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Early innate immune responses in European sea bass (Dicentrarchus labrax L.) following Tenacibaculum maritimum infection

IntroductionThe marine aquaculture industry has been witnessing a worldwide emergence of tenacibaculosis, a poorly understood bacterial disease caused by Tenacibaculum maritimum that affects commercially important fish. So far, knowledge on the T. maritimum virulence mechanisms is scarce and the pat...

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Published in:Frontiers in immunology 2023-09, Vol.14, p.1254677-1254677
Main Authors: Ferreira, Inês A., Peixoto, Diogo, Losada, Ana Paula, Quiroga, María Isabel, Vale, Ana do, Costas, Benjamín
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container_title Frontiers in immunology
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Peixoto, Diogo
Losada, Ana Paula
Quiroga, María Isabel
Vale, Ana do
Costas, Benjamín
description IntroductionThe marine aquaculture industry has been witnessing a worldwide emergence of tenacibaculosis, a poorly understood bacterial disease caused by Tenacibaculum maritimum that affects commercially important fish. So far, knowledge on the T. maritimum virulence mechanisms is scarce and the pathogen-host interaction operating in tenacibaculosis remain to be disclosed. This study aimed at contributing to a better understanding of this disease, by evaluating the early innate immune response triggered in European sea bass (Dicentrarchus labrax) by a bath-challenge with T. maritimum. MethodsGroups of sea bass were bath-challenged with T. maritimum (challenged fish) or mock-challenged. Undisturbed fish were used as controls (time 0). Samples of blood, liver and mucosal organs (skin, gills and posterior-intestine) were collected at 0 h (control) and at 6, 24, 48 and 72 h post-challenge (n=12). Mucosal organs were used for analyzing the expression of immune-related genes by RT-qPCR, as well as blood samples for assessing haematological and innate humoral parameters and liver for oxidative stress assessment. ResultsAn increased expression of il-1β, il8, mmp9 and hamp1 was detected in all mucosal organs of infected fish when compared with control and mock-challenged fish, suggesting a pro-inflammatory response against T. maritimum transversal to all organs. The faster induction of these pro-inflammatory genes was observed in the gills. Regarding the systemic response, challenged fish presented neutrophilia, monocytosis, signs of anemia, and a decrease of bactericidal and lysozyme activities in plasma. Almost no variations were observed regarding hepatic oxidative stress. Discussion/ConclusionsThe present study suggests that T. maritimum induces a local innate immune response upon bath infection not only in the skin of European sea bass, but also in the gills and posterior-intestine, likely triggered by the T. maritimum's capacity to adhere, colonize and damage these organs that can function as entry ways to bacteria, leading ultimately to the seen host's systemic response.
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So far, knowledge on the T. maritimum virulence mechanisms is scarce and the pathogen-host interaction operating in tenacibaculosis remain to be disclosed. This study aimed at contributing to a better understanding of this disease, by evaluating the early innate immune response triggered in European sea bass (Dicentrarchus labrax) by a bath-challenge with T. maritimum. MethodsGroups of sea bass were bath-challenged with T. maritimum (challenged fish) or mock-challenged. Undisturbed fish were used as controls (time 0). Samples of blood, liver and mucosal organs (skin, gills and posterior-intestine) were collected at 0 h (control) and at 6, 24, 48 and 72 h post-challenge (n=12). Mucosal organs were used for analyzing the expression of immune-related genes by RT-qPCR, as well as blood samples for assessing haematological and innate humoral parameters and liver for oxidative stress assessment. ResultsAn increased expression of il-1β, il8, mmp9 and hamp1 was detected in all mucosal organs of infected fish when compared with control and mock-challenged fish, suggesting a pro-inflammatory response against T. maritimum transversal to all organs. The faster induction of these pro-inflammatory genes was observed in the gills. Regarding the systemic response, challenged fish presented neutrophilia, monocytosis, signs of anemia, and a decrease of bactericidal and lysozyme activities in plasma. Almost no variations were observed regarding hepatic oxidative stress. Discussion/ConclusionsThe present study suggests that T. maritimum induces a local innate immune response upon bath infection not only in the skin of European sea bass, but also in the gills and posterior-intestine, likely triggered by the T. maritimum's capacity to adhere, colonize and damage these organs that can function as entry ways to bacteria, leading ultimately to the seen host's systemic response.</description><identifier>ISSN: 1664-3224</identifier><identifier>EISSN: 1664-3224</identifier><identifier>DOI: 10.3389/fimmu.2023.1254677</identifier><language>eng</language><publisher>Frontiers Media S.A</publisher><subject>aquaculture ; bacterial infection ; Immunology ; innate immunity ; mucosal immunity ; tenacibaculosis</subject><ispartof>Frontiers in immunology, 2023-09, Vol.14, p.1254677-1254677</ispartof><rights>Copyright © 2023 Ferreira, Peixoto, Losada, Quiroga, Vale and Costas 2023 Ferreira, Peixoto, Losada, Quiroga, Vale and Costas</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c446t-d141926805d5f5309de404cef6e8b57b6fa33c4214fe95ed46d2b8df82f8a05a3</citedby><cites>FETCH-LOGICAL-c446t-d141926805d5f5309de404cef6e8b57b6fa33c4214fe95ed46d2b8df82f8a05a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10507263/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10507263/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids></links><search><creatorcontrib>Ferreira, Inês A.</creatorcontrib><creatorcontrib>Peixoto, Diogo</creatorcontrib><creatorcontrib>Losada, Ana Paula</creatorcontrib><creatorcontrib>Quiroga, María Isabel</creatorcontrib><creatorcontrib>Vale, Ana do</creatorcontrib><creatorcontrib>Costas, Benjamín</creatorcontrib><title>Early innate immune responses in European sea bass (Dicentrarchus labrax L.) following Tenacibaculum maritimum infection</title><title>Frontiers in immunology</title><description>IntroductionThe marine aquaculture industry has been witnessing a worldwide emergence of tenacibaculosis, a poorly understood bacterial disease caused by Tenacibaculum maritimum that affects commercially important fish. So far, knowledge on the T. maritimum virulence mechanisms is scarce and the pathogen-host interaction operating in tenacibaculosis remain to be disclosed. This study aimed at contributing to a better understanding of this disease, by evaluating the early innate immune response triggered in European sea bass (Dicentrarchus labrax) by a bath-challenge with T. maritimum. MethodsGroups of sea bass were bath-challenged with T. maritimum (challenged fish) or mock-challenged. Undisturbed fish were used as controls (time 0). Samples of blood, liver and mucosal organs (skin, gills and posterior-intestine) were collected at 0 h (control) and at 6, 24, 48 and 72 h post-challenge (n=12). Mucosal organs were used for analyzing the expression of immune-related genes by RT-qPCR, as well as blood samples for assessing haematological and innate humoral parameters and liver for oxidative stress assessment. ResultsAn increased expression of il-1β, il8, mmp9 and hamp1 was detected in all mucosal organs of infected fish when compared with control and mock-challenged fish, suggesting a pro-inflammatory response against T. maritimum transversal to all organs. The faster induction of these pro-inflammatory genes was observed in the gills. Regarding the systemic response, challenged fish presented neutrophilia, monocytosis, signs of anemia, and a decrease of bactericidal and lysozyme activities in plasma. Almost no variations were observed regarding hepatic oxidative stress. Discussion/ConclusionsThe present study suggests that T. maritimum induces a local innate immune response upon bath infection not only in the skin of European sea bass, but also in the gills and posterior-intestine, likely triggered by the T. maritimum's capacity to adhere, colonize and damage these organs that can function as entry ways to bacteria, leading ultimately to the seen host's systemic response.</description><subject>aquaculture</subject><subject>bacterial infection</subject><subject>Immunology</subject><subject>innate immunity</subject><subject>mucosal immunity</subject><subject>tenacibaculosis</subject><issn>1664-3224</issn><issn>1664-3224</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNpVkU1vFDEMhkeISlSlf6CnHMtht_mezAmhspRKK3Ep5ygfzjZVJlmSGWj_PbPdFaK-2HptPbb8dt0VwWvG1HAT4jjOa4opWxMquOz7d905kZKvGKX8_X_1h-6ytSe8BB8YY-K8e96Yml5QzNlMgA6gDKhC25fcoC062sy17MFk1MAga1pD11-jgzxVU93j3FAytppntF1_QqGkVP7EvEMPkI2L1rg5zSMaTY1THJcq5gBuiiV_7M6CSQ0uT_mi-_lt83D7fbX9cXd_-2W7cpzLaeUJJwOVCgsvgmB48MAxdxAkKCt6K4NhzHFKeIBBgOfSU6t8UDQog4VhF939keuLedL7GpdbXnQxUb8Kpe60qVN0CTQD0QsMwLxlvLdUKWuFJzaowCjjamF9PrL2sx3BH5-Q3kDfdnJ81LvyWxMscE8lWwjXJ0Itv2Zokx5jc5CSyVDmpqmSPRGYDnQZpcdRV0trFcK_PQTrg-_61Xd98F2ffGd_AU_HpOI</recordid><startdate>20230904</startdate><enddate>20230904</enddate><creator>Ferreira, Inês A.</creator><creator>Peixoto, Diogo</creator><creator>Losada, Ana Paula</creator><creator>Quiroga, María Isabel</creator><creator>Vale, Ana do</creator><creator>Costas, Benjamín</creator><general>Frontiers Media S.A</general><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20230904</creationdate><title>Early innate immune responses in European sea bass (Dicentrarchus labrax L.) following Tenacibaculum maritimum infection</title><author>Ferreira, Inês A. ; Peixoto, Diogo ; Losada, Ana Paula ; Quiroga, María Isabel ; Vale, Ana do ; Costas, Benjamín</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c446t-d141926805d5f5309de404cef6e8b57b6fa33c4214fe95ed46d2b8df82f8a05a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>aquaculture</topic><topic>bacterial infection</topic><topic>Immunology</topic><topic>innate immunity</topic><topic>mucosal immunity</topic><topic>tenacibaculosis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ferreira, Inês A.</creatorcontrib><creatorcontrib>Peixoto, Diogo</creatorcontrib><creatorcontrib>Losada, Ana Paula</creatorcontrib><creatorcontrib>Quiroga, María Isabel</creatorcontrib><creatorcontrib>Vale, Ana do</creatorcontrib><creatorcontrib>Costas, Benjamín</creatorcontrib><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Frontiers in immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ferreira, Inês A.</au><au>Peixoto, Diogo</au><au>Losada, Ana Paula</au><au>Quiroga, María Isabel</au><au>Vale, Ana do</au><au>Costas, Benjamín</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Early innate immune responses in European sea bass (Dicentrarchus labrax L.) following Tenacibaculum maritimum infection</atitle><jtitle>Frontiers in immunology</jtitle><date>2023-09-04</date><risdate>2023</risdate><volume>14</volume><spage>1254677</spage><epage>1254677</epage><pages>1254677-1254677</pages><issn>1664-3224</issn><eissn>1664-3224</eissn><abstract>IntroductionThe marine aquaculture industry has been witnessing a worldwide emergence of tenacibaculosis, a poorly understood bacterial disease caused by Tenacibaculum maritimum that affects commercially important fish. So far, knowledge on the T. maritimum virulence mechanisms is scarce and the pathogen-host interaction operating in tenacibaculosis remain to be disclosed. This study aimed at contributing to a better understanding of this disease, by evaluating the early innate immune response triggered in European sea bass (Dicentrarchus labrax) by a bath-challenge with T. maritimum. MethodsGroups of sea bass were bath-challenged with T. maritimum (challenged fish) or mock-challenged. Undisturbed fish were used as controls (time 0). Samples of blood, liver and mucosal organs (skin, gills and posterior-intestine) were collected at 0 h (control) and at 6, 24, 48 and 72 h post-challenge (n=12). Mucosal organs were used for analyzing the expression of immune-related genes by RT-qPCR, as well as blood samples for assessing haematological and innate humoral parameters and liver for oxidative stress assessment. ResultsAn increased expression of il-1β, il8, mmp9 and hamp1 was detected in all mucosal organs of infected fish when compared with control and mock-challenged fish, suggesting a pro-inflammatory response against T. maritimum transversal to all organs. The faster induction of these pro-inflammatory genes was observed in the gills. Regarding the systemic response, challenged fish presented neutrophilia, monocytosis, signs of anemia, and a decrease of bactericidal and lysozyme activities in plasma. Almost no variations were observed regarding hepatic oxidative stress. Discussion/ConclusionsThe present study suggests that T. maritimum induces a local innate immune response upon bath infection not only in the skin of European sea bass, but also in the gills and posterior-intestine, likely triggered by the T. maritimum's capacity to adhere, colonize and damage these organs that can function as entry ways to bacteria, leading ultimately to the seen host's systemic response.</abstract><pub>Frontiers Media S.A</pub><doi>10.3389/fimmu.2023.1254677</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record>
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subjects aquaculture
bacterial infection
Immunology
innate immunity
mucosal immunity
tenacibaculosis
title Early innate immune responses in European sea bass (Dicentrarchus labrax L.) following Tenacibaculum maritimum infection
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