Impact of Menthol on Growth and Photosynthetic Function of Breviolum Minutum (Dinoflagellata, Dinophyceae, Symbiodiniaceae) and Interactions with its Aiptasia Host
Environmental change, including global warming and chemical pollution, can compromise cnidarian‐(e.g., coral‐) dinoflagellate symbioses and cause coral bleaching. Understanding the mechanisms that regulate these symbioses will inform strategies for sustaining healthy coral–reef communities. A model...
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description | Environmental change, including global warming and chemical pollution, can compromise cnidarian‐(e.g., coral‐) dinoflagellate symbioses and cause coral bleaching. Understanding the mechanisms that regulate these symbioses will inform strategies for sustaining healthy coral–reef communities. A model system for corals is the symbiosis between the sea anemone Exaiptasia pallida (common name Aiptasia) and its dinoflagellate partners (family Symbiodiniaceae). To complement existing studies of the interactions between these organisms, we examined the impact of menthol, a reagent often used to render cnidarians aposymbiotic, on the dinoflagellate Breviolum minutum, both in culture and in hospite. In both environments, the growth and photosynthesis of this alga were compromised at either 100 or 300 µM menthol. We observed reduction in PSII and PSI functions, the abundances of reaction‐center proteins, and, at 300 µM menthol, of total cellular proteins. Interestingly, for free‐living algae exposed to 100 µM menthol, an initial decline in growth, photosynthetic activities, pigmentation, and protein abundances reversed after 5–15 d, eventually approaching control levels. This behavior was observed in cells maintained in continuous light, but not in cells experiencing a light–dark regimen, suggesting that B. minutum can detoxify menthol or acclimate and repair damaged photosynthetic complexes in a light‐ and/or energy‐dependent manner. Extended exposures of cultured algae to 300 µM menthol ultimately resulted in algal death. Most symbiotic anemones were also unable to survive this menthol concentration for 30 d. Additionally, cells impaired for photosynthesis by pre‐treatment with 300 µM menthol exhibited reduced efficiency in re‐populating the anemone host. |
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Understanding the mechanisms that regulate these symbioses will inform strategies for sustaining healthy coral–reef communities. A model system for corals is the symbiosis between the sea anemone Exaiptasia pallida (common name Aiptasia) and its dinoflagellate partners (family Symbiodiniaceae). To complement existing studies of the interactions between these organisms, we examined the impact of menthol, a reagent often used to render cnidarians aposymbiotic, on the dinoflagellate Breviolum minutum, both in culture and in hospite. In both environments, the growth and photosynthesis of this alga were compromised at either 100 or 300 µM menthol. We observed reduction in PSII and PSI functions, the abundances of reaction‐center proteins, and, at 300 µM menthol, of total cellular proteins. Interestingly, for free‐living algae exposed to 100 µM menthol, an initial decline in growth, photosynthetic activities, pigmentation, and protein abundances reversed after 5–15 d, eventually approaching control levels. This behavior was observed in cells maintained in continuous light, but not in cells experiencing a light–dark regimen, suggesting that B. minutum can detoxify menthol or acclimate and repair damaged photosynthetic complexes in a light‐ and/or energy‐dependent manner. Extended exposures of cultured algae to 300 µM menthol ultimately resulted in algal death. Most symbiotic anemones were also unable to survive this menthol concentration for 30 d. Additionally, cells impaired for photosynthesis by pre‐treatment with 300 µM menthol exhibited reduced efficiency in re‐populating the anemone host.</description><identifier>ISSN: 0022-3646</identifier><identifier>EISSN: 1529-8817</identifier><identifier>DOI: 10.1111/jpy.13081</identifier><identifier>PMID: 33025575</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Abundance ; Aiptasia ; Algae ; Animals ; bleaching ; Cell culture ; Cells ; Chemical contamination ; Chemical pollutants ; Chemical pollution ; Climate change ; cnidaria ; Colour ; Coral bleaching ; Corals ; Dinoflagellates ; Dinoflagellida ; Environmental changes ; Exaiptasia pallida ; Global warming ; Growth ; holobiont ; Light ; Marine invertebrates ; Menthol ; Microalgae culture ; Microorganisms ; Photosynthesis ; Photosystem I ; Photosystem II ; Pigmentation ; Proteins ; Reagents ; sea anemone ; Sea Anemones ; Survival ; Symbiodiniaceae ; Symbiodinium ; Symbionts ; Symbiosis ; Vernacular names</subject><ispartof>Journal of phycology, 2021-02, Vol.57 (1), p.245-257</ispartof><rights>2020 Phycological Society of America</rights><rights>2020 Phycological Society of America.</rights><rights>2021 Phycological Society of America</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3531-e829a11ab75968e1b632fe1771ae6c9eac9a412da647e7f78c7e11feb079ab63</citedby><cites>FETCH-LOGICAL-c3531-e829a11ab75968e1b632fe1771ae6c9eac9a412da647e7f78c7e11feb079ab63</cites><orcidid>0000-0002-1787-2572 ; 0000-0003-3226-9840 ; 0000-0002-3747-5881</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fjpy.13081$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fjpy.13081$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,777,781,1412,27905,27906,45555,45556</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33025575$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Clowez, Sophie</creatorcontrib><creatorcontrib>Renicke, Christian</creatorcontrib><creatorcontrib>Pringle, John R.</creatorcontrib><creatorcontrib>Grossman, Arthur R.</creatorcontrib><title>Impact of Menthol on Growth and Photosynthetic Function of Breviolum Minutum (Dinoflagellata, Dinophyceae, Symbiodiniaceae) and Interactions with its Aiptasia Host</title><title>Journal of phycology</title><addtitle>J Phycol</addtitle><description>Environmental change, including global warming and chemical pollution, can compromise cnidarian‐(e.g., coral‐) dinoflagellate symbioses and cause coral bleaching. Understanding the mechanisms that regulate these symbioses will inform strategies for sustaining healthy coral–reef communities. A model system for corals is the symbiosis between the sea anemone Exaiptasia pallida (common name Aiptasia) and its dinoflagellate partners (family Symbiodiniaceae). To complement existing studies of the interactions between these organisms, we examined the impact of menthol, a reagent often used to render cnidarians aposymbiotic, on the dinoflagellate Breviolum minutum, both in culture and in hospite. In both environments, the growth and photosynthesis of this alga were compromised at either 100 or 300 µM menthol. We observed reduction in PSII and PSI functions, the abundances of reaction‐center proteins, and, at 300 µM menthol, of total cellular proteins. Interestingly, for free‐living algae exposed to 100 µM menthol, an initial decline in growth, photosynthetic activities, pigmentation, and protein abundances reversed after 5–15 d, eventually approaching control levels. This behavior was observed in cells maintained in continuous light, but not in cells experiencing a light–dark regimen, suggesting that B. minutum can detoxify menthol or acclimate and repair damaged photosynthetic complexes in a light‐ and/or energy‐dependent manner. Extended exposures of cultured algae to 300 µM menthol ultimately resulted in algal death. Most symbiotic anemones were also unable to survive this menthol concentration for 30 d. Additionally, cells impaired for photosynthesis by pre‐treatment with 300 µM menthol exhibited reduced efficiency in re‐populating the anemone host.</description><subject>Abundance</subject><subject>Aiptasia</subject><subject>Algae</subject><subject>Animals</subject><subject>bleaching</subject><subject>Cell culture</subject><subject>Cells</subject><subject>Chemical contamination</subject><subject>Chemical pollutants</subject><subject>Chemical pollution</subject><subject>Climate change</subject><subject>cnidaria</subject><subject>Colour</subject><subject>Coral bleaching</subject><subject>Corals</subject><subject>Dinoflagellates</subject><subject>Dinoflagellida</subject><subject>Environmental changes</subject><subject>Exaiptasia pallida</subject><subject>Global warming</subject><subject>Growth</subject><subject>holobiont</subject><subject>Light</subject><subject>Marine invertebrates</subject><subject>Menthol</subject><subject>Microalgae culture</subject><subject>Microorganisms</subject><subject>Photosynthesis</subject><subject>Photosystem I</subject><subject>Photosystem II</subject><subject>Pigmentation</subject><subject>Proteins</subject><subject>Reagents</subject><subject>sea anemone</subject><subject>Sea Anemones</subject><subject>Survival</subject><subject>Symbiodiniaceae</subject><subject>Symbiodinium</subject><subject>Symbionts</subject><subject>Symbiosis</subject><subject>Vernacular names</subject><issn>0022-3646</issn><issn>1529-8817</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kc9u1DAQhy0EosvCgRdAlrhQqWk9-efkWAptF7WiEr1wiibeCetVYgfbYZXn4UXx7hZu-DLy-PP3k2YYewviHOK52I7zOWSigmdsAUVaJ1UF8jlbCJGmSVbm5Ql75f1WCCHLAl6ykywTaVHIYsF-r4YRVeC24_dkwsb23Bp-4-wubDiaNX_Y2GD9HJ8oaMWvJ6OCjkj88NHRL237aeD32kwh1g-ftLFdjz-o7zHgGd_fx82sCOmMf5uHVtu1Nhr3jdODf2UCOTw4Pd_pmKqD55d6DOg18lvrw2v2osPe05unumSP158fr26Tu683q6vLu0RlRQYJVWmNANjKoi4rgrbM0o5ASkAqVU2oaswhXWOZS5KdrJQkgI5aIWuM8JK9P2pHZ39O5EOztZMzMbFJ8zhRgDzmLNnpkVLOeu-oa0anB3RzA6LZb6OJ22gO24jsuyfj1A60_kf-HX8ELo7ATvc0_9_UfHn4flT-AYjtltE</recordid><startdate>202102</startdate><enddate>202102</enddate><creator>Clowez, Sophie</creator><creator>Renicke, Christian</creator><creator>Pringle, John R.</creator><creator>Grossman, Arthur R.</creator><general>Wiley Subscription Services, Inc</general><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>7TN</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><orcidid>https://orcid.org/0000-0002-1787-2572</orcidid><orcidid>https://orcid.org/0000-0003-3226-9840</orcidid><orcidid>https://orcid.org/0000-0002-3747-5881</orcidid></search><sort><creationdate>202102</creationdate><title>Impact of Menthol on Growth and Photosynthetic Function of Breviolum Minutum (Dinoflagellata, Dinophyceae, Symbiodiniaceae) and Interactions with its Aiptasia Host</title><author>Clowez, Sophie ; Renicke, Christian ; Pringle, John R. ; Grossman, Arthur R.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3531-e829a11ab75968e1b632fe1771ae6c9eac9a412da647e7f78c7e11feb079ab63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Abundance</topic><topic>Aiptasia</topic><topic>Algae</topic><topic>Animals</topic><topic>bleaching</topic><topic>Cell culture</topic><topic>Cells</topic><topic>Chemical contamination</topic><topic>Chemical pollutants</topic><topic>Chemical pollution</topic><topic>Climate change</topic><topic>cnidaria</topic><topic>Colour</topic><topic>Coral bleaching</topic><topic>Corals</topic><topic>Dinoflagellates</topic><topic>Dinoflagellida</topic><topic>Environmental changes</topic><topic>Exaiptasia pallida</topic><topic>Global warming</topic><topic>Growth</topic><topic>holobiont</topic><topic>Light</topic><topic>Marine invertebrates</topic><topic>Menthol</topic><topic>Microalgae culture</topic><topic>Microorganisms</topic><topic>Photosynthesis</topic><topic>Photosystem I</topic><topic>Photosystem II</topic><topic>Pigmentation</topic><topic>Proteins</topic><topic>Reagents</topic><topic>sea anemone</topic><topic>Sea Anemones</topic><topic>Survival</topic><topic>Symbiodiniaceae</topic><topic>Symbiodinium</topic><topic>Symbionts</topic><topic>Symbiosis</topic><topic>Vernacular names</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Clowez, Sophie</creatorcontrib><creatorcontrib>Renicke, Christian</creatorcontrib><creatorcontrib>Pringle, John R.</creatorcontrib><creatorcontrib>Grossman, Arthur R.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Oceanic Abstracts</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><jtitle>Journal of phycology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Clowez, Sophie</au><au>Renicke, Christian</au><au>Pringle, John R.</au><au>Grossman, Arthur R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Impact of Menthol on Growth and Photosynthetic Function of Breviolum Minutum (Dinoflagellata, Dinophyceae, Symbiodiniaceae) and Interactions with its Aiptasia Host</atitle><jtitle>Journal of phycology</jtitle><addtitle>J Phycol</addtitle><date>2021-02</date><risdate>2021</risdate><volume>57</volume><issue>1</issue><spage>245</spage><epage>257</epage><pages>245-257</pages><issn>0022-3646</issn><eissn>1529-8817</eissn><abstract>Environmental change, including global warming and chemical pollution, can compromise cnidarian‐(e.g., coral‐) dinoflagellate symbioses and cause coral bleaching. Understanding the mechanisms that regulate these symbioses will inform strategies for sustaining healthy coral–reef communities. A model system for corals is the symbiosis between the sea anemone Exaiptasia pallida (common name Aiptasia) and its dinoflagellate partners (family Symbiodiniaceae). To complement existing studies of the interactions between these organisms, we examined the impact of menthol, a reagent often used to render cnidarians aposymbiotic, on the dinoflagellate Breviolum minutum, both in culture and in hospite. In both environments, the growth and photosynthesis of this alga were compromised at either 100 or 300 µM menthol. We observed reduction in PSII and PSI functions, the abundances of reaction‐center proteins, and, at 300 µM menthol, of total cellular proteins. Interestingly, for free‐living algae exposed to 100 µM menthol, an initial decline in growth, photosynthetic activities, pigmentation, and protein abundances reversed after 5–15 d, eventually approaching control levels. This behavior was observed in cells maintained in continuous light, but not in cells experiencing a light–dark regimen, suggesting that B. minutum can detoxify menthol or acclimate and repair damaged photosynthetic complexes in a light‐ and/or energy‐dependent manner. Extended exposures of cultured algae to 300 µM menthol ultimately resulted in algal death. Most symbiotic anemones were also unable to survive this menthol concentration for 30 d. Additionally, cells impaired for photosynthesis by pre‐treatment with 300 µM menthol exhibited reduced efficiency in re‐populating the anemone host.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>33025575</pmid><doi>10.1111/jpy.13081</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-1787-2572</orcidid><orcidid>https://orcid.org/0000-0003-3226-9840</orcidid><orcidid>https://orcid.org/0000-0002-3747-5881</orcidid></addata></record> |
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subjects | Abundance Aiptasia Algae Animals bleaching Cell culture Cells Chemical contamination Chemical pollutants Chemical pollution Climate change cnidaria Colour Coral bleaching Corals Dinoflagellates Dinoflagellida Environmental changes Exaiptasia pallida Global warming Growth holobiont Light Marine invertebrates Menthol Microalgae culture Microorganisms Photosynthesis Photosystem I Photosystem II Pigmentation Proteins Reagents sea anemone Sea Anemones Survival Symbiodiniaceae Symbiodinium Symbionts Symbiosis Vernacular names |
title | Impact of Menthol on Growth and Photosynthetic Function of Breviolum Minutum (Dinoflagellata, Dinophyceae, Symbiodiniaceae) and Interactions with its Aiptasia Host |
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