Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance
This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitut...
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creator | Leles, S. G. Mitra, A. Flynn, K. J. Stoecker, D. K. Hansen, P. J. Calbet, A. McManus, G. B. Sanders, R. W. Caron, D. A. Not, F. Hallegraeff, G. M. Pitta, P. Raven, J. A. Johnson, M. D. Glibert, P. M. Våge, S. |
description | This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40–60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on ‘stolen’ chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research. |
doi_str_mv | 10.1098/rspb.2017.0664 |
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G. ; Mitra, A. ; Flynn, K. J. ; Stoecker, D. K. ; Hansen, P. J. ; Calbet, A. ; McManus, G. B. ; Sanders, R. W. ; Caron, D. A. ; Not, F. ; Hallegraeff, G. M. ; Pitta, P. ; Raven, J. A. ; Johnson, M. D. ; Glibert, P. M. ; Våge, S.</creator><creatorcontrib>Leles, S. G. ; Mitra, A. ; Flynn, K. J. ; Stoecker, D. K. ; Hansen, P. J. ; Calbet, A. ; McManus, G. B. ; Sanders, R. W. ; Caron, D. A. ; Not, F. ; Hallegraeff, G. M. ; Pitta, P. ; Raven, J. A. ; Johnson, M. D. ; Glibert, P. M. ; Våge, S.</creatorcontrib><description>This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40–60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on ‘stolen’ chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research.</description><edition>Royal Society (Great Britain)</edition><identifier>ISSN: 0962-8452</identifier><identifier>EISSN: 1471-2954</identifier><identifier>DOI: 10.1098/rspb.2017.0664</identifier><identifier>PMID: 28768886</identifier><language>eng</language><publisher>England: The Royal Society</publisher><subject>Abundance ; Acquired Phototrophy ; Biogeography ; Chloroplasts ; Chloroplasts - physiology ; Data processing ; Distribution patterns ; Ecology ; Endosymbionts ; Environmental Sciences ; Eukaryota ; Food Chain ; Food chains ; Food webs ; Functional groups ; Kleptoplasty ; Marine Protists ; Mixotrophy ; Oceans and Seas ; Photosymbiosis ; Photosynthesis ; Phototrophic Processes ; Phototrophy ; Plankton ; Plankton - physiology ; Plastids ; Prey ; Seasonal distribution ; Spatial distribution ; Spatio-Temporal Analysis ; Symbionts ; Symbiosis</subject><ispartof>Proceedings of the Royal Society. B, Biological sciences, 2017-08, Vol.284 (1860), p.20170664-20170664</ispartof><rights>2017 The Author(s)</rights><rights>2017 The Author(s).</rights><rights>Copyright The Royal Society Publishing Aug 16, 2017</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2017 The Author(s) 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c596t-9aea5594355f6ae2fc8a42d56fb324cce5d28af965b5d0efa07e435fe2e7d0ef3</citedby><cites>FETCH-LOGICAL-c596t-9aea5594355f6ae2fc8a42d56fb324cce5d28af965b5d0efa07e435fe2e7d0ef3</cites><orcidid>0000-0001-8464-7343 ; 0000-0001-7264-1059 ; 0000-0002-2768-1286 ; 0000-0001-5572-9331 ; 0000-0002-2789-3297 ; 0000-0003-1069-212X ; 0000-0001-6913-5884 ; 0000-0001-5690-1674 ; 0000-0002-9342-195X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5563798/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5563798/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28768886$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03971685$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Leles, S. G.</creatorcontrib><creatorcontrib>Mitra, A.</creatorcontrib><creatorcontrib>Flynn, K. J.</creatorcontrib><creatorcontrib>Stoecker, D. K.</creatorcontrib><creatorcontrib>Hansen, P. J.</creatorcontrib><creatorcontrib>Calbet, A.</creatorcontrib><creatorcontrib>McManus, G. B.</creatorcontrib><creatorcontrib>Sanders, R. W.</creatorcontrib><creatorcontrib>Caron, D. A.</creatorcontrib><creatorcontrib>Not, F.</creatorcontrib><creatorcontrib>Hallegraeff, G. M.</creatorcontrib><creatorcontrib>Pitta, P.</creatorcontrib><creatorcontrib>Raven, J. A.</creatorcontrib><creatorcontrib>Johnson, M. D.</creatorcontrib><creatorcontrib>Glibert, P. M.</creatorcontrib><creatorcontrib>Våge, S.</creatorcontrib><title>Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance</title><title>Proceedings of the Royal Society. B, Biological sciences</title><addtitle>Proc. R. Soc. B</addtitle><addtitle>Proc Biol Sci</addtitle><description>This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40–60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on ‘stolen’ chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. Mixotrophs with acquired phototrophy (NCMs) warrant greater recognition in marine research.</description><subject>Abundance</subject><subject>Acquired Phototrophy</subject><subject>Biogeography</subject><subject>Chloroplasts</subject><subject>Chloroplasts - physiology</subject><subject>Data processing</subject><subject>Distribution patterns</subject><subject>Ecology</subject><subject>Endosymbionts</subject><subject>Environmental Sciences</subject><subject>Eukaryota</subject><subject>Food Chain</subject><subject>Food chains</subject><subject>Food webs</subject><subject>Functional groups</subject><subject>Kleptoplasty</subject><subject>Marine Protists</subject><subject>Mixotrophy</subject><subject>Oceans and Seas</subject><subject>Photosymbiosis</subject><subject>Photosynthesis</subject><subject>Phototrophic Processes</subject><subject>Phototrophy</subject><subject>Plankton</subject><subject>Plankton - physiology</subject><subject>Plastids</subject><subject>Prey</subject><subject>Seasonal distribution</subject><subject>Spatial distribution</subject><subject>Spatio-Temporal Analysis</subject><subject>Symbionts</subject><subject>Symbiosis</subject><issn>0962-8452</issn><issn>1471-2954</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kc1v1DAQxSMEokvhyhFF4gKH3dqO7dgXpLYCirRSER9ny3HGG5ddO7WTRctfj8MupS2Ck2XPb-a98SuK5xgtMJLiJKa-WRCE6wXinD4oZpjWeE4kow-LGZKczAVl5Kh4ktIVQkgywR4XR0TUXAjBZ4W_NKC9M2Ufw-DSkMrvbujK1lkLEfxQ2hA3qQy21OZ6dBHasu_CEIYY-m6XudSv9a40wQ9Rp8H5Vdm4sIKwirrvHKRS-7bUzehb7Q08LR5ZvU7w7HAeF1_fvf1yfjFfXr7_cH66nBsm-TCXGjRjklaMWa6BWCM0JS3jtqkINQZYS4S2krOGtQisRjVk2AKBerpXx8Wb_dx-bDbQGpjsrVUf3UbHnQraqbsV7zq1ClvFGK9qKfKA1_sB3b22i9Olmt5QJWvMBdvizL46iMVwPUIa1MYlA-u19hDGpLAkTGSvhGf05T30KozR56_IlKAVrysmM7XYUyaGlCLYGwcYqSl2NcWuptjVFHtueHF73Rv8d84Z-LYHYthlsWAcDLs_2p8-fzzbEkEdFhwpJCqMakqIUD9cf9ASVLmURlC_kLv6f9up_qf2jyV-AhRy4Tw</recordid><startdate>20170816</startdate><enddate>20170816</enddate><creator>Leles, S. 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G. ; Mitra, A. ; Flynn, K. J. ; Stoecker, D. K. ; Hansen, P. J. ; Calbet, A. ; McManus, G. B. ; Sanders, R. W. ; Caron, D. A. ; Not, F. ; Hallegraeff, G. M. ; Pitta, P. ; Raven, J. A. ; Johnson, M. D. ; Glibert, P. 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B</stitle><addtitle>Proc Biol Sci</addtitle><date>2017-08-16</date><risdate>2017</risdate><volume>284</volume><issue>1860</issue><spage>20170664</spage><epage>20170664</epage><pages>20170664-20170664</pages><issn>0962-8452</issn><eissn>1471-2954</eissn><abstract>This first comprehensive analysis of the global biogeography of marine protistan plankton with acquired phototrophy shows these mixotrophic organisms to be ubiquitous and abundant; however, their biogeography differs markedly between different functional groups. These mixotrophs, lacking a constitutive capacity for photosynthesis (i.e. non-constitutive mixotrophs, NCMs), acquire their phototrophic potential through either integration of prey-plastids or through endosymbiotic associations with photosynthetic microbes. Analysis of field data reveals that 40–60% of plankton traditionally labelled as (non-phototrophic) microzooplankton are actually NCMs, employing acquired phototrophy in addition to phagotrophy. Specialist NCMs acquire chloroplasts or endosymbionts from specific prey, while generalist NCMs obtain chloroplasts from a variety of prey. These contrasting functional types of NCMs exhibit distinct seasonal and spatial global distribution patterns. Mixotrophs reliant on ‘stolen’ chloroplasts, controlled by prey diversity and abundance, dominate in high-biomass areas. Mixotrophs harbouring intact symbionts are present in all waters and dominate particularly in oligotrophic open ocean systems. The contrasting temporal and spatial patterns of distribution of different mixotroph functional types across the oceanic provinces, as revealed in this study, challenges traditional interpretations of marine food web structures. 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subjects | Abundance Acquired Phototrophy Biogeography Chloroplasts Chloroplasts - physiology Data processing Distribution patterns Ecology Endosymbionts Environmental Sciences Eukaryota Food Chain Food chains Food webs Functional groups Kleptoplasty Marine Protists Mixotrophy Oceans and Seas Photosymbiosis Photosynthesis Phototrophic Processes Phototrophy Plankton Plankton - physiology Plastids Prey Seasonal distribution Spatial distribution Spatio-Temporal Analysis Symbionts Symbiosis |
title | Oceanic protists with different forms of acquired phototrophy display contrasting biogeographies and abundance |
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