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Viral ecogenomics across the Porifera

Cecília Pascelli, Patrick W. Laffy, Emmanuelle Botté, Marija Kupresanin, Thomas Rattei, Miguel Lurgi Rivera Orcid Logo, Timothy Ravasi, Nicole S. Webster

Microbiome, Volume: 8, Issue: 1

Swansea University Author: Miguel Lurgi Rivera Orcid Logo

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Abstract

BackgroundViruses directly affect the most important biological processes in the ocean via their regulation of prokaryotic and eukaryotic populations. Marine sponges form stable symbiotic partnerships with a wide diversity of microorganisms and this high symbiont complexity makes them an ideal model...

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Published in: Microbiome
ISSN: 2049-2618
Published: Springer Science and Business Media LLC 2020
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fullrecord <?xml version="1.0"?><rfc1807><datestamp>2021-03-08T13:47:51.0749512</datestamp><bib-version>v2</bib-version><id>55350</id><entry>2020-10-06</entry><title>Viral ecogenomics across the Porifera</title><swanseaauthors><author><sid>947df89d116a1ab75515e421089e0443</sid><ORCID>0000-0001-9891-895X</ORCID><firstname>Miguel</firstname><surname>Lurgi Rivera</surname><name>Miguel Lurgi Rivera</name><active>true</active><ethesisStudent>false</ethesisStudent></author></swanseaauthors><date>2020-10-06</date><deptcode>SBI</deptcode><abstract>BackgroundViruses directly affect the most important biological processes in the ocean via their regulation of prokaryotic and eukaryotic populations. Marine sponges form stable symbiotic partnerships with a wide diversity of microorganisms and this high symbiont complexity makes them an ideal model for studying viral ecology. Here, we used morphological and molecular approaches to illuminate the diversity and function of viruses inhabiting nine sponge species from the Great Barrier Reef and seven from the Red Sea.ResultsViromic sequencing revealed host-specific and site-specific patterns in the viral assemblages, with all sponge species dominated by the bacteriophage order Caudovirales but also containing variable representation from the nucleocytoplasmic large DNA virus families Mimiviridae, Marseilleviridae, Phycodnaviridae, Ascoviridae, Iridoviridae, Asfarviridae and Poxviridae. Whilst core viral functions related to replication, infection and structure were largely consistent across the sponge viromes, functional profiles varied significantly between species and sites largely due to differential representation of putative auxiliary metabolic genes (AMGs) and accessory genes, including those associated with herbicide resistance, heavy metal resistance and nylon degradation. Furthermore, putative AMGs varied with the composition and abundance of the sponge-associated microbiome. For instance, genes associated with antimicrobial activity were enriched in low microbial abundance sponges, genes associated with nitrogen metabolism were enriched in high microbial abundance sponges and genes related to cellulose biosynthesis were enriched in species that host photosynthetic symbionts.ConclusionsOur results highlight the diverse functional roles that viruses can play in marine sponges and are consistent with our current understanding of sponge ecology. Differential representation of putative viral AMGs and accessory genes across sponge species illustrate the diverse suite of beneficial roles viruses can play in the functional ecology of these complex reef holobionts.</abstract><type>Journal Article</type><journal>Microbiome</journal><volume>8</volume><journalNumber>1</journalNumber><paginationStart/><paginationEnd/><publisher>Springer Science and Business Media LLC</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint/><issnElectronic>2049-2618</issnElectronic><keywords>Viromics, Viral ecology, Functional diversity, AMGs, Coral reef sponges</keywords><publishedDay>1</publishedDay><publishedMonth>12</publishedMonth><publishedYear>2020</publishedYear><publishedDate>2020-12-01</publishedDate><doi>10.1186/s40168-020-00919-5</doi><url/><notes/><college>COLLEGE NANME</college><department>Biosciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>SBI</DepartmentCode><institution>Swansea University</institution><apcterm/><lastEdited>2021-03-08T13:47:51.0749512</lastEdited><Created>2020-10-06T14:31:57.3893730</Created><path><level id="1">Faculty of Science and Engineering</level><level id="2">School of Biosciences, Geography and Physics - Biosciences</level></path><authors><author><firstname>Cec&#xED;lia</firstname><surname>Pascelli</surname><order>1</order></author><author><firstname>Patrick W.</firstname><surname>Laffy</surname><order>2</order></author><author><firstname>Emmanuelle</firstname><surname>Bott&#xE9;</surname><order>3</order></author><author><firstname>Marija</firstname><surname>Kupresanin</surname><order>4</order></author><author><firstname>Thomas</firstname><surname>Rattei</surname><order>5</order></author><author><firstname>Miguel</firstname><surname>Lurgi Rivera</surname><orcid>0000-0001-9891-895X</orcid><order>6</order></author><author><firstname>Timothy</firstname><surname>Ravasi</surname><order>7</order></author><author><firstname>Nicole S.</firstname><surname>Webster</surname><order>8</order></author></authors><documents><document><filename>55350__18340__5cd0b6e34518485e8cd3cf0d7d387d35.pdf</filename><originalFilename>s40168-020-00919-5.pdf</originalFilename><uploaded>2020-10-06T14:39:51.8939731</uploaded><type>Output</type><contentLength>4238364</contentLength><contentType>application/pdf</contentType><version>Version of Record</version><cronfaStatus>true</cronfaStatus><documentNotes>&#xA9; The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License</documentNotes><copyrightCorrect>true</copyrightCorrect><language>eng</language><licence>http://creativecommons.org/licenses/by/4.0/</licence></document></documents><OutputDurs/></rfc1807>
spelling 2021-03-08T13:47:51.0749512 v2 55350 2020-10-06 Viral ecogenomics across the Porifera 947df89d116a1ab75515e421089e0443 0000-0001-9891-895X Miguel Lurgi Rivera Miguel Lurgi Rivera true false 2020-10-06 SBI BackgroundViruses directly affect the most important biological processes in the ocean via their regulation of prokaryotic and eukaryotic populations. Marine sponges form stable symbiotic partnerships with a wide diversity of microorganisms and this high symbiont complexity makes them an ideal model for studying viral ecology. Here, we used morphological and molecular approaches to illuminate the diversity and function of viruses inhabiting nine sponge species from the Great Barrier Reef and seven from the Red Sea.ResultsViromic sequencing revealed host-specific and site-specific patterns in the viral assemblages, with all sponge species dominated by the bacteriophage order Caudovirales but also containing variable representation from the nucleocytoplasmic large DNA virus families Mimiviridae, Marseilleviridae, Phycodnaviridae, Ascoviridae, Iridoviridae, Asfarviridae and Poxviridae. Whilst core viral functions related to replication, infection and structure were largely consistent across the sponge viromes, functional profiles varied significantly between species and sites largely due to differential representation of putative auxiliary metabolic genes (AMGs) and accessory genes, including those associated with herbicide resistance, heavy metal resistance and nylon degradation. Furthermore, putative AMGs varied with the composition and abundance of the sponge-associated microbiome. For instance, genes associated with antimicrobial activity were enriched in low microbial abundance sponges, genes associated with nitrogen metabolism were enriched in high microbial abundance sponges and genes related to cellulose biosynthesis were enriched in species that host photosynthetic symbionts.ConclusionsOur results highlight the diverse functional roles that viruses can play in marine sponges and are consistent with our current understanding of sponge ecology. Differential representation of putative viral AMGs and accessory genes across sponge species illustrate the diverse suite of beneficial roles viruses can play in the functional ecology of these complex reef holobionts. Journal Article Microbiome 8 1 Springer Science and Business Media LLC 2049-2618 Viromics, Viral ecology, Functional diversity, AMGs, Coral reef sponges 1 12 2020 2020-12-01 10.1186/s40168-020-00919-5 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University 2021-03-08T13:47:51.0749512 2020-10-06T14:31:57.3893730 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Cecília Pascelli 1 Patrick W. Laffy 2 Emmanuelle Botté 3 Marija Kupresanin 4 Thomas Rattei 5 Miguel Lurgi Rivera 0000-0001-9891-895X 6 Timothy Ravasi 7 Nicole S. Webster 8 55350__18340__5cd0b6e34518485e8cd3cf0d7d387d35.pdf s40168-020-00919-5.pdf 2020-10-06T14:39:51.8939731 Output 4238364 application/pdf Version of Record true © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License true eng http://creativecommons.org/licenses/by/4.0/
title Viral ecogenomics across the Porifera
spellingShingle Viral ecogenomics across the Porifera
Miguel Lurgi Rivera
title_short Viral ecogenomics across the Porifera
title_full Viral ecogenomics across the Porifera
title_fullStr Viral ecogenomics across the Porifera
title_full_unstemmed Viral ecogenomics across the Porifera
title_sort Viral ecogenomics across the Porifera
author_id_str_mv 947df89d116a1ab75515e421089e0443
author_id_fullname_str_mv 947df89d116a1ab75515e421089e0443_***_Miguel Lurgi Rivera
author Miguel Lurgi Rivera
author2 Cecília Pascelli
Patrick W. Laffy
Emmanuelle Botté
Marija Kupresanin
Thomas Rattei
Miguel Lurgi Rivera
Timothy Ravasi
Nicole S. Webster
format Journal article
container_title Microbiome
container_volume 8
container_issue 1
publishDate 2020
institution Swansea University
issn 2049-2618
doi_str_mv 10.1186/s40168-020-00919-5
publisher Springer Science and Business Media LLC
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
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description BackgroundViruses directly affect the most important biological processes in the ocean via their regulation of prokaryotic and eukaryotic populations. Marine sponges form stable symbiotic partnerships with a wide diversity of microorganisms and this high symbiont complexity makes them an ideal model for studying viral ecology. Here, we used morphological and molecular approaches to illuminate the diversity and function of viruses inhabiting nine sponge species from the Great Barrier Reef and seven from the Red Sea.ResultsViromic sequencing revealed host-specific and site-specific patterns in the viral assemblages, with all sponge species dominated by the bacteriophage order Caudovirales but also containing variable representation from the nucleocytoplasmic large DNA virus families Mimiviridae, Marseilleviridae, Phycodnaviridae, Ascoviridae, Iridoviridae, Asfarviridae and Poxviridae. Whilst core viral functions related to replication, infection and structure were largely consistent across the sponge viromes, functional profiles varied significantly between species and sites largely due to differential representation of putative auxiliary metabolic genes (AMGs) and accessory genes, including those associated with herbicide resistance, heavy metal resistance and nylon degradation. Furthermore, putative AMGs varied with the composition and abundance of the sponge-associated microbiome. For instance, genes associated with antimicrobial activity were enriched in low microbial abundance sponges, genes associated with nitrogen metabolism were enriched in high microbial abundance sponges and genes related to cellulose biosynthesis were enriched in species that host photosynthetic symbionts.ConclusionsOur results highlight the diverse functional roles that viruses can play in marine sponges and are consistent with our current understanding of sponge ecology. Differential representation of putative viral AMGs and accessory genes across sponge species illustrate the diverse suite of beneficial roles viruses can play in the functional ecology of these complex reef holobionts.
published_date 2020-12-01T04:09:29Z
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