cross</sourceid><recordid>TN_cdi_crossref_primary_10_1073_pnas_1501160112</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>26464986</jstor_id><sourcerecordid>26464986</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4822-384726005d2c22452c2d375aec515e3ce78ef78bdbea47f100c3c0bb554acf533</originalsourceid><addsrcrecordid>eNqNkj2P1DAQhi0E4paDmgpkiYYmd-Nvb4OETseHdBINNDSW40xus0riYCeL9t_j1S7LQUVhT-HHj8bzmpCXDK4YGHE9jT5fMQWM6bL4I7JisGaVlmt4TFYA3FRWcnlBnuW8BYC1svCUXHDNrRDSrsj327GJeT_UXRznTDEHPyFt0Dd0s29SnDeYBt_THY4znZcaf8Y0ZDpHimPqwoYWgLYJseq7XTfe0ylOS-_nontOnrS-z_jiVC_Jtw-3X28-VXdfPn6-eX9XBWk5r4SVhmsA1fDAuVRlb4RRHoNiCkVAY7E1tm5q9NK0DCCIAHWtlPShVUJckndH77TUAzahdJp876bUDT7tXfSd-_tk7DbuPu6cVNpqpYvg7UmQ4o8F8-yGLgfsez9iXLJjhhtthFjb_0DL_K3UbF3QN_-g27iksUziQAllpTWmUNdHKqSYc8L23DcDd4jYHSJ2fyIuN14_fO6Z_51pAegJONw86xh3QpciAAry6ohs8xzTA4UsP8dq8QtBBbdf</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1713584877</pqid></control><display><type>article</type><title>Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population</title><source>MEDLINE</source><source>JSTOR Archive Collection A-Z Listing</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><source>Free Full-Text Journals in Chemistry</source><creator>Klose, Julia ; Polz, Martin F. ; Wagner, Michael ; Schimak, Mario P. ; Gollner, Sabine ; Bright, Monika</creator><creatorcontrib>Klose, Julia ; Polz, Martin F. ; Wagner, Michael ; Schimak, Mario P. ; Gollner, Sabine ; Bright, Monika</creatorcontrib><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 surfaceswhere they proliferate. Estimating symbiont release from our experiments taken together with wellknown 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.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1501160112</identifier><identifier>PMID: 26283348</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animal populations ; Animals ; Bacteria ; Bacteria - genetics ; Bacteria - growth & development ; Bacteria - ultrastructure ; Bacterial Load ; Biological Sciences ; Cell Death ; Environmental Microbiology ; Host-Pathogen Interactions ; Hydrothermal Vents - parasitology ; In Situ Hybridization, Fluorescence ; Invertebrates ; Larva - microbiology ; Microscopy, Electron, Transmission ; Mutualism ; Polychaeta - genetics ; Polychaeta - microbiology ; Polychaeta - ultrastructure ; RNA, Ribosomal, 16S - genetics ; Seawater - microbiology ; Siboglinidae ; Symbiosis ; Vestimentifera</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2015-09, Vol.112 (36), p.11300-11305</ispartof><rights>Volumes 1–89 and 106–112, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Sep 8, 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4822-384726005d2c22452c2d375aec515e3ce78ef78bdbea47f100c3c0bb554acf533</citedby><cites>FETCH-LOGICAL-c4822-384726005d2c22452c2d375aec515e3ce78ef78bdbea47f100c3c0bb554acf533</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/112/36.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26464986$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26464986$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26283348$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Klose, Julia</creatorcontrib><creatorcontrib>Polz, Martin F.</creatorcontrib><creatorcontrib>Wagner, Michael</creatorcontrib><creatorcontrib>Schimak, Mario P.</creatorcontrib><creatorcontrib>Gollner, Sabine</creatorcontrib><creatorcontrib>Bright, Monika</creatorcontrib><title>Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><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 surfaceswhere they proliferate. Estimating symbiont release from our experiments taken together with wellknown 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.</description><subject>Animal populations</subject><subject>Animals</subject><subject>Bacteria</subject><subject>Bacteria - genetics</subject><subject>Bacteria - growth & development</subject><subject>Bacteria - ultrastructure</subject><subject>Bacterial Load</subject><subject>Biological Sciences</subject><subject>Cell Death</subject><subject>Environmental Microbiology</subject><subject>Host-Pathogen Interactions</subject><subject>Hydrothermal Vents - parasitology</subject><subject>In Situ Hybridization, Fluorescence</subject><subject>Invertebrates</subject><subject>Larva - microbiology</subject><subject>Microscopy, Electron, Transmission</subject><subject>Mutualism</subject><subject>Polychaeta - genetics</subject><subject>Polychaeta - microbiology</subject><subject>Polychaeta - ultrastructure</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>Seawater - microbiology</subject><subject>Siboglinidae</subject><subject>Symbiosis</subject><subject>Vestimentifera</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkj2P1DAQhi0E4paDmgpkiYYmd-Nvb4OETseHdBINNDSW40xus0riYCeL9t_j1S7LQUVhT-HHj8bzmpCXDK4YGHE9jT5fMQWM6bL4I7JisGaVlmt4TFYA3FRWcnlBnuW8BYC1svCUXHDNrRDSrsj327GJeT_UXRznTDEHPyFt0Dd0s29SnDeYBt_THY4znZcaf8Y0ZDpHimPqwoYWgLYJseq7XTfe0ylOS-_nontOnrS-z_jiVC_Jtw-3X28-VXdfPn6-eX9XBWk5r4SVhmsA1fDAuVRlb4RRHoNiCkVAY7E1tm5q9NK0DCCIAHWtlPShVUJckndH77TUAzahdJp876bUDT7tXfSd-_tk7DbuPu6cVNpqpYvg7UmQ4o8F8-yGLgfsez9iXLJjhhtthFjb_0DL_K3UbF3QN_-g27iksUziQAllpTWmUNdHKqSYc8L23DcDd4jYHSJ2fyIuN14_fO6Z_51pAegJONw86xh3QpciAAry6ohs8xzTA4UsP8dq8QtBBbdf</recordid><startdate>20150908</startdate><enddate>20150908</enddate><creator>Klose, Julia</creator><creator>Polz, Martin F.</creator><creator>Wagner, Michael</creator><creator>Schimak, Mario P.</creator><creator>Gollner, Sabine</creator><creator>Bright, Monika</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20150908</creationdate><title>Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population</title><author>Klose, Julia ; Polz, Martin F. ; Wagner, Michael ; Schimak, Mario P. ; Gollner, Sabine ; Bright, Monika</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4822-384726005d2c22452c2d375aec515e3ce78ef78bdbea47f100c3c0bb554acf533</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animal populations</topic><topic>Animals</topic><topic>Bacteria</topic><topic>Bacteria - genetics</topic><topic>Bacteria - growth & development</topic><topic>Bacteria - ultrastructure</topic><topic>Bacterial Load</topic><topic>Biological Sciences</topic><topic>Cell Death</topic><topic>Environmental Microbiology</topic><topic>Host-Pathogen Interactions</topic><topic>Hydrothermal Vents - parasitology</topic><topic>In Situ Hybridization, Fluorescence</topic><topic>Invertebrates</topic><topic>Larva - microbiology</topic><topic>Microscopy, Electron, Transmission</topic><topic>Mutualism</topic><topic>Polychaeta - genetics</topic><topic>Polychaeta - microbiology</topic><topic>Polychaeta - ultrastructure</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>Seawater - microbiology</topic><topic>Siboglinidae</topic><topic>Symbiosis</topic><topic>Vestimentifera</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Klose, Julia</creatorcontrib><creatorcontrib>Polz, Martin F.</creatorcontrib><creatorcontrib>Wagner, Michael</creatorcontrib><creatorcontrib>Schimak, Mario P.</creatorcontrib><creatorcontrib>Gollner, Sabine</creatorcontrib><creatorcontrib>Bright, Monika</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Klose, Julia</au><au>Polz, Martin F.</au><au>Wagner, Michael</au><au>Schimak, Mario P.</au><au>Gollner, Sabine</au><au>Bright, Monika</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2015-09-08</date><risdate>2015</risdate><volume>112</volume><issue>36</issue><spage>11300</spage><epage>11305</epage><pages>11300-11305</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><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 surfaceswhere they proliferate. Estimating symbiont release from our experiments taken together with wellknown 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.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>26283348</pmid><doi>10.1073/pnas.1501160112</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0027-8424 |
ispartof | Proceedings of the National Academy of Sciences - PNAS, 2015-09, Vol.112 (36), p.11300-11305 |
issn | 0027-8424 1091-6490 |
language | eng |
recordid | cdi_crossref_primary_10_1073_pnas_1501160112 |
source | MEDLINE; JSTOR Archive Collection A-Z Listing; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
subjects | Animal populations Animals Bacteria Bacteria - genetics Bacteria - growth & development Bacteria - ultrastructure Bacterial Load Biological Sciences Cell Death Environmental Microbiology Host-Pathogen Interactions Hydrothermal Vents - parasitology In Situ Hybridization, Fluorescence Invertebrates Larva - microbiology Microscopy, Electron, Transmission Mutualism Polychaeta - genetics Polychaeta - microbiology Polychaeta - ultrastructure RNA, Ribosomal, 16S - genetics Seawater - microbiology Siboglinidae Symbiosis Vestimentifera |
title | Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-27T21%3A41%3A32IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Endosymbionts%20escape%20dead%20hydrothermal%20vent%20tubeworms%20to%20enrich%20the%20free-living%20population&rft.jtitle=Proceedings%20of%20the%20National%20Academy%20of%20Sciences%20-%20PNAS&rft.au=Klose,%20Julia&rft.date=2015-09-08&rft.volume=112&rft.issue=36&rft.spage=11300&rft.epage=11305&rft.pages=11300-11305&rft.issn=0027-8424&rft.eissn=1091-6490&rft_id=info:doi/10.1073/pnas.1501160112&rft_dat=%3Cjstor_cross%3E26464986%3C/jstor_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1713584877&rft_id=info:pmid/26283348&rft_jstor_id=26464986&rfr_iscdi=true |