Vibrio coralliilyticus infection triggers a behavioural response and perturbs nutritional exchange and tissue integrity in a symbiotic coral
Under homoeostatic conditions, the relationship between the coral Pocillopora damicornis and Vibrio coralliilyticus is commensal. An increase in temperature, or in the abundance of V. coralliilyticus , can turn this association pathogenic, causing tissue lysis, expulsion of the corals’ symbiotic alg...
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description | Under homoeostatic conditions, the relationship between the coral
Pocillopora damicornis
and
Vibrio coralliilyticus
is commensal. An increase in temperature, or in the abundance of
V. coralliilyticus
, can turn this association pathogenic, causing tissue lysis, expulsion of the corals’ symbiotic algae (genus
Symbiodinium
), and eventually coral death. Using a combination of microfluidics, fluorescence microscopy, stable isotopes, electron microscopy and NanoSIMS isotopic imaging, we provide insights into the onset and progression of
V
.
coralliilyticus
infection in the daytime and at night, at the tissue and (sub-)cellular level. The objective of our study was to connect the macro-scale behavioural response of the coral to the micro-scale nutritional interactions that occur between the host and its symbiont. In the daytime, polyps enhanced their mucus production, and actively spewed pathogens.
Vibrio
infection primarily resulted in the formation of tissue lesions in the coenosarc. NanoSIMS analysis revealed infection reduced
13
C-assimilation in
Symbiodinium
, but increased
13
C-assimilation in the host. In the night incubations, no mucus spewing was observed, and a mucus film was formed on the coral surface.
Vibrio
inoculation and infection at night showed reduced
13
C-turnover in
Symbiodinium
, but did not impact host
13
C-turnover. Our results show that both the nutritional interactions that occur between the two symbiotic partners and the behavioural response of the host organism play key roles in determining the progression and severity of host-pathogen interactions. More generally, our approach provides a new means of studying interactions (ranging from behavioural to metabolic scales) between partners involved in complex holobiont systems, under both homoeostatic and pathogenic conditions. |
doi_str_mv | 10.1038/s41396-018-0327-2 |
format | Article |
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Pocillopora damicornis
and
Vibrio coralliilyticus
is commensal. An increase in temperature, or in the abundance of
V. coralliilyticus
, can turn this association pathogenic, causing tissue lysis, expulsion of the corals’ symbiotic algae (genus
Symbiodinium
), and eventually coral death. Using a combination of microfluidics, fluorescence microscopy, stable isotopes, electron microscopy and NanoSIMS isotopic imaging, we provide insights into the onset and progression of
V
.
coralliilyticus
infection in the daytime and at night, at the tissue and (sub-)cellular level. The objective of our study was to connect the macro-scale behavioural response of the coral to the micro-scale nutritional interactions that occur between the host and its symbiont. In the daytime, polyps enhanced their mucus production, and actively spewed pathogens.
Vibrio
infection primarily resulted in the formation of tissue lesions in the coenosarc. NanoSIMS analysis revealed infection reduced
13
C-assimilation in
Symbiodinium
, but increased
13
C-assimilation in the host. In the night incubations, no mucus spewing was observed, and a mucus film was formed on the coral surface.
Vibrio
inoculation and infection at night showed reduced
13
C-turnover in
Symbiodinium
, but did not impact host
13
C-turnover. Our results show that both the nutritional interactions that occur between the two symbiotic partners and the behavioural response of the host organism play key roles in determining the progression and severity of host-pathogen interactions. More generally, our approach provides a new means of studying interactions (ranging from behavioural to metabolic scales) between partners involved in complex holobiont systems, under both homoeostatic and pathogenic conditions.</description><identifier>ISSN: 1751-7362</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/s41396-018-0327-2</identifier><identifier>PMID: 30542077</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/31 ; 13/62 ; 14/19 ; 631/158/855 ; 631/326/171/1878 ; 631/443/319 ; Algae ; Animals ; Anthozoa - anatomy & histology ; Anthozoa - metabolism ; Anthozoa - microbiology ; Anthozoa - physiology ; Assimilation ; Behavior, Animal ; Biomedical and Life Sciences ; Carbon 13 ; Corals ; Daytime ; Dinoflagellida - metabolism ; Ecology ; Electron microscopy ; Evolutionary Biology ; Expulsion ; Fluorescence ; Fluorescence microscopy ; Host-Pathogen Interactions ; Infections ; Inoculation ; Isotopes ; Lesions ; Life Sciences ; Lysis ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Microfluidics ; Microscopy ; Mucus ; Night ; Nutrients ; Pathogens ; Polyps (organisms) ; Stable isotopes ; Symbiodinium ; Symbiosis ; Temperature ; Vibrio ; Vibrio - physiology ; Vibrio coralliilyticus ; Waterborne diseases</subject><ispartof>The ISME Journal, 2019-04, Vol.13 (4), p.989-1003</ispartof><rights>The Author(s) 2018</rights><rights>2018. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c470t-61eb199b504a73024e71b253abd73fcff872a178133c4a05c7a9bd275e3f15a53</citedby><cites>FETCH-LOGICAL-c470t-61eb199b504a73024e71b253abd73fcff872a178133c4a05c7a9bd275e3f15a53</cites><orcidid>0000-0001-9059-5869 ; 0000-0001-6715-4897 ; 0000-0002-8132-8870 ; 0000-0002-7079-0234 ; 0000-0002-3222-9809</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/PMC6462045/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6462045/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30542077$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gibbin, E.</creatorcontrib><creatorcontrib>Gavish, A.</creatorcontrib><creatorcontrib>Krueger, T.</creatorcontrib><creatorcontrib>Kramarsky-Winter, E.</creatorcontrib><creatorcontrib>Shapiro, O.</creatorcontrib><creatorcontrib>Guiet, R.</creatorcontrib><creatorcontrib>Jensen, L.</creatorcontrib><creatorcontrib>Vardi, A.</creatorcontrib><creatorcontrib>Meibom, A.</creatorcontrib><title>Vibrio coralliilyticus infection triggers a behavioural response and perturbs nutritional exchange and tissue integrity in a symbiotic coral</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>Under homoeostatic conditions, the relationship between the coral
Pocillopora damicornis
and
Vibrio coralliilyticus
is commensal. An increase in temperature, or in the abundance of
V. coralliilyticus
, can turn this association pathogenic, causing tissue lysis, expulsion of the corals’ symbiotic algae (genus
Symbiodinium
), and eventually coral death. Using a combination of microfluidics, fluorescence microscopy, stable isotopes, electron microscopy and NanoSIMS isotopic imaging, we provide insights into the onset and progression of
V
.
coralliilyticus
infection in the daytime and at night, at the tissue and (sub-)cellular level. The objective of our study was to connect the macro-scale behavioural response of the coral to the micro-scale nutritional interactions that occur between the host and its symbiont. In the daytime, polyps enhanced their mucus production, and actively spewed pathogens.
Vibrio
infection primarily resulted in the formation of tissue lesions in the coenosarc. NanoSIMS analysis revealed infection reduced
13
C-assimilation in
Symbiodinium
, but increased
13
C-assimilation in the host. In the night incubations, no mucus spewing was observed, and a mucus film was formed on the coral surface.
Vibrio
inoculation and infection at night showed reduced
13
C-turnover in
Symbiodinium
, but did not impact host
13
C-turnover. Our results show that both the nutritional interactions that occur between the two symbiotic partners and the behavioural response of the host organism play key roles in determining the progression and severity of host-pathogen interactions. More generally, our approach provides a new means of studying interactions (ranging from behavioural to metabolic scales) between partners involved in complex holobiont systems, under both homoeostatic and pathogenic conditions.</description><subject>13/31</subject><subject>13/62</subject><subject>14/19</subject><subject>631/158/855</subject><subject>631/326/171/1878</subject><subject>631/443/319</subject><subject>Algae</subject><subject>Animals</subject><subject>Anthozoa - anatomy & histology</subject><subject>Anthozoa - metabolism</subject><subject>Anthozoa - microbiology</subject><subject>Anthozoa - physiology</subject><subject>Assimilation</subject><subject>Behavior, Animal</subject><subject>Biomedical and Life Sciences</subject><subject>Carbon 13</subject><subject>Corals</subject><subject>Daytime</subject><subject>Dinoflagellida - metabolism</subject><subject>Ecology</subject><subject>Electron microscopy</subject><subject>Evolutionary Biology</subject><subject>Expulsion</subject><subject>Fluorescence</subject><subject>Fluorescence microscopy</subject><subject>Host-Pathogen Interactions</subject><subject>Infections</subject><subject>Inoculation</subject><subject>Isotopes</subject><subject>Lesions</subject><subject>Life Sciences</subject><subject>Lysis</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Microfluidics</subject><subject>Microscopy</subject><subject>Mucus</subject><subject>Night</subject><subject>Nutrients</subject><subject>Pathogens</subject><subject>Polyps (organisms)</subject><subject>Stable isotopes</subject><subject>Symbiodinium</subject><subject>Symbiosis</subject><subject>Temperature</subject><subject>Vibrio</subject><subject>Vibrio - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The ISME Journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gibbin, E.</au><au>Gavish, A.</au><au>Krueger, T.</au><au>Kramarsky-Winter, E.</au><au>Shapiro, O.</au><au>Guiet, R.</au><au>Jensen, L.</au><au>Vardi, A.</au><au>Meibom, A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Vibrio coralliilyticus infection triggers a behavioural response and perturbs nutritional exchange and tissue integrity in a symbiotic coral</atitle><jtitle>The ISME Journal</jtitle><stitle>ISME J</stitle><addtitle>ISME J</addtitle><date>2019-04-01</date><risdate>2019</risdate><volume>13</volume><issue>4</issue><spage>989</spage><epage>1003</epage><pages>989-1003</pages><issn>1751-7362</issn><eissn>1751-7370</eissn><abstract>Under homoeostatic conditions, the relationship between the coral
Pocillopora damicornis
and
Vibrio coralliilyticus
is commensal. An increase in temperature, or in the abundance of
V. coralliilyticus
, can turn this association pathogenic, causing tissue lysis, expulsion of the corals’ symbiotic algae (genus
Symbiodinium
), and eventually coral death. Using a combination of microfluidics, fluorescence microscopy, stable isotopes, electron microscopy and NanoSIMS isotopic imaging, we provide insights into the onset and progression of
V
.
coralliilyticus
infection in the daytime and at night, at the tissue and (sub-)cellular level. The objective of our study was to connect the macro-scale behavioural response of the coral to the micro-scale nutritional interactions that occur between the host and its symbiont. In the daytime, polyps enhanced their mucus production, and actively spewed pathogens.
Vibrio
infection primarily resulted in the formation of tissue lesions in the coenosarc. NanoSIMS analysis revealed infection reduced
13
C-assimilation in
Symbiodinium
, but increased
13
C-assimilation in the host. In the night incubations, no mucus spewing was observed, and a mucus film was formed on the coral surface.
Vibrio
inoculation and infection at night showed reduced
13
C-turnover in
Symbiodinium
, but did not impact host
13
C-turnover. Our results show that both the nutritional interactions that occur between the two symbiotic partners and the behavioural response of the host organism play key roles in determining the progression and severity of host-pathogen interactions. More generally, our approach provides a new means of studying interactions (ranging from behavioural to metabolic scales) between partners involved in complex holobiont systems, under both homoeostatic and pathogenic conditions.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>30542077</pmid><doi>10.1038/s41396-018-0327-2</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-9059-5869</orcidid><orcidid>https://orcid.org/0000-0001-6715-4897</orcidid><orcidid>https://orcid.org/0000-0002-8132-8870</orcidid><orcidid>https://orcid.org/0000-0002-7079-0234</orcidid><orcidid>https://orcid.org/0000-0002-3222-9809</orcidid><oa>free_for_read</oa></addata></record> |
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source | Oxford Journals Open Access Collection; MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central |
subjects | 13/31 13/62 14/19 631/158/855 631/326/171/1878 631/443/319 Algae Animals Anthozoa - anatomy & histology Anthozoa - metabolism Anthozoa - microbiology Anthozoa - physiology Assimilation Behavior, Animal Biomedical and Life Sciences Carbon 13 Corals Daytime Dinoflagellida - metabolism Ecology Electron microscopy Evolutionary Biology Expulsion Fluorescence Fluorescence microscopy Host-Pathogen Interactions Infections Inoculation Isotopes Lesions Life Sciences Lysis Microbial Ecology Microbial Genetics and Genomics Microbiology Microfluidics Microscopy Mucus Night Nutrients Pathogens Polyps (organisms) Stable isotopes Symbiodinium Symbiosis Temperature Vibrio Vibrio - physiology Vibrio coralliilyticus Waterborne diseases |
title | Vibrio coralliilyticus infection triggers a behavioural response and perturbs nutritional exchange and tissue integrity in a symbiotic coral |
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