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Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans
The abundance, genetic diversity, and crucial ecological and evolutionary roles of marine phages have prompted a large number of metagenomic studies. However, obtaining a thorough understanding of marine phages has been hampered by the low number of phage isolates infecting major bacterial groups ot...
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Published in: | Proceedings of the National Academy of Sciences - PNAS 2013-07, Vol.110 (30), p.12343-12348 |
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creator | Kang, Ilnam Oh, Hyun-Myung Kang, Dongmin Cho, Jang-Cheon |
description | The abundance, genetic diversity, and crucial ecological and evolutionary roles of marine phages have prompted a large number of metagenomic studies. However, obtaining a thorough understanding of marine phages has been hampered by the low number of phage isolates infecting major bacterial groups other than cyanophages and pelagiphages. Therefore, there is an urgent requirement for the isolation of phages that infect abundant marine bacterial groups. In this study, we isolated and characterized HMO-2011, a phage infecting a bacterium of the SAR116 clade, one of the most abundant marine bacterial lineages. HMO-2011, which infects “ Candidatus Puniceispirillum marinum” strain IMCC1322, has an ∼55-kb dsDNA genome that harbors many genes with novel features rarely found in cultured organisms, including genes encoding a DNA polymerase with a partial DnaJ central domain and an atypical methanesulfonate monooxygenase. Furthermore, homologs of nearly all HMO-2011 genes were predominantly found in marine metagenomes rather than cultured organisms, suggesting the novelty of HMO-2011 and the prevalence of this phage type in the oceans. A significant number of the viral metagenome sequences obtained from the ocean surface were best assigned to the HMO-2011 genome. The number of reads assigned to HMO-2011 accounted for 10.3%–25.3% of the total reads assigned to viruses in seven viromes from the Pacific and Indian Oceans, making the HMO-2011 genome the most or second-most frequently assigned viral genome. Given its ability to infect the abundant SAR116 clade and its widespread distribution, Puniceispirillum phage HMO-2011 could be an important resource for marine virus research. |
doi_str_mv | 10.1073/pnas.1219930110 |
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However, obtaining a thorough understanding of marine phages has been hampered by the low number of phage isolates infecting major bacterial groups other than cyanophages and pelagiphages. Therefore, there is an urgent requirement for the isolation of phages that infect abundant marine bacterial groups. In this study, we isolated and characterized HMO-2011, a phage infecting a bacterium of the SAR116 clade, one of the most abundant marine bacterial lineages. HMO-2011, which infects “ Candidatus Puniceispirillum marinum” strain IMCC1322, has an ∼55-kb dsDNA genome that harbors many genes with novel features rarely found in cultured organisms, including genes encoding a DNA polymerase with a partial DnaJ central domain and an atypical methanesulfonate monooxygenase. Furthermore, homologs of nearly all HMO-2011 genes were predominantly found in marine metagenomes rather than cultured organisms, suggesting the novelty of HMO-2011 and the prevalence of this phage type in the oceans. A significant number of the viral metagenome sequences obtained from the ocean surface were best assigned to the HMO-2011 genome. The number of reads assigned to HMO-2011 accounted for 10.3%–25.3% of the total reads assigned to viruses in seven viromes from the Pacific and Indian Oceans, making the HMO-2011 genome the most or second-most frequently assigned viral genome. Given its ability to infect the abundant SAR116 clade and its widespread distribution, Puniceispirillum phage HMO-2011 could be an important resource for marine virus research.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1219930110</identifier><identifier>PMID: 23798439</identifier><identifier>CODEN: PNASA6</identifier><language>eng</language><publisher>Washington, DC: National Academy of Sciences</publisher><subject>Amino Acid Sequence ; Animal and plant ecology ; Animal, plant and microbial ecology ; Bacteria ; Bacteriophages ; Bacteriophages - enzymology ; Bacteriophages - genetics ; Bacteriophages - isolation & purification ; Biological and medical sciences ; Biological Sciences ; DNA polymerase ; DNA-Directed DNA Polymerase - chemistry ; DNA-Directed DNA Polymerase - metabolism ; Fundamental and applied biological sciences. Psychology ; Genes ; Genome, Viral ; Genomes ; Genomics ; Marine Biology ; Metagenomics ; Microbiology ; Molecular Sequence Data ; Mutation ; Oceans ; Oceans and Seas ; Open Reading Frames ; Protein metabolism ; Sea water ecosystems ; Sequence Homology, Amino Acid ; Synecology ; Systematics ; Virology ; Viruses ; Water Microbiology</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2013-07, Vol.110 (30), p.12343-12348</ispartof><rights>copyright © 1993-2008 National Academy of Sciences of the United States of America</rights><rights>2015 INIST-CNRS</rights><rights>Copyright National Academy of Sciences Jul 23, 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c522t-a88d27931666b07029a6fde65916e32394db6ab3ffaea791980d42966e15834b3</citedby><cites>FETCH-LOGICAL-c522t-a88d27931666b07029a6fde65916e32394db6ab3ffaea791980d42966e15834b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/110/30.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/42712593$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/42712593$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793,58238,58471</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=27569204$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23798439$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kang, Ilnam</creatorcontrib><creatorcontrib>Oh, Hyun-Myung</creatorcontrib><creatorcontrib>Kang, Dongmin</creatorcontrib><creatorcontrib>Cho, Jang-Cheon</creatorcontrib><title>Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The abundance, genetic diversity, and crucial ecological and evolutionary roles of marine phages have prompted a large number of metagenomic studies. However, obtaining a thorough understanding of marine phages has been hampered by the low number of phage isolates infecting major bacterial groups other than cyanophages and pelagiphages. Therefore, there is an urgent requirement for the isolation of phages that infect abundant marine bacterial groups. In this study, we isolated and characterized HMO-2011, a phage infecting a bacterium of the SAR116 clade, one of the most abundant marine bacterial lineages. HMO-2011, which infects “ Candidatus Puniceispirillum marinum” strain IMCC1322, has an ∼55-kb dsDNA genome that harbors many genes with novel features rarely found in cultured organisms, including genes encoding a DNA polymerase with a partial DnaJ central domain and an atypical methanesulfonate monooxygenase. Furthermore, homologs of nearly all HMO-2011 genes were predominantly found in marine metagenomes rather than cultured organisms, suggesting the novelty of HMO-2011 and the prevalence of this phage type in the oceans. A significant number of the viral metagenome sequences obtained from the ocean surface were best assigned to the HMO-2011 genome. The number of reads assigned to HMO-2011 accounted for 10.3%–25.3% of the total reads assigned to viruses in seven viromes from the Pacific and Indian Oceans, making the HMO-2011 genome the most or second-most frequently assigned viral genome. Given its ability to infect the abundant SAR116 clade and its widespread distribution, Puniceispirillum phage HMO-2011 could be an important resource for marine virus research.</description><subject>Amino Acid Sequence</subject><subject>Animal and plant ecology</subject><subject>Animal, plant and microbial ecology</subject><subject>Bacteria</subject><subject>Bacteriophages</subject><subject>Bacteriophages - enzymology</subject><subject>Bacteriophages - genetics</subject><subject>Bacteriophages - isolation & purification</subject><subject>Biological and medical sciences</subject><subject>Biological Sciences</subject><subject>DNA polymerase</subject><subject>DNA-Directed DNA Polymerase - chemistry</subject><subject>DNA-Directed DNA Polymerase - metabolism</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Genes</subject><subject>Genome, Viral</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Marine Biology</subject><subject>Metagenomics</subject><subject>Microbiology</subject><subject>Molecular Sequence Data</subject><subject>Mutation</subject><subject>Oceans</subject><subject>Oceans and Seas</subject><subject>Open Reading Frames</subject><subject>Protein metabolism</subject><subject>Sea water ecosystems</subject><subject>Sequence Homology, Amino Acid</subject><subject>Synecology</subject><subject>Systematics</subject><subject>Virology</subject><subject>Viruses</subject><subject>Water Microbiology</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><recordid>eNpd0U1v1DAQBuAIgei2cOYEWEJIXNKOP2LHF6SqgoJUCYlSrtYkcTZZZe1gZ4v67-s0yxY45TCP583ozbJXFE4pKH42OoynlFGtOVAKT7IVBU1zKTQ8zVYATOWlYOIoO45xAwC6KOF5dsS40qXgepX9vLTOby3xLUFyff6dUkkqrCcbej92uLYkdv53JFNnyRjsLQ7W1Q986vpIFjLdjZb07gH52qKLL7JnLQ7Rvtx_T7Kbz59-XHzJr75dfr04v8rrgrEpx7JsmNKcSikrUMA0yraxstBUWs64Fk0lseJtixaVprqERjAtpaVFyUXFT7KPy95xV21tU1s3BRzMGPothjvjsTf_TlzfmbW_NVyxAjRLCz7sFwT_a2fjZLZ9rO0woLN-Fw0VlBWUiwISffcf3fhdcOm8WRVKlJrLpM4WVQcfY7Dt4WcomLkzM3dmHjtLL978fcPB_ykpgfd7gLHGoQ3o6j4-OlVIzUAkR_ZuTjjEplyeohkXPJHXC9nEyYeDEUylM_U8f7vMW_QG1yHF3FwzoBKAclkoye8BF3q6wg</recordid><startdate>20130723</startdate><enddate>20130723</enddate><creator>Kang, Ilnam</creator><creator>Oh, Hyun-Myung</creator><creator>Kang, Dongmin</creator><creator>Cho, Jang-Cheon</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><scope>IQODW</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20130723</creationdate><title>Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans</title><author>Kang, Ilnam ; Oh, Hyun-Myung ; Kang, Dongmin ; Cho, Jang-Cheon</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c522t-a88d27931666b07029a6fde65916e32394db6ab3ffaea791980d42966e15834b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Amino Acid Sequence</topic><topic>Animal and plant ecology</topic><topic>Animal, plant and microbial ecology</topic><topic>Bacteria</topic><topic>Bacteriophages</topic><topic>Bacteriophages - enzymology</topic><topic>Bacteriophages - genetics</topic><topic>Bacteriophages - isolation & purification</topic><topic>Biological and medical sciences</topic><topic>Biological Sciences</topic><topic>DNA polymerase</topic><topic>DNA-Directed DNA Polymerase - chemistry</topic><topic>DNA-Directed DNA Polymerase - metabolism</topic><topic>Fundamental and applied biological sciences. 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However, obtaining a thorough understanding of marine phages has been hampered by the low number of phage isolates infecting major bacterial groups other than cyanophages and pelagiphages. Therefore, there is an urgent requirement for the isolation of phages that infect abundant marine bacterial groups. In this study, we isolated and characterized HMO-2011, a phage infecting a bacterium of the SAR116 clade, one of the most abundant marine bacterial lineages. HMO-2011, which infects “ Candidatus Puniceispirillum marinum” strain IMCC1322, has an ∼55-kb dsDNA genome that harbors many genes with novel features rarely found in cultured organisms, including genes encoding a DNA polymerase with a partial DnaJ central domain and an atypical methanesulfonate monooxygenase. Furthermore, homologs of nearly all HMO-2011 genes were predominantly found in marine metagenomes rather than cultured organisms, suggesting the novelty of HMO-2011 and the prevalence of this phage type in the oceans. A significant number of the viral metagenome sequences obtained from the ocean surface were best assigned to the HMO-2011 genome. The number of reads assigned to HMO-2011 accounted for 10.3%–25.3% of the total reads assigned to viruses in seven viromes from the Pacific and Indian Oceans, making the HMO-2011 genome the most or second-most frequently assigned viral genome. Given its ability to infect the abundant SAR116 clade and its widespread distribution, Puniceispirillum phage HMO-2011 could be an important resource for marine virus research.</abstract><cop>Washington, DC</cop><pub>National Academy of Sciences</pub><pmid>23798439</pmid><doi>10.1073/pnas.1219930110</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Sequence Animal and plant ecology Animal, plant and microbial ecology Bacteria Bacteriophages Bacteriophages - enzymology Bacteriophages - genetics Bacteriophages - isolation & purification Biological and medical sciences Biological Sciences DNA polymerase DNA-Directed DNA Polymerase - chemistry DNA-Directed DNA Polymerase - metabolism Fundamental and applied biological sciences. Psychology Genes Genome, Viral Genomes Genomics Marine Biology Metagenomics Microbiology Molecular Sequence Data Mutation Oceans Oceans and Seas Open Reading Frames Protein metabolism Sea water ecosystems Sequence Homology, Amino Acid Synecology Systematics Virology Viruses Water Microbiology |
title | Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans |
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