The dual nature of haemocyanin in the establishment and persistence of the squid–vibrio symbiosis
We identified and sequenced from the squid Euprymna scolopes two isoforms of haemocyanin that share the common structural/physiological characteristics of haemocyanin from a closely related cephalopod, Sepia officinalis, including a pronounced Bohr effect. We examined the potential roles for haemocy...
Gespeichert in:
| Veröffentlicht in: | Proceedings of the Royal Society. B, Biological sciences Biological sciences, 2014-06, Vol.281 (1785), p.20140504-20140504 |
|---|---|
| Hauptverfasser: | , , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | 20140504 |
|---|---|
| container_issue | 1785 |
| container_start_page | 20140504 |
| container_title | Proceedings of the Royal Society. B, Biological sciences |
| container_volume | 281 |
| creator | Kremer, Natacha Schwartzman, Julia Augustin, René Zhou, Lawrence Ruby, Edward G. Hourdez, Stéphane McFall-Ngai, Margaret J. |
| description | We identified and sequenced from the squid Euprymna scolopes two isoforms of haemocyanin that share the common structural/physiological characteristics of haemocyanin from a closely related cephalopod, Sepia officinalis, including a pronounced Bohr effect. We examined the potential roles for haemocyanin in the animal's symbiosis with the luminous bacterium Vibrio fischeri. Our data demonstrate that, as in other cephalopods, the haemocyanin is primarily synthesized in the gills. It transits through the general circulation into other tissues and is exported into crypt spaces that support the bacterial partner, which requires oxygen for its bioluminescence. We showed that the gradient of pH between the circulating haemolymph and the matrix of the crypt spaces in adult squid favours offloading of oxygen from the haemocyanin to the symbionts. Haemocyanin is also localized to the apical surfaces and associated mucus of a juvenile-specific epithelium on which the symbionts gather, and where their specificity is determined during the recruitment into the association. The haemocyanin has an antimicrobial activity, which may be involved in this enrichment of V. fischeri during symbiont initiation. Taken together, these data provide evidence that the haemocyanin plays a role in shaping two stages of the squid–vibrio partnership. |
| doi_str_mv | 10.1098/rspb.2014.0504 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmed_primary_24807261</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1523403695</sourcerecordid><originalsourceid>FETCH-LOGICAL-c576t-c46c2813d52bf1855f779134822d16d45881d3214ccec0ce6c49038b28c90afc3</originalsourceid><addsrcrecordid>eNp1kc1u1DAUhS0EotPCliXKEhYZrv8Se4NUhpYijYBFYWs5jsO4JPHUTkZkxzvwhjwJDikjQEKyZNn-zvG99yD0BMMagxQvQtxXawKYrYEDu4dWmJU4J5Lx-2gFsiC5YJycoNMYbwBAcsEfohPCBJSkwCtkrnc2q0fdZr0exmAz32Q7bTtvJt27PktrSISNg65aF3ed7YdM93W2tyG6ONje_NLMULwdXf3j2_eDq4LzWZy6yvkEPUIPGt1G-_huP0MfLy-uN1f59v2bt5vzbW54WQy5YYUhAtOak6rBgvOmLCWmTBBS46JmXAhcU4KZMdaAsYVhEqioiDASdGPoGXq5-O7HqrO1SaUG3ap9cJ0Ok_Laqb9ferdTn_1BMSCMQpEMni8Gu39kV-dbNd8BJhwklAec2Gd3nwV_O6b5qM5FY9tW99aPUWFOKANaSJ7Q9YKa4GMMtjl6Y1BzimpOUc0pqjnFJHj6ZyNH_HdsCaALEPyUJuqNs8OkbvwY-nT8v22-qObcvh5ddfiiipKWXH0STL273HyA13KrXtGfN2W7Ew</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1523403695</pqid></control><display><type>article</type><title>The dual nature of haemocyanin in the establishment and persistence of the squid–vibrio symbiosis</title><source>MEDLINE</source><source>Jstor Complete Legacy</source><source>PubMed Central</source><creator>Kremer, Natacha ; Schwartzman, Julia ; Augustin, René ; Zhou, Lawrence ; Ruby, Edward G. ; Hourdez, Stéphane ; McFall-Ngai, Margaret J.</creator><creatorcontrib>Kremer, Natacha ; Schwartzman, Julia ; Augustin, René ; Zhou, Lawrence ; Ruby, Edward G. ; Hourdez, Stéphane ; McFall-Ngai, Margaret J.</creatorcontrib><description>We identified and sequenced from the squid Euprymna scolopes two isoforms of haemocyanin that share the common structural/physiological characteristics of haemocyanin from a closely related cephalopod, Sepia officinalis, including a pronounced Bohr effect. We examined the potential roles for haemocyanin in the animal's symbiosis with the luminous bacterium Vibrio fischeri. Our data demonstrate that, as in other cephalopods, the haemocyanin is primarily synthesized in the gills. It transits through the general circulation into other tissues and is exported into crypt spaces that support the bacterial partner, which requires oxygen for its bioluminescence. We showed that the gradient of pH between the circulating haemolymph and the matrix of the crypt spaces in adult squid favours offloading of oxygen from the haemocyanin to the symbionts. Haemocyanin is also localized to the apical surfaces and associated mucus of a juvenile-specific epithelium on which the symbionts gather, and where their specificity is determined during the recruitment into the association. The haemocyanin has an antimicrobial activity, which may be involved in this enrichment of V. fischeri during symbiont initiation. Taken together, these data provide evidence that the haemocyanin plays a role in shaping two stages of the squid–vibrio partnership.</description><identifier>ISSN: 0962-8452</identifier><identifier>EISSN: 1471-2945</identifier><identifier>EISSN: 1471-2954</identifier><identifier>DOI: 10.1098/rspb.2014.0504</identifier><identifier>PMID: 24807261</identifier><language>eng</language><publisher>England: The Royal Society</publisher><subject>Aliivibrio fischeri - genetics ; Aliivibrio fischeri - physiology ; Amino Acid Sequence ; Animals ; Decapodiformes - microbiology ; Decapodiformes - physiology ; Environmental Sciences ; Haemocyanin ; Hawaii ; Hemocyanins - chemistry ; Hemocyanins - genetics ; Hemocyanins - metabolism ; Host–symbiont Interaction ; Immunohistochemistry ; Life Sciences ; Molecular Sequence Data ; Oxygen Provision ; Phylogeny ; Protein Isoforms - chemistry ; Protein Isoforms - genetics ; Protein Isoforms - metabolism ; Reverse Transcriptase Polymerase Chain Reaction ; Sequence Alignment ; Specificity ; Symbiosis</subject><ispartof>Proceedings of the Royal Society. B, Biological sciences, 2014-06, Vol.281 (1785), p.20140504-20140504</ispartof><rights>2014 The Author(s) Published by the Royal Society. All rights reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2014 The Author(s) Published by the Royal Society. All rights reserved. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c576t-c46c2813d52bf1855f779134822d16d45881d3214ccec0ce6c49038b28c90afc3</citedby><cites>FETCH-LOGICAL-c576t-c46c2813d52bf1855f779134822d16d45881d3214ccec0ce6c49038b28c90afc3</cites><orcidid>0000-0001-5678-9416 ; 0000-0001-6418-3887</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4024306/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4024306/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,724,777,781,882,27905,27906,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24807261$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01250907$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Kremer, Natacha</creatorcontrib><creatorcontrib>Schwartzman, Julia</creatorcontrib><creatorcontrib>Augustin, René</creatorcontrib><creatorcontrib>Zhou, Lawrence</creatorcontrib><creatorcontrib>Ruby, Edward G.</creatorcontrib><creatorcontrib>Hourdez, Stéphane</creatorcontrib><creatorcontrib>McFall-Ngai, Margaret J.</creatorcontrib><title>The dual nature of haemocyanin in the establishment and persistence of the squid–vibrio symbiosis</title><title>Proceedings of the Royal Society. B, Biological sciences</title><addtitle>Proc. R. Soc. B</addtitle><addtitle>Proc. R. Soc. B</addtitle><description>We identified and sequenced from the squid Euprymna scolopes two isoforms of haemocyanin that share the common structural/physiological characteristics of haemocyanin from a closely related cephalopod, Sepia officinalis, including a pronounced Bohr effect. We examined the potential roles for haemocyanin in the animal's symbiosis with the luminous bacterium Vibrio fischeri. Our data demonstrate that, as in other cephalopods, the haemocyanin is primarily synthesized in the gills. It transits through the general circulation into other tissues and is exported into crypt spaces that support the bacterial partner, which requires oxygen for its bioluminescence. We showed that the gradient of pH between the circulating haemolymph and the matrix of the crypt spaces in adult squid favours offloading of oxygen from the haemocyanin to the symbionts. Haemocyanin is also localized to the apical surfaces and associated mucus of a juvenile-specific epithelium on which the symbionts gather, and where their specificity is determined during the recruitment into the association. The haemocyanin has an antimicrobial activity, which may be involved in this enrichment of V. fischeri during symbiont initiation. Taken together, these data provide evidence that the haemocyanin plays a role in shaping two stages of the squid–vibrio partnership.</description><subject>Aliivibrio fischeri - genetics</subject><subject>Aliivibrio fischeri - physiology</subject><subject>Amino Acid Sequence</subject><subject>Animals</subject><subject>Decapodiformes - microbiology</subject><subject>Decapodiformes - physiology</subject><subject>Environmental Sciences</subject><subject>Haemocyanin</subject><subject>Hawaii</subject><subject>Hemocyanins - chemistry</subject><subject>Hemocyanins - genetics</subject><subject>Hemocyanins - metabolism</subject><subject>Host–symbiont Interaction</subject><subject>Immunohistochemistry</subject><subject>Life Sciences</subject><subject>Molecular Sequence Data</subject><subject>Oxygen Provision</subject><subject>Phylogeny</subject><subject>Protein Isoforms - chemistry</subject><subject>Protein Isoforms - genetics</subject><subject>Protein Isoforms - metabolism</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Sequence Alignment</subject><subject>Specificity</subject><subject>Symbiosis</subject><issn>0962-8452</issn><issn>1471-2945</issn><issn>1471-2954</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kc1u1DAUhS0EotPCliXKEhYZrv8Se4NUhpYijYBFYWs5jsO4JPHUTkZkxzvwhjwJDikjQEKyZNn-zvG99yD0BMMagxQvQtxXawKYrYEDu4dWmJU4J5Lx-2gFsiC5YJycoNMYbwBAcsEfohPCBJSkwCtkrnc2q0fdZr0exmAz32Q7bTtvJt27PktrSISNg65aF3ed7YdM93W2tyG6ONje_NLMULwdXf3j2_eDq4LzWZy6yvkEPUIPGt1G-_huP0MfLy-uN1f59v2bt5vzbW54WQy5YYUhAtOak6rBgvOmLCWmTBBS46JmXAhcU4KZMdaAsYVhEqioiDASdGPoGXq5-O7HqrO1SaUG3ap9cJ0Ok_Laqb9ferdTn_1BMSCMQpEMni8Gu39kV-dbNd8BJhwklAec2Gd3nwV_O6b5qM5FY9tW99aPUWFOKANaSJ7Q9YKa4GMMtjl6Y1BzimpOUc0pqjnFJHj6ZyNH_HdsCaALEPyUJuqNs8OkbvwY-nT8v22-qObcvh5ddfiiipKWXH0STL273HyA13KrXtGfN2W7Ew</recordid><startdate>20140622</startdate><enddate>20140622</enddate><creator>Kremer, Natacha</creator><creator>Schwartzman, Julia</creator><creator>Augustin, René</creator><creator>Zhou, Lawrence</creator><creator>Ruby, Edward G.</creator><creator>Hourdez, Stéphane</creator><creator>McFall-Ngai, Margaret J.</creator><general>The Royal Society</general><general>Royal Society, The</general><scope>BSCLL</scope><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>7X8</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5678-9416</orcidid><orcidid>https://orcid.org/0000-0001-6418-3887</orcidid></search><sort><creationdate>20140622</creationdate><title>The dual nature of haemocyanin in the establishment and persistence of the squid–vibrio symbiosis</title><author>Kremer, Natacha ; Schwartzman, Julia ; Augustin, René ; Zhou, Lawrence ; Ruby, Edward G. ; Hourdez, Stéphane ; McFall-Ngai, Margaret J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c576t-c46c2813d52bf1855f779134822d16d45881d3214ccec0ce6c49038b28c90afc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Aliivibrio fischeri - genetics</topic><topic>Aliivibrio fischeri - physiology</topic><topic>Amino Acid Sequence</topic><topic>Animals</topic><topic>Decapodiformes - microbiology</topic><topic>Decapodiformes - physiology</topic><topic>Environmental Sciences</topic><topic>Haemocyanin</topic><topic>Hawaii</topic><topic>Hemocyanins - chemistry</topic><topic>Hemocyanins - genetics</topic><topic>Hemocyanins - metabolism</topic><topic>Host–symbiont Interaction</topic><topic>Immunohistochemistry</topic><topic>Life Sciences</topic><topic>Molecular Sequence Data</topic><topic>Oxygen Provision</topic><topic>Phylogeny</topic><topic>Protein Isoforms - chemistry</topic><topic>Protein Isoforms - genetics</topic><topic>Protein Isoforms - metabolism</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>Sequence Alignment</topic><topic>Specificity</topic><topic>Symbiosis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kremer, Natacha</creatorcontrib><creatorcontrib>Schwartzman, Julia</creatorcontrib><creatorcontrib>Augustin, René</creatorcontrib><creatorcontrib>Zhou, Lawrence</creatorcontrib><creatorcontrib>Ruby, Edward G.</creatorcontrib><creatorcontrib>Hourdez, Stéphane</creatorcontrib><creatorcontrib>McFall-Ngai, Margaret J.</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the Royal Society. B, Biological sciences</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kremer, Natacha</au><au>Schwartzman, Julia</au><au>Augustin, René</au><au>Zhou, Lawrence</au><au>Ruby, Edward G.</au><au>Hourdez, Stéphane</au><au>McFall-Ngai, Margaret J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The dual nature of haemocyanin in the establishment and persistence of the squid–vibrio symbiosis</atitle><jtitle>Proceedings of the Royal Society. B, Biological sciences</jtitle><stitle>Proc. R. Soc. B</stitle><addtitle>Proc. R. Soc. B</addtitle><date>2014-06-22</date><risdate>2014</risdate><volume>281</volume><issue>1785</issue><spage>20140504</spage><epage>20140504</epage><pages>20140504-20140504</pages><issn>0962-8452</issn><eissn>1471-2945</eissn><eissn>1471-2954</eissn><abstract>We identified and sequenced from the squid Euprymna scolopes two isoforms of haemocyanin that share the common structural/physiological characteristics of haemocyanin from a closely related cephalopod, Sepia officinalis, including a pronounced Bohr effect. We examined the potential roles for haemocyanin in the animal's symbiosis with the luminous bacterium Vibrio fischeri. Our data demonstrate that, as in other cephalopods, the haemocyanin is primarily synthesized in the gills. It transits through the general circulation into other tissues and is exported into crypt spaces that support the bacterial partner, which requires oxygen for its bioluminescence. We showed that the gradient of pH between the circulating haemolymph and the matrix of the crypt spaces in adult squid favours offloading of oxygen from the haemocyanin to the symbionts. Haemocyanin is also localized to the apical surfaces and associated mucus of a juvenile-specific epithelium on which the symbionts gather, and where their specificity is determined during the recruitment into the association. The haemocyanin has an antimicrobial activity, which may be involved in this enrichment of V. fischeri during symbiont initiation. Taken together, these data provide evidence that the haemocyanin plays a role in shaping two stages of the squid–vibrio partnership.</abstract><cop>England</cop><pub>The Royal Society</pub><pmid>24807261</pmid><doi>10.1098/rspb.2014.0504</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-5678-9416</orcidid><orcidid>https://orcid.org/0000-0001-6418-3887</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0962-8452 |
| ispartof | Proceedings of the Royal Society. B, Biological sciences, 2014-06, Vol.281 (1785), p.20140504-20140504 |
| issn | 0962-8452 1471-2945 1471-2954 |
| language | eng |
| recordid | cdi_pubmed_primary_24807261 |
| source | MEDLINE; Jstor Complete Legacy; PubMed Central |
| subjects | Aliivibrio fischeri - genetics Aliivibrio fischeri - physiology Amino Acid Sequence Animals Decapodiformes - microbiology Decapodiformes - physiology Environmental Sciences Haemocyanin Hawaii Hemocyanins - chemistry Hemocyanins - genetics Hemocyanins - metabolism Host–symbiont Interaction Immunohistochemistry Life Sciences Molecular Sequence Data Oxygen Provision Phylogeny Protein Isoforms - chemistry Protein Isoforms - genetics Protein Isoforms - metabolism Reverse Transcriptase Polymerase Chain Reaction Sequence Alignment Specificity Symbiosis |
| title | The dual nature of haemocyanin in the establishment and persistence of the squid–vibrio symbiosis |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-18T07%3A31%3A16IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20dual%20nature%20of%20haemocyanin%20in%20the%20establishment%20and%20persistence%20of%20the%20squid%E2%80%93vibrio%20symbiosis&rft.jtitle=Proceedings%20of%20the%20Royal%20Society.%20B,%20Biological%20sciences&rft.au=Kremer,%20Natacha&rft.date=2014-06-22&rft.volume=281&rft.issue=1785&rft.spage=20140504&rft.epage=20140504&rft.pages=20140504-20140504&rft.issn=0962-8452&rft.eissn=1471-2945&rft_id=info:doi/10.1098/rspb.2014.0504&rft_dat=%3Cproquest_pubme%3E1523403695%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1523403695&rft_id=info:pmid/24807261&rfr_iscdi=true |