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influence of symbiont type on photosynthetic carbon flux in a model cnidarian–dinoflagellate symbiosis
We measured the relationship between symbiont diversity, nutritional potential, and symbiotic success in the cnidarian–dinoflagellate symbiosis, by infecting aposymbiotic (i.e. symbiont-free) specimens of the model sea anemone Aiptasia sp. with a range of Symbiodinium types. Four cultured heterologo...
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Published in: | Marine biology 2014-03, Vol.161 (3), p.711-724 |
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description | We measured the relationship between symbiont diversity, nutritional potential, and symbiotic success in the cnidarian–dinoflagellate symbiosis, by infecting aposymbiotic (i.e. symbiont-free) specimens of the model sea anemone Aiptasia sp. with a range of Symbiodinium types. Four cultured heterologous Symbiodinium types (i.e. originally isolated from other host species) were used, plus both cultured and freshly isolated homologous zooxanthellae (i.e. from Aiptasia sp.). Rates of photosynthesis, respiration, and symbiont growth were measured during symbiosis establishment and used to estimate the contribution of the zooxanthellae to the animal’s respiratory carbon demands (CZAR). Anemones containing Symbiodinium B1 (both homologous and heterologous) tended to attain higher CZAR values and hence benefit most from their symbiotic partners. This was despite Symbiodinium B1 not achieving the highest cell densities, though it did grow more quickly during the earliest stages of the infection process. Rather, the heterologous Symbiodinium types A1.4, E2, and F5.1 attained the highest densities, with populations of E2 and F5.1 also exhibiting the highest photosynthetic rates. This apparent success was countered, however, by very high rates of symbiosis respiration that ultimately resulted in lower CZAR values. This study highlights the impact of symbiont type on the functionality and autotrophic potential of the symbiosis. Most interestingly, it suggests that certain heterologous symbionts may behave opportunistically, proliferating rapidly but in a manner that is energetically costly to the host. Such negative host–symbiont interactions may contribute to the host–symbiont specificity seen in cnidarian–dinoflagellate symbioses and potentially limit the potential for partner switching as an adaptive mechanism. |
doi_str_mv | 10.1007/s00227-013-2372-8 |
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Four cultured heterologous Symbiodinium types (i.e. originally isolated from other host species) were used, plus both cultured and freshly isolated homologous zooxanthellae (i.e. from Aiptasia sp.). Rates of photosynthesis, respiration, and symbiont growth were measured during symbiosis establishment and used to estimate the contribution of the zooxanthellae to the animal’s respiratory carbon demands (CZAR). Anemones containing Symbiodinium B1 (both homologous and heterologous) tended to attain higher CZAR values and hence benefit most from their symbiotic partners. This was despite Symbiodinium B1 not achieving the highest cell densities, though it did grow more quickly during the earliest stages of the infection process. Rather, the heterologous Symbiodinium types A1.4, E2, and F5.1 attained the highest densities, with populations of E2 and F5.1 also exhibiting the highest photosynthetic rates. This apparent success was countered, however, by very high rates of symbiosis respiration that ultimately resulted in lower CZAR values. This study highlights the impact of symbiont type on the functionality and autotrophic potential of the symbiosis. Most interestingly, it suggests that certain heterologous symbionts may behave opportunistically, proliferating rapidly but in a manner that is energetically costly to the host. Such negative host–symbiont interactions may contribute to the host–symbiont specificity seen in cnidarian–dinoflagellate symbioses and potentially limit the potential for partner switching as an adaptive mechanism.</description><identifier>ISSN: 0025-3162</identifier><identifier>EISSN: 1432-1793</identifier><identifier>DOI: 10.1007/s00227-013-2372-8</identifier><identifier>CODEN: MBIOAJ</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer-Verlag</publisher><subject>Aiptasia ; Animal and plant ecology ; Animal, plant and microbial ecology ; Aquatic life ; Biological and medical sciences ; Biomedical and Life Sciences ; Carbon ; Cnidaria. Ctenaria ; Coelenterata ; dietary nutrient sources ; Dinoflagellates ; Environment ; Environmental aspects ; Freshwater & Marine Ecology ; Fundamental and applied biological sciences. Psychology ; Invertebrates ; Life Sciences ; Marine ; Marine & Freshwater Sciences ; Marine biology ; Microbiology ; Oceanography ; Original Paper ; Photosynthesis ; Respiration ; Sea water ecosystems ; Symbiodinium ; symbionts ; Symbiosis ; Synecology ; Zoology</subject><ispartof>Marine biology, 2014-03, Vol.161 (3), p.711-724</ispartof><rights>Springer-Verlag Berlin Heidelberg 2013</rights><rights>2015 INIST-CNRS</rights><rights>COPYRIGHT 2014 Springer</rights><rights>Springer-Verlag Berlin Heidelberg 2014</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c508t-e4cc234230f3a2ab895b65a0d6dfa52616ea4cd938387c1f4aa16a4f4b65fc943</citedby><cites>FETCH-LOGICAL-c508t-e4cc234230f3a2ab895b65a0d6dfa52616ea4cd938387c1f4aa16a4f4b65fc943</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27903,27904</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=28596345$$DView record in Pascal Francis$$Hfree_for_read</backlink></links><search><creatorcontrib>Starzak, Dorota E</creatorcontrib><creatorcontrib>Quinnell, Rosanne G</creatorcontrib><creatorcontrib>Nitschke, Matthew R</creatorcontrib><creatorcontrib>Davy, Simon K</creatorcontrib><title>influence of symbiont type on photosynthetic carbon flux in a model cnidarian–dinoflagellate symbiosis</title><title>Marine biology</title><addtitle>Mar Biol</addtitle><description>We measured the relationship between symbiont diversity, nutritional potential, and symbiotic success in the cnidarian–dinoflagellate symbiosis, by infecting aposymbiotic (i.e. symbiont-free) specimens of the model sea anemone Aiptasia sp. with a range of Symbiodinium types. Four cultured heterologous Symbiodinium types (i.e. originally isolated from other host species) were used, plus both cultured and freshly isolated homologous zooxanthellae (i.e. from Aiptasia sp.). Rates of photosynthesis, respiration, and symbiont growth were measured during symbiosis establishment and used to estimate the contribution of the zooxanthellae to the animal’s respiratory carbon demands (CZAR). Anemones containing Symbiodinium B1 (both homologous and heterologous) tended to attain higher CZAR values and hence benefit most from their symbiotic partners. This was despite Symbiodinium B1 not achieving the highest cell densities, though it did grow more quickly during the earliest stages of the infection process. Rather, the heterologous Symbiodinium types A1.4, E2, and F5.1 attained the highest densities, with populations of E2 and F5.1 also exhibiting the highest photosynthetic rates. This apparent success was countered, however, by very high rates of symbiosis respiration that ultimately resulted in lower CZAR values. This study highlights the impact of symbiont type on the functionality and autotrophic potential of the symbiosis. Most interestingly, it suggests that certain heterologous symbionts may behave opportunistically, proliferating rapidly but in a manner that is energetically costly to the host. Such negative host–symbiont interactions may contribute to the host–symbiont specificity seen in cnidarian–dinoflagellate symbioses and potentially limit the potential for partner switching as an adaptive mechanism.</description><subject>Aiptasia</subject><subject>Animal and plant ecology</subject><subject>Animal, plant and microbial ecology</subject><subject>Aquatic life</subject><subject>Biological and medical sciences</subject><subject>Biomedical and Life Sciences</subject><subject>Carbon</subject><subject>Cnidaria. Ctenaria</subject><subject>Coelenterata</subject><subject>dietary nutrient sources</subject><subject>Dinoflagellates</subject><subject>Environment</subject><subject>Environmental aspects</subject><subject>Freshwater & Marine Ecology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Invertebrates</subject><subject>Life Sciences</subject><subject>Marine</subject><subject>Marine & Freshwater Sciences</subject><subject>Marine biology</subject><subject>Microbiology</subject><subject>Oceanography</subject><subject>Original Paper</subject><subject>Photosynthesis</subject><subject>Respiration</subject><subject>Sea water ecosystems</subject><subject>Symbiodinium</subject><subject>symbionts</subject><subject>Symbiosis</subject><subject>Synecology</subject><subject>Zoology</subject><issn>0025-3162</issn><issn>1432-1793</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><recordid>eNp9ksuKFDEUhgtRsB19AFcWiOCmxpN71XIYvMGAC511OJ1KqjNUJW1SDfZu3sE39ElMUY03Gski5Jzv_zk5_FX1nMAlAVBvMgClqgHCGsoUbdoH1YZwRhuiOvaw2pS2aBiR9HH1JOc7KG9F2aba-eDGgw3G1tHV-ThtfQxzPR_3pRDq_S7OMR_DvLOzN7XBtC3VovhW-1BjPcXejrUJvsfkMfy4_977EN2Igx1HnO3JMfv8tHrkcMz22em-qG7fvf1y_aG5-fT-4_XVTWMEtHNjuTGUccrAMaS4bTuxlQKhl71DQSWRFrnpO9ayVhniOCKRyB0vlDMdZxfV69V3n-LXg82znnw2yzTBxkPWRIBgjEquCvryH_QuHlIo0y0UdNBKRX5TA45Wl3XFOaFZTPUVkwIUKLZQzRlqsMEmHGOwzpfyX_zlGb6c3k7enBWQVWBSzDlZp_fJT5iOmoBeIqDXCOgSAb1EQLdF8-r0QcwGR5cwGJ9_CWkrOsm4KBxduVxaYbDpj0X8x_zFKnIYNQ6pGN9-pkA4AKGc0pb9BPTZyZk</recordid><startdate>20140301</startdate><enddate>20140301</enddate><creator>Starzak, Dorota E</creator><creator>Quinnell, Rosanne G</creator><creator>Nitschke, Matthew R</creator><creator>Davy, Simon K</creator><general>Springer-Verlag</general><general>Springer Berlin Heidelberg</general><general>Springer</general><general>Springer Nature B.V</general><scope>FBQ</scope><scope>IQODW</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QG</scope><scope>7SN</scope><scope>7ST</scope><scope>7TN</scope><scope>7U7</scope><scope>7XB</scope><scope>88A</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>F1W</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H95</scope><scope>HCIFZ</scope><scope>L.G</scope><scope>LK8</scope><scope>M2O</scope><scope>M7N</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PCBAR</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>R05</scope><scope>RC3</scope><scope>SOI</scope></search><sort><creationdate>20140301</creationdate><title>influence of symbiont type on photosynthetic carbon flux in a model cnidarian–dinoflagellate symbiosis</title><author>Starzak, Dorota E ; Quinnell, Rosanne G ; Nitschke, Matthew R ; Davy, Simon K</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c508t-e4cc234230f3a2ab895b65a0d6dfa52616ea4cd938387c1f4aa16a4f4b65fc943</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Aiptasia</topic><topic>Animal and plant ecology</topic><topic>Animal, plant and microbial ecology</topic><topic>Aquatic life</topic><topic>Biological and medical sciences</topic><topic>Biomedical and Life Sciences</topic><topic>Carbon</topic><topic>Cnidaria. 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Four cultured heterologous Symbiodinium types (i.e. originally isolated from other host species) were used, plus both cultured and freshly isolated homologous zooxanthellae (i.e. from Aiptasia sp.). Rates of photosynthesis, respiration, and symbiont growth were measured during symbiosis establishment and used to estimate the contribution of the zooxanthellae to the animal’s respiratory carbon demands (CZAR). Anemones containing Symbiodinium B1 (both homologous and heterologous) tended to attain higher CZAR values and hence benefit most from their symbiotic partners. This was despite Symbiodinium B1 not achieving the highest cell densities, though it did grow more quickly during the earliest stages of the infection process. Rather, the heterologous Symbiodinium types A1.4, E2, and F5.1 attained the highest densities, with populations of E2 and F5.1 also exhibiting the highest photosynthetic rates. This apparent success was countered, however, by very high rates of symbiosis respiration that ultimately resulted in lower CZAR values. This study highlights the impact of symbiont type on the functionality and autotrophic potential of the symbiosis. Most interestingly, it suggests that certain heterologous symbionts may behave opportunistically, proliferating rapidly but in a manner that is energetically costly to the host. Such negative host–symbiont interactions may contribute to the host–symbiont specificity seen in cnidarian–dinoflagellate symbioses and potentially limit the potential for partner switching as an adaptive mechanism.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer-Verlag</pub><doi>10.1007/s00227-013-2372-8</doi><tpages>14</tpages></addata></record> |
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subjects | Aiptasia Animal and plant ecology Animal, plant and microbial ecology Aquatic life Biological and medical sciences Biomedical and Life Sciences Carbon Cnidaria. Ctenaria Coelenterata dietary nutrient sources Dinoflagellates Environment Environmental aspects Freshwater & Marine Ecology Fundamental and applied biological sciences. Psychology Invertebrates Life Sciences Marine Marine & Freshwater Sciences Marine biology Microbiology Oceanography Original Paper Photosynthesis Respiration Sea water ecosystems Symbiodinium symbionts Symbiosis Synecology Zoology |
title | influence of symbiont type on photosynthetic carbon flux in a model cnidarian–dinoflagellate symbiosis |
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