Immune-Challenged Fish Up-Regulate Their Metabolic Scope to Support Locomotion
Identifieur interne : 002807 ( Pmc/Curation ); précédent : 002806; suivant : 002808Immune-Challenged Fish Up-Regulate Their Metabolic Scope to Support Locomotion
Auteurs : Camille Bonneaud [Royaume-Uni, France] ; Robbie S. Wilson [Australie] ; Frank Seebacher [Australie]Source :
- PLoS ONE [ 1932-6203 ] ; 2016.
Abstract
Energy-based trade-offs occur when investment in one fitness-related trait diverts energy away from other traits. The extent to which such trade-offs are shaped by limits on the rate of conversion of energy ingested in food (e.g. carbohydrates) into chemical energy (ATP) by oxidative metabolism rather than by the amount of food ingested in the first place is, however, unclear. Here we tested whether the ATP required for mounting an immune response will lead to a trade-off with ATP available for physical activity in mosquitofish (
Url:
DOI: 10.1371/journal.pone.0166028
PubMed: 27851769
PubMed Central: 5113038
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Immune-Challenged Fish Up-Regulate Their Metabolic Scope to Support Locomotion</title><author><name sortKey="Bonneaud, Camille" sort="Bonneaud, Camille" uniqKey="Bonneaud C" first="Camille" last="Bonneaud">Camille Bonneaud</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Centre for Ecology & Conservation, University of Exeter Penryn Campus, Penryn TR10 9FE, Cornwall, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Centre for Ecology & Conservation, University of Exeter Penryn Campus, Penryn TR10 9FE, Cornwall</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Station d’Ecologie Expérimentale du CNRS, USR 2936, 09200 Moulis, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Station d’Ecologie Expérimentale du CNRS, USR 2936, 09200 Moulis</wicri:regionArea></affiliation></author><author><name sortKey="Wilson, Robbie S" sort="Wilson, Robbie S" uniqKey="Wilson R" first="Robbie S." last="Wilson">Robbie S. Wilson</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>School of Biological Sciences, University of Queensland, Brisbane St Lucia QLD 4072, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>School of Biological Sciences, University of Queensland, Brisbane St Lucia QLD 4072</wicri:regionArea></affiliation></author><author><name sortKey="Seebacher, Frank" sort="Seebacher, Frank" uniqKey="Seebacher F" first="Frank" last="Seebacher">Frank Seebacher</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>School of Biological Sciences, University of Sydney, Sydney NSW 2006, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>School of Biological Sciences, University of Sydney, Sydney NSW 2006</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27851769</idno><idno type="pmc">5113038</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5113038</idno><idno type="RBID">PMC:5113038</idno><idno type="doi">10.1371/journal.pone.0166028</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">002957</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">002957</idno><idno type="wicri:Area/Pmc/Curation">002807</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">002807</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Immune-Challenged Fish Up-Regulate Their Metabolic Scope to Support Locomotion</title><author><name sortKey="Bonneaud, Camille" sort="Bonneaud, Camille" uniqKey="Bonneaud C" first="Camille" last="Bonneaud">Camille Bonneaud</name><affiliation wicri:level="1"><nlm:aff id="aff001"><addr-line>Centre for Ecology & Conservation, University of Exeter Penryn Campus, Penryn TR10 9FE, Cornwall, United Kingdom</addr-line></nlm:aff><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Centre for Ecology & Conservation, University of Exeter Penryn Campus, Penryn TR10 9FE, Cornwall</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Station d’Ecologie Expérimentale du CNRS, USR 2936, 09200 Moulis, France</addr-line></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea>Station d’Ecologie Expérimentale du CNRS, USR 2936, 09200 Moulis</wicri:regionArea></affiliation></author><author><name sortKey="Wilson, Robbie S" sort="Wilson, Robbie S" uniqKey="Wilson R" first="Robbie S." last="Wilson">Robbie S. Wilson</name><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>School of Biological Sciences, University of Queensland, Brisbane St Lucia QLD 4072, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>School of Biological Sciences, University of Queensland, Brisbane St Lucia QLD 4072</wicri:regionArea></affiliation></author><author><name sortKey="Seebacher, Frank" sort="Seebacher, Frank" uniqKey="Seebacher F" first="Frank" last="Seebacher">Frank Seebacher</name><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>School of Biological Sciences, University of Sydney, Sydney NSW 2006, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>School of Biological Sciences, University of Sydney, Sydney NSW 2006</wicri:regionArea></affiliation></author></analytic><series><title level="j">PLoS ONE</title><idno type="eISSN">1932-6203</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Energy-based trade-offs occur when investment in one fitness-related trait diverts energy away from other traits. The extent to which such trade-offs are shaped by limits on the rate of conversion of energy ingested in food (e.g. carbohydrates) into chemical energy (ATP) by oxidative metabolism rather than by the amount of food ingested in the first place is, however, unclear. Here we tested whether the ATP required for mounting an immune response will lead to a trade-off with ATP available for physical activity in mosquitofish (<italic>Gambusia holbrooki</italic>). To this end, we challenged fish either with lipopolysaccharide (LPS) from <italic>E</italic>. <italic>coli</italic> or with Sheep Red Blood Cells (SRBC), and measured oxygen consumption at rest and during swimming at maximum speed 24h, 48h and 7 days post-challenge in order to estimate metabolic rates. Relative to saline-injected controls, only LPS-injected fish showed a significantly greater resting metabolic rate two days post-challenge and significantly higher maximal metabolic rates two and seven days post-challenge. This resulted in a significantly greater metabolic scope two days post-challenge, with LPS-fish transiently overcompensating by increasing maximal ATP production more than would be required for swimming in the absence of an immune challenge. LPS-challenged fish therefore increased their production of ATP to compensate physiologically for the energetic requirements of immune functioning. This response would avoid ATP shortages and allow fish to engage in an aerobically-challenging activity (swimming) even when simultaneously mounting an immune response. Nevertheless, relative to controls, both LPS- and SRBC-fish displayed reduced body mass gain one week post-injection, and LPS-fish actually lost mass. The concomitant increase in metabolic scope and reduced body mass gain of LPS-challenged fish indicates that immune-associated trade-offs are not likely to be shaped by limited oxidative metabolic capacities, but may instead result from limitations in the acquisition, assimilation or efficient use of resources.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Barreiro, L B" uniqKey="Barreiro L">L.B. Barreiro</name></author><author><name sortKey="Quintana Murci, L" uniqKey="Quintana Murci L">L. Quintana-Murci</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Fumagalli, M" uniqKey="Fumagalli M">M. Fumagalli</name></author><author><name sortKey="Sironi, M" uniqKey="Sironi M">M. Sironi</name></author><author><name sortKey="Pozzoli, U" uniqKey="Pozzoli U">U. Pozzoli</name></author><author><name sortKey="Ferrer Admettla, A" uniqKey="Ferrer Admettla A">A. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id><journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id><journal-id journal-id-type="publisher-id">plos</journal-id><journal-id journal-id-type="pmc">plosone</journal-id><journal-title-group><journal-title>PLoS ONE</journal-title></journal-title-group><issn pub-type="epub">1932-6203</issn><publisher><publisher-name>Public Library of Science</publisher-name><publisher-loc>San Francisco, CA USA</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27851769</article-id><article-id pub-id-type="pmc">5113038</article-id><article-id pub-id-type="doi">10.1371/journal.pone.0166028</article-id><article-id pub-id-type="publisher-id">PONE-D-16-04036</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Metabolism</subject><subj-group><subject>Oxygen Metabolism</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Organisms</subject><subj-group><subject>Animals</subject><subj-group><subject>Vertebrates</subject><subj-group><subject>Fishes</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Physiological Processes</subject><subj-group><subject>Respiration</subject><subj-group><subject>Oxygen Consumption</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Physiological Processes</subject><subj-group><subject>Respiration</subject><subj-group><subject>Oxygen Consumption</subject></subj-group></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune Response</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Immunology</subject><subj-group><subject>Immune Response</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject><subj-group><subject>Bioassays and Physiological Analysis</subject><subj-group><subject>Metabolic Analysis</subject><subj-group><subject>Basal Metabolic Rate Measurement</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biomechanics</subject><subj-group><subject>Biological Locomotion</subject><subj-group><subject>Swimming</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Biological Locomotion</subject><subj-group><subject>Swimming</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Medicine and Health Sciences</subject><subj-group><subject>Physiology</subject><subj-group><subject>Biological Locomotion</subject><subj-group><subject>Swimming</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Biochemistry</subject><subj-group><subject>Bioenergetics</subject></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Zoology</subject><subj-group><subject>Fish Biology</subject><subj-group><subject>Fish Physiology</subject></subj-group></subj-group></subj-group></subj-group><subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject><subj-group><subject>Zoology</subject><subj-group><subject>Animal Physiology</subject><subj-group><subject>Vertebrate Physiology</subject><subj-group><subject>Fish Physiology</subject></subj-group></subj-group></subj-group></subj-group></subj-group></article-categories><title-group><article-title>Immune-Challenged Fish Up-Regulate Their Metabolic Scope to Support Locomotion</article-title><alt-title alt-title-type="running-head">Immune Function and Aerobic Scope</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Bonneaud</surname><given-names>Camille</given-names></name><xref ref-type="aff" rid="aff001"><sup>1</sup></xref><xref ref-type="aff" rid="aff002"><sup>2</sup></xref><xref ref-type="corresp" rid="cor001">*</xref></contrib><contrib contrib-type="author"><name><surname>Wilson</surname><given-names>Robbie S.</given-names></name><xref ref-type="aff" rid="aff003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Seebacher</surname><given-names>Frank</given-names></name><xref ref-type="aff" rid="aff004"><sup>4</sup></xref></contrib></contrib-group><aff id="aff001"><label>1</label><addr-line>Centre for Ecology & Conservation, University of Exeter Penryn Campus, Penryn TR10 9FE, Cornwall, United Kingdom</addr-line></aff><aff id="aff002"><label>2</label><addr-line>Station d’Ecologie Expérimentale du CNRS, USR 2936, 09200 Moulis, France</addr-line></aff><aff id="aff003"><label>3</label><addr-line>School of Biological Sciences, University of Queensland, Brisbane St Lucia QLD 4072, Australia</addr-line></aff><aff id="aff004"><label>4</label><addr-line>School of Biological Sciences, University of Sydney, Sydney NSW 2006, Australia</addr-line></aff><contrib-group><contrib contrib-type="editor"><name><surname>Moreno-Rueda</surname><given-names>Gregorio</given-names></name><role>Editor</role><xref ref-type="aff" rid="edit1"></xref></contrib></contrib-group><aff id="edit1"><addr-line>Universidad de Granada, SPAIN</addr-line></aff><author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>The authors have declared that no competing interests exist.</p></fn><fn fn-type="con"><p><list list-type="simple"><list-item><p><bold>Conceptualization:</bold> CB RW FS.</p></list-item><list-item><p><bold>Data curation:</bold> CB FS.</p></list-item><list-item><p><bold>Formal analysis:</bold> CB.</p></list-item><list-item><p><bold>Investigation:</bold> CB FS.</p></list-item><list-item><p><bold>Methodology:</bold> CB RW FS.</p></list-item><list-item><p><bold>Resources:</bold> CB RW FS.</p></list-item><list-item><p><bold>Visualization:</bold> CB.</p></list-item><list-item><p><bold>Writing – original draft:</bold> CB.</p></list-item><list-item><p><bold>Writing – review & editing:</bold> CB RW FS.</p></list-item></list></p></fn><corresp id="cor001">* E-mail: <email>c.bonneaud@exeter.ac.uk</email></corresp></author-notes><pub-date pub-type="epub"><day>16</day><month>11</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>11</volume><issue>11</issue><elocation-id>e0166028</elocation-id><history><date date-type="received"><day>16</day><month>2</month><year>2016</year></date><date date-type="accepted"><day>22</day><month>10</month><year>2016</year></date></history><permissions><copyright-statement>© 2016 Bonneaud et al</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>Bonneaud et al</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="pone.0166028.pdf"></self-uri><abstract><p>Energy-based trade-offs occur when investment in one fitness-related trait diverts energy away from other traits. The extent to which such trade-offs are shaped by limits on the rate of conversion of energy ingested in food (e.g. carbohydrates) into chemical energy (ATP) by oxidative metabolism rather than by the amount of food ingested in the first place is, however, unclear. Here we tested whether the ATP required for mounting an immune response will lead to a trade-off with ATP available for physical activity in mosquitofish (<italic>Gambusia holbrooki</italic>). To this end, we challenged fish either with lipopolysaccharide (LPS) from <italic>E</italic>. <italic>coli</italic> or with Sheep Red Blood Cells (SRBC), and measured oxygen consumption at rest and during swimming at maximum speed 24h, 48h and 7 days post-challenge in order to estimate metabolic rates. Relative to saline-injected controls, only LPS-injected fish showed a significantly greater resting metabolic rate two days post-challenge and significantly higher maximal metabolic rates two and seven days post-challenge. This resulted in a significantly greater metabolic scope two days post-challenge, with LPS-fish transiently overcompensating by increasing maximal ATP production more than would be required for swimming in the absence of an immune challenge. LPS-challenged fish therefore increased their production of ATP to compensate physiologically for the energetic requirements of immune functioning. This response would avoid ATP shortages and allow fish to engage in an aerobically-challenging activity (swimming) even when simultaneously mounting an immune response. Nevertheless, relative to controls, both LPS- and SRBC-fish displayed reduced body mass gain one week post-injection, and LPS-fish actually lost mass. The concomitant increase in metabolic scope and reduced body mass gain of LPS-challenged fish indicates that immune-associated trade-offs are not likely to be shaped by limited oxidative metabolic capacities, but may instead result from limitations in the acquisition, assimilation or efficient use of resources.</p></abstract><funding-group><award-group id="award001"><funding-source><institution>Marie Curie Reintegration Grant</institution></funding-source><award-id>FP7-PEOPLE-IRG-2008 #239257</award-id><principal-award-recipient><name><surname>Bonneaud</surname><given-names>Camille</given-names></name></principal-award-recipient></award-group><award-group id="award002"><funding-source><institution-wrap><institution-id institution-id-type="funder-id">http://dx.doi.org/10.13039/501100000270</institution-id><institution>Natural Environment Research Council</institution></institution-wrap></funding-source><award-id>NE/M00256X</award-id><principal-award-recipient><name><surname>Bonneaud</surname><given-names>Camille</given-names></name></principal-award-recipient></award-group><funding-statement>This research was supported by a Marie Curie Reintegration Grant (FP7-PEOPLE-IRG-2008 #239257) to Dr Camille Bonneaud; Natural Environment Research Council (NE/M00256X) to Dr Camille Bonneaud; Australian Research Council Discovery Projects (DP120101215) to Prof Frank Seebacher and Prof Robbie Wilson. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.</funding-statement></funding-group><counts><fig-count count="3"></fig-count><table-count count="1"></table-count><page-count count="14"></page-count></counts><custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name><meta-value>Data are available in DRYAD at DOI: doi:<ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.5061/dryad.km3qd">10.5061/dryad.km3qd</ext-link>.</meta-value></custom-meta></custom-meta-group></article-meta><notes><title>Data Availability</title><p>Data are available in DRYAD at DOI: doi:<ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.5061/dryad.km3qd">10.5061/dryad.km3qd</ext-link>.</p></notes></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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