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Most Low-Abundance “Background” Symbiodinium spp. Are Transitory and Have Minimal Functional Significance for Symbiotic Corals
Speculation surrounds the importance of ecologically cryptic Symbiodinium spp. (dinoflagellates) that occur at low abundances in reef-building corals and in the surrounding environment. Evidence acquired from extensive sampling, long-term monitoring, and experimental manipulation can allow us to ded...
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Published in: | Microbial ecology 2016-04, Vol.71 (3), p.771-783 |
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description | Speculation surrounds the importance of ecologically cryptic Symbiodinium spp. (dinoflagellates) that occur at low abundances in reef-building corals and in the surrounding environment. Evidence acquired from extensive sampling, long-term monitoring, and experimental manipulation can allow us to deduce the ecology and functional significance of these populations and whether they might contribute to the response of coral-dinoflagellate mutualisms to climate change. Quantitative PCR was used here to diagnose the prevalence, seasonal variation, and abundances of Symbiodinium spp. within and between colonies of the coral, Alveopora japonica. Consistent with broader geographic sampling, only one species comprised 99.9 %, or greater, the population of symbionts in every sample. However, other Symbiodinium including the non-mutualistic species, Symbiodinium voratum, were often detected, but at estimated cell densities thousands-fold less than the dominant symbiont. The temporal variation in prevalence and abundances of these “background” Symbiodinium could not be definitively related to any particular environmental factor including seasonality and water chemistry. The prevalence (proportion detected among host samples), but not abundance, of S. voratum may weakly correspond to increases in environmental inorganic silica (SiO₂) and possibly nitrogen (NO₃). When multiple background Symbiodinium occurred within an individual polyp, the average cell densities were positively correlated, suggesting non-specific processes of cell sorting and retention by the animal. While these findings substantiate the existence of a broader, yet uncharacterized, diversity of Symbiodinium, we conclude that only those species which can occur in high abundance and are temporally stable are ultimately important to coral-dinoflagellate mutualisms. Many transient Symbiodinium spp., which occur only at trace abundances in the coral’s microbiome, belong to different functional guilds and likely have little, if any, importance to a coral’s physiology. The successful integration between host and symbiont into a stable functional unit should therefore be considered when defining host-symbiont specificity. |
doi_str_mv | 10.1007/s00248-015-0724-2 |
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Evidence acquired from extensive sampling, long-term monitoring, and experimental manipulation can allow us to deduce the ecology and functional significance of these populations and whether they might contribute to the response of coral-dinoflagellate mutualisms to climate change. Quantitative PCR was used here to diagnose the prevalence, seasonal variation, and abundances of Symbiodinium spp. within and between colonies of the coral, Alveopora japonica. Consistent with broader geographic sampling, only one species comprised 99.9 %, or greater, the population of symbionts in every sample. However, other Symbiodinium including the non-mutualistic species, Symbiodinium voratum, were often detected, but at estimated cell densities thousands-fold less than the dominant symbiont. The temporal variation in prevalence and abundances of these “background” Symbiodinium could not be definitively related to any particular environmental factor including seasonality and water chemistry. The prevalence (proportion detected among host samples), but not abundance, of S. voratum may weakly correspond to increases in environmental inorganic silica (SiO₂) and possibly nitrogen (NO₃). When multiple background Symbiodinium occurred within an individual polyp, the average cell densities were positively correlated, suggesting non-specific processes of cell sorting and retention by the animal. While these findings substantiate the existence of a broader, yet uncharacterized, diversity of Symbiodinium, we conclude that only those species which can occur in high abundance and are temporally stable are ultimately important to coral-dinoflagellate mutualisms. Many transient Symbiodinium spp., which occur only at trace abundances in the coral’s microbiome, belong to different functional guilds and likely have little, if any, importance to a coral’s physiology. The successful integration between host and symbiont into a stable functional unit should therefore be considered when defining host-symbiont specificity.</description><identifier>ISSN: 0095-3628</identifier><identifier>EISSN: 1432-184X</identifier><identifier>DOI: 10.1007/s00248-015-0724-2</identifier><identifier>PMID: 26781946</identifier><language>eng</language><publisher>New York: Springer US</publisher><subject>Alveopora japonica ; Animals ; Anthozoa - parasitology ; Biodiversity ; Biomedical and Life Sciences ; Climate change ; coral reefs ; corals ; correlation ; Dinoflagellida - classification ; Dinoflagellida - isolation & purification ; Dinoflagellida - physiology ; Ecology ; Environmental factors ; Geoecology/Natural Processes ; HOST MICROBE INTERACTIONS ; hydrochemistry ; Life Sciences ; Microbial Ecology ; Microbiology ; microbiome ; monitoring ; Nature Conservation ; nitrogen ; Nitrogen - metabolism ; Phylogeny ; physiology ; quantitative polymerase chain reaction ; seasonal variation ; Seasonal variations ; Seasons ; Silica ; Symbiodinium ; symbionts ; Symbiosis ; Water chemistry ; Water Quality/Water Pollution</subject><ispartof>Microbial ecology, 2016-04, Vol.71 (3), p.771-783</ispartof><rights>Springer Science+Business Media New York 2016</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c517t-406915e11f2a238798e31ba5d8760356452b664c2e9e0955fd3775f614b960533</citedby><cites>FETCH-LOGICAL-c517t-406915e11f2a238798e31ba5d8760356452b664c2e9e0955fd3775f614b960533</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/48722744$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/48722744$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26781946$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lee, Moo Joon</creatorcontrib><creatorcontrib>Jeong, Hae Jin</creatorcontrib><creatorcontrib>Jang, Se Hyeon</creatorcontrib><creatorcontrib>Lee, Sung Yeon</creatorcontrib><creatorcontrib>Kang, Nam Seon</creatorcontrib><creatorcontrib>Lee, Kyung Ha</creatorcontrib><creatorcontrib>Kim, Hyung Seop</creatorcontrib><creatorcontrib>Wham, Drew C</creatorcontrib><creatorcontrib>LaJeunesse, Todd C</creatorcontrib><title>Most Low-Abundance “Background” Symbiodinium spp. Are Transitory and Have Minimal Functional Significance for Symbiotic Corals</title><title>Microbial ecology</title><addtitle>Microb Ecol</addtitle><addtitle>Microb Ecol</addtitle><description>Speculation surrounds the importance of ecologically cryptic Symbiodinium spp. (dinoflagellates) that occur at low abundances in reef-building corals and in the surrounding environment. Evidence acquired from extensive sampling, long-term monitoring, and experimental manipulation can allow us to deduce the ecology and functional significance of these populations and whether they might contribute to the response of coral-dinoflagellate mutualisms to climate change. Quantitative PCR was used here to diagnose the prevalence, seasonal variation, and abundances of Symbiodinium spp. within and between colonies of the coral, Alveopora japonica. Consistent with broader geographic sampling, only one species comprised 99.9 %, or greater, the population of symbionts in every sample. However, other Symbiodinium including the non-mutualistic species, Symbiodinium voratum, were often detected, but at estimated cell densities thousands-fold less than the dominant symbiont. The temporal variation in prevalence and abundances of these “background” Symbiodinium could not be definitively related to any particular environmental factor including seasonality and water chemistry. The prevalence (proportion detected among host samples), but not abundance, of S. voratum may weakly correspond to increases in environmental inorganic silica (SiO₂) and possibly nitrogen (NO₃). When multiple background Symbiodinium occurred within an individual polyp, the average cell densities were positively correlated, suggesting non-specific processes of cell sorting and retention by the animal. While these findings substantiate the existence of a broader, yet uncharacterized, diversity of Symbiodinium, we conclude that only those species which can occur in high abundance and are temporally stable are ultimately important to coral-dinoflagellate mutualisms. Many transient Symbiodinium spp., which occur only at trace abundances in the coral’s microbiome, belong to different functional guilds and likely have little, if any, importance to a coral’s physiology. The successful integration between host and symbiont into a stable functional unit should therefore be considered when defining host-symbiont specificity.</description><subject>Alveopora japonica</subject><subject>Animals</subject><subject>Anthozoa - parasitology</subject><subject>Biodiversity</subject><subject>Biomedical and Life Sciences</subject><subject>Climate change</subject><subject>coral reefs</subject><subject>corals</subject><subject>correlation</subject><subject>Dinoflagellida - classification</subject><subject>Dinoflagellida - isolation & purification</subject><subject>Dinoflagellida - physiology</subject><subject>Ecology</subject><subject>Environmental factors</subject><subject>Geoecology/Natural Processes</subject><subject>HOST MICROBE INTERACTIONS</subject><subject>hydrochemistry</subject><subject>Life Sciences</subject><subject>Microbial Ecology</subject><subject>Microbiology</subject><subject>microbiome</subject><subject>monitoring</subject><subject>Nature Conservation</subject><subject>nitrogen</subject><subject>Nitrogen - metabolism</subject><subject>Phylogeny</subject><subject>physiology</subject><subject>quantitative polymerase chain reaction</subject><subject>seasonal variation</subject><subject>Seasonal variations</subject><subject>Seasons</subject><subject>Silica</subject><subject>Symbiodinium</subject><subject>symbionts</subject><subject>Symbiosis</subject><subject>Water chemistry</subject><subject>Water Quality/Water Pollution</subject><issn>0095-3628</issn><issn>1432-184X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><recordid>eNqNks1u1DAUhS0EotPCA7AALHXDJsW-_s1yGFGKNBWLaSV2lpM4Iw-TeLAT0OwqngNerk-CS4YKsUCsruX7nXN1fYzQM0rOKCHqdSIEuC4IFQVRwAt4gGaUMyio5h8fohkhpSiYBH2EjlPaEEKVBPYYHYFUmpZcztC3y5AGvAxfi3k19o3ta4dvb76_sfWndQz55vbmB17tu8qHxvd-7HDa7c7wPDp8FW2f_BDiHtu-wRf2i8OXmensFp-PfT340Ofjyq973_r6l3Ub4sFt8DVehGi36Ql61Obinh7qCbo-f3u1uCiWH969X8yXRS2oGgpOZEmFo7QFC0yrUjtGKysarSRhQnIBlZS8Ble6vLdoG6aUaCXlVSmJYOwEvZp8dzF8Hl0aTOdT7bZb27swJkOVynopJf0fFDSTspQZPf0L3YQx5sUnigPoUmeKTlQdQ0rRtWYX80PFvaHE3GVppixNztLcZWkga14cnMeqc8294nd4GYAJSLnVr138Y_Q_XJ9Pok3K0d2bcq0AFOe5_3LqtzYYu44-mesVECrz7wEGeeOf2d-8dQ</recordid><startdate>20160401</startdate><enddate>20160401</enddate><creator>Lee, Moo Joon</creator><creator>Jeong, Hae Jin</creator><creator>Jang, Se Hyeon</creator><creator>Lee, Sung Yeon</creator><creator>Kang, Nam Seon</creator><creator>Lee, Kyung Ha</creator><creator>Kim, Hyung Seop</creator><creator>Wham, Drew C</creator><creator>LaJeunesse, Todd C</creator><general>Springer US</general><general>Springer Science + Business Media</general><general>Springer Nature B.V</general><scope>FBQ</scope><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>3V.</scope><scope>7QL</scope><scope>7SN</scope><scope>7T7</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</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>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>H95</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>L.G</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PCBAR</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20160401</creationdate><title>Most Low-Abundance “Background” Symbiodinium spp. Are Transitory and Have Minimal Functional Significance for Symbiotic Corals</title><author>Lee, Moo Joon ; Jeong, Hae Jin ; Jang, Se Hyeon ; Lee, Sung Yeon ; Kang, Nam Seon ; Lee, Kyung Ha ; Kim, Hyung Seop ; Wham, Drew C ; LaJeunesse, Todd C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c517t-406915e11f2a238798e31ba5d8760356452b664c2e9e0955fd3775f614b960533</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Alveopora japonica</topic><topic>Animals</topic><topic>Anthozoa - parasitology</topic><topic>Biodiversity</topic><topic>Biomedical and Life Sciences</topic><topic>Climate change</topic><topic>coral reefs</topic><topic>corals</topic><topic>correlation</topic><topic>Dinoflagellida - classification</topic><topic>Dinoflagellida - isolation & purification</topic><topic>Dinoflagellida - physiology</topic><topic>Ecology</topic><topic>Environmental factors</topic><topic>Geoecology/Natural Processes</topic><topic>HOST MICROBE INTERACTIONS</topic><topic>hydrochemistry</topic><topic>Life Sciences</topic><topic>Microbial Ecology</topic><topic>Microbiology</topic><topic>microbiome</topic><topic>monitoring</topic><topic>Nature Conservation</topic><topic>nitrogen</topic><topic>Nitrogen - metabolism</topic><topic>Phylogeny</topic><topic>physiology</topic><topic>quantitative polymerase chain reaction</topic><topic>seasonal variation</topic><topic>Seasonal variations</topic><topic>Seasons</topic><topic>Silica</topic><topic>Symbiodinium</topic><topic>symbionts</topic><topic>Symbiosis</topic><topic>Water chemistry</topic><topic>Water Quality/Water Pollution</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lee, Moo Joon</creatorcontrib><creatorcontrib>Jeong, Hae Jin</creatorcontrib><creatorcontrib>Jang, Se Hyeon</creatorcontrib><creatorcontrib>Lee, Sung Yeon</creatorcontrib><creatorcontrib>Kang, Nam Seon</creatorcontrib><creatorcontrib>Lee, Kyung Ha</creatorcontrib><creatorcontrib>Kim, Hyung Seop</creatorcontrib><creatorcontrib>Wham, Drew C</creatorcontrib><creatorcontrib>LaJeunesse, Todd C</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Complete (ProQuest Database)</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Earth, Atmospheric & Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Earth, Atmospheric & Aquatic Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Microbial ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lee, Moo Joon</au><au>Jeong, Hae Jin</au><au>Jang, Se Hyeon</au><au>Lee, Sung Yeon</au><au>Kang, Nam Seon</au><au>Lee, Kyung Ha</au><au>Kim, Hyung Seop</au><au>Wham, Drew C</au><au>LaJeunesse, Todd C</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Most Low-Abundance “Background” Symbiodinium spp. Are Transitory and Have Minimal Functional Significance for Symbiotic Corals</atitle><jtitle>Microbial ecology</jtitle><stitle>Microb Ecol</stitle><addtitle>Microb Ecol</addtitle><date>2016-04-01</date><risdate>2016</risdate><volume>71</volume><issue>3</issue><spage>771</spage><epage>783</epage><pages>771-783</pages><issn>0095-3628</issn><eissn>1432-184X</eissn><abstract>Speculation surrounds the importance of ecologically cryptic Symbiodinium spp. (dinoflagellates) that occur at low abundances in reef-building corals and in the surrounding environment. Evidence acquired from extensive sampling, long-term monitoring, and experimental manipulation can allow us to deduce the ecology and functional significance of these populations and whether they might contribute to the response of coral-dinoflagellate mutualisms to climate change. Quantitative PCR was used here to diagnose the prevalence, seasonal variation, and abundances of Symbiodinium spp. within and between colonies of the coral, Alveopora japonica. Consistent with broader geographic sampling, only one species comprised 99.9 %, or greater, the population of symbionts in every sample. However, other Symbiodinium including the non-mutualistic species, Symbiodinium voratum, were often detected, but at estimated cell densities thousands-fold less than the dominant symbiont. The temporal variation in prevalence and abundances of these “background” Symbiodinium could not be definitively related to any particular environmental factor including seasonality and water chemistry. The prevalence (proportion detected among host samples), but not abundance, of S. voratum may weakly correspond to increases in environmental inorganic silica (SiO₂) and possibly nitrogen (NO₃). When multiple background Symbiodinium occurred within an individual polyp, the average cell densities were positively correlated, suggesting non-specific processes of cell sorting and retention by the animal. While these findings substantiate the existence of a broader, yet uncharacterized, diversity of Symbiodinium, we conclude that only those species which can occur in high abundance and are temporally stable are ultimately important to coral-dinoflagellate mutualisms. Many transient Symbiodinium spp., which occur only at trace abundances in the coral’s microbiome, belong to different functional guilds and likely have little, if any, importance to a coral’s physiology. The successful integration between host and symbiont into a stable functional unit should therefore be considered when defining host-symbiont specificity.</abstract><cop>New York</cop><pub>Springer US</pub><pmid>26781946</pmid><doi>10.1007/s00248-015-0724-2</doi><tpages>13</tpages></addata></record> |
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subjects | Alveopora japonica Animals Anthozoa - parasitology Biodiversity Biomedical and Life Sciences Climate change coral reefs corals correlation Dinoflagellida - classification Dinoflagellida - isolation & purification Dinoflagellida - physiology Ecology Environmental factors Geoecology/Natural Processes HOST MICROBE INTERACTIONS hydrochemistry Life Sciences Microbial Ecology Microbiology microbiome monitoring Nature Conservation nitrogen Nitrogen - metabolism Phylogeny physiology quantitative polymerase chain reaction seasonal variation Seasonal variations Seasons Silica Symbiodinium symbionts Symbiosis Water chemistry Water Quality/Water Pollution |
title | Most Low-Abundance “Background” Symbiodinium spp. Are Transitory and Have Minimal Functional Significance for Symbiotic Corals |
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