Influence of light on the infection of Aureococcus anophagefferens CCMP 1984 by a "giant virus"
The pelagophyte Aureococcus anophagefferens has caused recurrent brown tide blooms along the northeast coast of the United States since the mid-1980's, and more recently spread to other regions of the globe. These blooms, due to the high cell densities, are associated with severe light attenuat...
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description | The pelagophyte Aureococcus anophagefferens has caused recurrent brown tide blooms along the northeast coast of the United States since the mid-1980's, and more recently spread to other regions of the globe. These blooms, due to the high cell densities, are associated with severe light attenuation that destroys the sea grass beds which provide the basis for many fisheries. Data collected by transmission electron microscopy, PCR, and metatranscriptomic studies of the blooms, support the hypothesis that large dsDNA viruses play a role in bloom dynamics. While a large (~140 nm) icosahedral virus, with a 371 kbp genome, was first isolated more than a decade ago, the constraints imposed by environmental parameters on bloom infection dynamics by Aureococcus anophagefferens Virus, (AaV) remain unknown. To investigate the role light plays in infection by this virus, we acclimated A. anophagefferens to light intensities of 30 (low), 60 (medium) or 90 μmol photons m-2 s-1 (high) and infected cultures at these irradiance levels. Moreover, we completed light shift experiments where acclimated cultures were exposed to even lower light intensities (0, 5, and 15 μmol photons m-2 s-1) consistent with irradiance found during the peak of the bloom when cell concentrations are highest. The abundance of viruses produced per lytic event (burst size) was lower in the low irradiance acclimated cultures compared to the medium and high acclimated cultures. Transferring infected cultures to more-limiting light availabilities further decreased burst size and increased the length of time it took for cultures to lyse, regardless of acclimation irradiance level. A hypothetical mechanism for the reduced efficiency of the infection cycle in low light due to ribosome biogenesis was predicted from pre-existing transcriptomes. Overall, these studies provide a framework for understanding light effects on infection dynamics over the course of the summer months when A. anophagefferens blooms occur. |
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Roger</contributor><creatorcontrib>Gann, Eric R ; Gainer, P Jackson ; Reynolds, Todd B ; Wilhelm, Steven W ; Anderson, O. Roger</creatorcontrib><description>The pelagophyte Aureococcus anophagefferens has caused recurrent brown tide blooms along the northeast coast of the United States since the mid-1980's, and more recently spread to other regions of the globe. These blooms, due to the high cell densities, are associated with severe light attenuation that destroys the sea grass beds which provide the basis for many fisheries. Data collected by transmission electron microscopy, PCR, and metatranscriptomic studies of the blooms, support the hypothesis that large dsDNA viruses play a role in bloom dynamics. While a large (~140 nm) icosahedral virus, with a 371 kbp genome, was first isolated more than a decade ago, the constraints imposed by environmental parameters on bloom infection dynamics by Aureococcus anophagefferens Virus, (AaV) remain unknown. To investigate the role light plays in infection by this virus, we acclimated A. anophagefferens to light intensities of 30 (low), 60 (medium) or 90 μmol photons m-2 s-1 (high) and infected cultures at these irradiance levels. Moreover, we completed light shift experiments where acclimated cultures were exposed to even lower light intensities (0, 5, and 15 μmol photons m-2 s-1) consistent with irradiance found during the peak of the bloom when cell concentrations are highest. The abundance of viruses produced per lytic event (burst size) was lower in the low irradiance acclimated cultures compared to the medium and high acclimated cultures. Transferring infected cultures to more-limiting light availabilities further decreased burst size and increased the length of time it took for cultures to lyse, regardless of acclimation irradiance level. A hypothetical mechanism for the reduced efficiency of the infection cycle in low light due to ribosome biogenesis was predicted from pre-existing transcriptomes. Overall, these studies provide a framework for understanding light effects on infection dynamics over the course of the summer months when A. anophagefferens blooms occur.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0226758</identifier><identifier>PMID: 31899921</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acclimation ; Acclimatization ; Algae ; Atoms & subatomic particles ; Attenuation ; Aureococcus anophagefferens ; Biology and Life Sciences ; Biosynthesis ; Brown tides ; Burst size ; Cultures ; DNA Virus Infections - virology ; Electron microscopy ; Environmental parameters ; Experiments ; Fisheries ; Genomes ; Genomics ; Giant Viruses - physiology ; Health aspects ; Host-Pathogen Interactions ; Icosahedral phase ; Infections ; Influence ; Irradiance ; Light ; Light attenuation ; Light effects ; Light levels ; Luminous intensity ; Medical research ; Microalgae - growth & development ; Microalgae - radiation effects ; Microalgae - virology ; Microscopy ; Photons ; Physical Sciences ; Population ; Research and Analysis Methods ; Scientific equipment industry ; Transmission electron microscopy ; Viral infections ; Virus Replication - radiation effects ; Viruses ; Water quality</subject><ispartof>PloS one, 2020-01, Vol.15 (1), p.e0226758-e0226758</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Gann et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Roger</contributor><creatorcontrib>Gann, Eric R</creatorcontrib><creatorcontrib>Gainer, P Jackson</creatorcontrib><creatorcontrib>Reynolds, Todd B</creatorcontrib><creatorcontrib>Wilhelm, Steven W</creatorcontrib><title>Influence of light on the infection of Aureococcus anophagefferens CCMP 1984 by a "giant virus"</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The pelagophyte Aureococcus anophagefferens has caused recurrent brown tide blooms along the northeast coast of the United States since the mid-1980's, and more recently spread to other regions of the globe. These blooms, due to the high cell densities, are associated with severe light attenuation that destroys the sea grass beds which provide the basis for many fisheries. Data collected by transmission electron microscopy, PCR, and metatranscriptomic studies of the blooms, support the hypothesis that large dsDNA viruses play a role in bloom dynamics. While a large (~140 nm) icosahedral virus, with a 371 kbp genome, was first isolated more than a decade ago, the constraints imposed by environmental parameters on bloom infection dynamics by Aureococcus anophagefferens Virus, (AaV) remain unknown. To investigate the role light plays in infection by this virus, we acclimated A. anophagefferens to light intensities of 30 (low), 60 (medium) or 90 μmol photons m-2 s-1 (high) and infected cultures at these irradiance levels. Moreover, we completed light shift experiments where acclimated cultures were exposed to even lower light intensities (0, 5, and 15 μmol photons m-2 s-1) consistent with irradiance found during the peak of the bloom when cell concentrations are highest. The abundance of viruses produced per lytic event (burst size) was lower in the low irradiance acclimated cultures compared to the medium and high acclimated cultures. Transferring infected cultures to more-limiting light availabilities further decreased burst size and increased the length of time it took for cultures to lyse, regardless of acclimation irradiance level. A hypothetical mechanism for the reduced efficiency of the infection cycle in low light due to ribosome biogenesis was predicted from pre-existing transcriptomes. 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growth & development</subject><subject>Microalgae - radiation effects</subject><subject>Microalgae - virology</subject><subject>Microscopy</subject><subject>Photons</subject><subject>Physical Sciences</subject><subject>Population</subject><subject>Research and Analysis Methods</subject><subject>Scientific equipment industry</subject><subject>Transmission electron microscopy</subject><subject>Viral infections</subject><subject>Virus Replication - radiation effects</subject><subject>Viruses</subject><subject>Water quality</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk1uL1DAUx4so7rr6DUTDCqIPM-bSps2LMAxeBlZWvL2GNDlpO3SSsWkX99ub7nSXqeyDJJDb7_xPcnJOkjwneElYTt5t_dA51S733sESU8rzrHiQnBLB6IJTzB4ezU-SJyFsMc5Ywfnj5ISRQghByWkiN862AzgNyFvUNlXdI-9QXwNqnAXdN3EVT1ZDB157rYeAlPP7WlVgLXTgAlqvv3xFRBQpKq-RQudVo1yPrppuCOdPk0dWtQGeTeNZ8vPjhx_rz4uLy0-b9epiobmg_aLgNisNFDotRJYZRjkApzQjRWloDpgCK9IyLwVjBow1oPPc5JYZlmXAUsrOkpcH3X3rg5xiEyRlLPYszXEkNgfCeLWV-67Zqe5aetXImw3fVVJ1faNbkNZqYVPCDddZWpaqxHlJdUoLZiHLRR613k_ehnIHRoPrO9XOROcnrqll5a8kFykRVESBN5NA538PEHq5a4KGtlUO_HBzb8YxF3z09eof9P7XTVSl4gPi1_noV4-icsUJZgKTYqSW91CxGdg1OiaSbeL-zODtzCAyPfzpKzWEIDffv_0_e_lrzr4-YmtQbV8H3w5juoU5mB5A3fkQOrB3QSZYjnVwGw051oGc6iCavTj-oDuj28RnfwGDcgEH</recordid><startdate>20200103</startdate><enddate>20200103</enddate><creator>Gann, Eric R</creator><creator>Gainer, P Jackson</creator><creator>Reynolds, Todd B</creator><creator>Wilhelm, Steven W</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-9410-7949</orcidid><orcidid>https://orcid.org/0000-0001-6283-8077</orcidid></search><sort><creationdate>20200103</creationdate><title>Influence of light on the infection of Aureococcus anophagefferens CCMP 1984 by a "giant virus"</title><author>Gann, Eric R ; Gainer, P Jackson ; Reynolds, Todd B ; Wilhelm, Steven W</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-86f5bde8c48955d326ee622518bd27e02e384b7b933dedfdec77d7f3d355e3423</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Acclimation</topic><topic>Acclimatization</topic><topic>Algae</topic><topic>Atoms & subatomic particles</topic><topic>Attenuation</topic><topic>Aureococcus anophagefferens</topic><topic>Biology and Life Sciences</topic><topic>Biosynthesis</topic><topic>Brown tides</topic><topic>Burst size</topic><topic>Cultures</topic><topic>DNA Virus Infections - virology</topic><topic>Electron microscopy</topic><topic>Environmental parameters</topic><topic>Experiments</topic><topic>Fisheries</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Giant Viruses - physiology</topic><topic>Health aspects</topic><topic>Host-Pathogen Interactions</topic><topic>Icosahedral phase</topic><topic>Infections</topic><topic>Influence</topic><topic>Irradiance</topic><topic>Light</topic><topic>Light attenuation</topic><topic>Light effects</topic><topic>Light levels</topic><topic>Luminous intensity</topic><topic>Medical research</topic><topic>Microalgae - growth & development</topic><topic>Microalgae - radiation effects</topic><topic>Microalgae - virology</topic><topic>Microscopy</topic><topic>Photons</topic><topic>Physical Sciences</topic><topic>Population</topic><topic>Research and Analysis Methods</topic><topic>Scientific equipment industry</topic><topic>Transmission electron microscopy</topic><topic>Viral infections</topic><topic>Virus Replication - radiation effects</topic><topic>Viruses</topic><topic>Water quality</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gann, Eric R</creatorcontrib><creatorcontrib>Gainer, P Jackson</creatorcontrib><creatorcontrib>Reynolds, Todd B</creatorcontrib><creatorcontrib>Wilhelm, Steven W</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology 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>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>Proquest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</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>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Roger</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Influence of light on the infection of Aureococcus anophagefferens CCMP 1984 by a "giant virus"</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2020-01-03</date><risdate>2020</risdate><volume>15</volume><issue>1</issue><spage>e0226758</spage><epage>e0226758</epage><pages>e0226758-e0226758</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>The pelagophyte Aureococcus anophagefferens has caused recurrent brown tide blooms along the northeast coast of the United States since the mid-1980's, and more recently spread to other regions of the globe. These blooms, due to the high cell densities, are associated with severe light attenuation that destroys the sea grass beds which provide the basis for many fisheries. Data collected by transmission electron microscopy, PCR, and metatranscriptomic studies of the blooms, support the hypothesis that large dsDNA viruses play a role in bloom dynamics. While a large (~140 nm) icosahedral virus, with a 371 kbp genome, was first isolated more than a decade ago, the constraints imposed by environmental parameters on bloom infection dynamics by Aureococcus anophagefferens Virus, (AaV) remain unknown. To investigate the role light plays in infection by this virus, we acclimated A. anophagefferens to light intensities of 30 (low), 60 (medium) or 90 μmol photons m-2 s-1 (high) and infected cultures at these irradiance levels. Moreover, we completed light shift experiments where acclimated cultures were exposed to even lower light intensities (0, 5, and 15 μmol photons m-2 s-1) consistent with irradiance found during the peak of the bloom when cell concentrations are highest. The abundance of viruses produced per lytic event (burst size) was lower in the low irradiance acclimated cultures compared to the medium and high acclimated cultures. Transferring infected cultures to more-limiting light availabilities further decreased burst size and increased the length of time it took for cultures to lyse, regardless of acclimation irradiance level. A hypothetical mechanism for the reduced efficiency of the infection cycle in low light due to ribosome biogenesis was predicted from pre-existing transcriptomes. Overall, these studies provide a framework for understanding light effects on infection dynamics over the course of the summer months when A. anophagefferens blooms occur.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>31899921</pmid><doi>10.1371/journal.pone.0226758</doi><tpages>e0226758</tpages><orcidid>https://orcid.org/0000-0001-9410-7949</orcidid><orcidid>https://orcid.org/0000-0001-6283-8077</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Acclimation Acclimatization Algae Atoms & subatomic particles Attenuation Aureococcus anophagefferens Biology and Life Sciences Biosynthesis Brown tides Burst size Cultures DNA Virus Infections - virology Electron microscopy Environmental parameters Experiments Fisheries Genomes Genomics Giant Viruses - physiology Health aspects Host-Pathogen Interactions Icosahedral phase Infections Influence Irradiance Light Light attenuation Light effects Light levels Luminous intensity Medical research Microalgae - growth & development Microalgae - radiation effects Microalgae - virology Microscopy Photons Physical Sciences Population Research and Analysis Methods Scientific equipment industry Transmission electron microscopy Viral infections Virus Replication - radiation effects Viruses Water quality |
title | Influence of light on the infection of Aureococcus anophagefferens CCMP 1984 by a "giant virus" |
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