A genome-wide cytotoxicity screen of cluster F1 mycobacteriophage Girr reveals novel inhibitors of Mycobacterium smegmatis growth
Abstract Over the past decade, thousands of bacteriophage genomes have been sequenced and annotated. A striking observation from this work is that known structural features and functions cannot be assigned for >65% of the encoded proteins. One approach to begin experimentally elucidating the func...
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| creator | Pollenz, Richard S Barnhill, Kaylee Biggs, Abbigail Bland, Jackson Carter, Victoria Chase, Michael Clark, Hayley Coleman, Caitlyn Daffner, Marshall Deam, Caitlyn Finocchiaro, Alyssa Franco, Vanessa Fuller, Thomas Pinera, Juan Gallardo Horne, Mae Howard, Zoe Kanahan, Olivia Miklaszewski, Christopher Miller, Sydney Morgan, Ryan Onalaja, Oluwatobi Otero, Louis Padhye, Shivani Rainey, Emily Rasul, Fareed Robichaux, Kobe Rodier, Alexandra Schlosser, Sydni Sciacchitano, Ava Stewart, Emma Thakkar, Rajvi Heller, Danielle M |
| description | Abstract
Over the past decade, thousands of bacteriophage genomes have been sequenced and annotated. A striking observation from this work is that known structural features and functions cannot be assigned for >65% of the encoded proteins. One approach to begin experimentally elucidating the function of these uncharacterized gene products is genome-wide screening to identify phage genes that confer phenotypes of interest like inhibition of host growth. This study describes the results of a screen evaluating the effects of overexpressing each gene encoded by the temperate Cluster F1 mycobacteriophage Girr on the growth of the host bacterium Mycobacterium smegmatis. Overexpression of 29 of the 102 Girr genes (~28% of the genome) resulted in mild to severe cytotoxicity. Of the 29 toxic genes described, 12 have no known function and are predominately small proteins of |
| doi_str_mv | 10.1093/g3journal/jkae049 |
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Over the past decade, thousands of bacteriophage genomes have been sequenced and annotated. A striking observation from this work is that known structural features and functions cannot be assigned for >65% of the encoded proteins. One approach to begin experimentally elucidating the function of these uncharacterized gene products is genome-wide screening to identify phage genes that confer phenotypes of interest like inhibition of host growth. This study describes the results of a screen evaluating the effects of overexpressing each gene encoded by the temperate Cluster F1 mycobacteriophage Girr on the growth of the host bacterium Mycobacterium smegmatis. Overexpression of 29 of the 102 Girr genes (~28% of the genome) resulted in mild to severe cytotoxicity. Of the 29 toxic genes described, 12 have no known function and are predominately small proteins of <125 amino acids. Overexpression of the majority of these 12 cytotoxic no known functions proteins resulted in moderate to severe growth reduction and represent novel antimicrobial products. The remaining 17 toxic genes have predicted functions, encoding products involved in phage structure, DNA replication/modification, DNA binding/gene regulation, or other enzymatic activity. Comparison of this dataset with prior genome-wide cytotoxicity screens of mycobacteriophages Waterfoul and Hammy reveals some common functional themes, though several of the predicted Girr functions associated with cytotoxicity in our report, including genes involved in lysogeny, have not been described previously. This study, completed as part of the HHMI-supported SEA-GENES project, highlights the power of parallel, genome-wide overexpression screens to identify novel interactions between phages and their hosts.</description><identifier>ISSN: 2160-1836</identifier><identifier>EISSN: 2160-1836</identifier><identifier>DOI: 10.1093/g3journal/jkae049</identifier><identifier>PMID: 38456318</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Genome, Viral ; Mutant Screen Report ; Mycobacteriophages - genetics ; Mycobacterium smegmatis - virology ; Viral Proteins - genetics ; Viral Proteins - metabolism</subject><ispartof>G3 : genes - genomes - genetics, 2024-05, Vol.14 (5)</ispartof><rights>The Author(s) 2024. Published by Oxford University Press on behalf of The Genetics Society of America. 2024</rights><rights>The Author(s) 2024. Published by Oxford University Press on behalf of The Genetics Society of America.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c389t-4e0869b63073ab245abf437cd9bf810fb98d56a1b401172c935f4ac59786e7d63</cites><orcidid>0000-0002-6581-1256 ; 0000-0001-8891-6053</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/PMC11075535/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11075535/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,1598,27903,27904,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38456318$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Jamann, T</contributor><creatorcontrib>Pollenz, Richard S</creatorcontrib><creatorcontrib>Barnhill, Kaylee</creatorcontrib><creatorcontrib>Biggs, Abbigail</creatorcontrib><creatorcontrib>Bland, Jackson</creatorcontrib><creatorcontrib>Carter, Victoria</creatorcontrib><creatorcontrib>Chase, Michael</creatorcontrib><creatorcontrib>Clark, Hayley</creatorcontrib><creatorcontrib>Coleman, Caitlyn</creatorcontrib><creatorcontrib>Daffner, Marshall</creatorcontrib><creatorcontrib>Deam, Caitlyn</creatorcontrib><creatorcontrib>Finocchiaro, Alyssa</creatorcontrib><creatorcontrib>Franco, Vanessa</creatorcontrib><creatorcontrib>Fuller, Thomas</creatorcontrib><creatorcontrib>Pinera, Juan Gallardo</creatorcontrib><creatorcontrib>Horne, Mae</creatorcontrib><creatorcontrib>Howard, Zoe</creatorcontrib><creatorcontrib>Kanahan, Olivia</creatorcontrib><creatorcontrib>Miklaszewski, Christopher</creatorcontrib><creatorcontrib>Miller, Sydney</creatorcontrib><creatorcontrib>Morgan, Ryan</creatorcontrib><creatorcontrib>Onalaja, Oluwatobi</creatorcontrib><creatorcontrib>Otero, Louis</creatorcontrib><creatorcontrib>Padhye, Shivani</creatorcontrib><creatorcontrib>Rainey, Emily</creatorcontrib><creatorcontrib>Rasul, Fareed</creatorcontrib><creatorcontrib>Robichaux, Kobe</creatorcontrib><creatorcontrib>Rodier, Alexandra</creatorcontrib><creatorcontrib>Schlosser, Sydni</creatorcontrib><creatorcontrib>Sciacchitano, Ava</creatorcontrib><creatorcontrib>Stewart, Emma</creatorcontrib><creatorcontrib>Thakkar, Rajvi</creatorcontrib><creatorcontrib>Heller, Danielle M</creatorcontrib><title>A genome-wide cytotoxicity screen of cluster F1 mycobacteriophage Girr reveals novel inhibitors of Mycobacterium smegmatis growth</title><title>G3 : genes - genomes - genetics</title><addtitle>G3 (Bethesda)</addtitle><description>Abstract
Over the past decade, thousands of bacteriophage genomes have been sequenced and annotated. A striking observation from this work is that known structural features and functions cannot be assigned for >65% of the encoded proteins. One approach to begin experimentally elucidating the function of these uncharacterized gene products is genome-wide screening to identify phage genes that confer phenotypes of interest like inhibition of host growth. This study describes the results of a screen evaluating the effects of overexpressing each gene encoded by the temperate Cluster F1 mycobacteriophage Girr on the growth of the host bacterium Mycobacterium smegmatis. Overexpression of 29 of the 102 Girr genes (~28% of the genome) resulted in mild to severe cytotoxicity. Of the 29 toxic genes described, 12 have no known function and are predominately small proteins of <125 amino acids. Overexpression of the majority of these 12 cytotoxic no known functions proteins resulted in moderate to severe growth reduction and represent novel antimicrobial products. The remaining 17 toxic genes have predicted functions, encoding products involved in phage structure, DNA replication/modification, DNA binding/gene regulation, or other enzymatic activity. Comparison of this dataset with prior genome-wide cytotoxicity screens of mycobacteriophages Waterfoul and Hammy reveals some common functional themes, though several of the predicted Girr functions associated with cytotoxicity in our report, including genes involved in lysogeny, have not been described previously. This study, completed as part of the HHMI-supported SEA-GENES project, highlights the power of parallel, genome-wide overexpression screens to identify novel interactions between phages and their hosts.</description><subject>Genome, Viral</subject><subject>Mutant Screen Report</subject><subject>Mycobacteriophages - genetics</subject><subject>Mycobacterium smegmatis - virology</subject><subject>Viral Proteins - genetics</subject><subject>Viral Proteins - metabolism</subject><issn>2160-1836</issn><issn>2160-1836</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNqNkU1v1DAQhi0EolXpD-CCfORAqB1_xSdUVf1AKuICZ8t2JlkvSbzYzpY98s-bapel3JjLjDXv846lF6G3lHykRLOLnq3jnCY7XKx_WCBcv0CnNZWkog2TL5_NJ-g85zVZSggpuXyNTljDhWS0OUW_L3EPUxyheggtYL8rscRfwYeyw9kngAnHDvthzgUSvqF43PnorF9eIW5Wtgd8G1LCCbZgh4ynuIUBh2kVXCgx5Sf6y19kHnEeoR9tCRn3KT6U1Rv0qltIOD_0M_T95vrb1V11__X289XlfeVZo0vFgTRSO8mIYtbVXFjXcaZ8q13XUNI53bRCWuo4oVTVXjPRceuFVo0E1Up2hj7tfTezG6H1MJVkB7NJYbRpZ6IN5t_NFFamj1tDKVFCMLE4vD84pPhzhlzMGLKHYbATxDmbWguulBSqXqR0L_Up5pygO96hxDzFZ47xmUN8C_Pu-QePxJ-wFsGHvSDOm__wewRCyazZ</recordid><startdate>20240507</startdate><enddate>20240507</enddate><creator>Pollenz, Richard S</creator><creator>Barnhill, Kaylee</creator><creator>Biggs, Abbigail</creator><creator>Bland, Jackson</creator><creator>Carter, Victoria</creator><creator>Chase, Michael</creator><creator>Clark, Hayley</creator><creator>Coleman, Caitlyn</creator><creator>Daffner, Marshall</creator><creator>Deam, Caitlyn</creator><creator>Finocchiaro, Alyssa</creator><creator>Franco, Vanessa</creator><creator>Fuller, Thomas</creator><creator>Pinera, Juan Gallardo</creator><creator>Horne, Mae</creator><creator>Howard, Zoe</creator><creator>Kanahan, Olivia</creator><creator>Miklaszewski, Christopher</creator><creator>Miller, Sydney</creator><creator>Morgan, Ryan</creator><creator>Onalaja, Oluwatobi</creator><creator>Otero, Louis</creator><creator>Padhye, Shivani</creator><creator>Rainey, Emily</creator><creator>Rasul, Fareed</creator><creator>Robichaux, Kobe</creator><creator>Rodier, Alexandra</creator><creator>Schlosser, Sydni</creator><creator>Sciacchitano, Ava</creator><creator>Stewart, Emma</creator><creator>Thakkar, Rajvi</creator><creator>Heller, Danielle M</creator><general>Oxford University Press</general><scope>TOX</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6581-1256</orcidid><orcidid>https://orcid.org/0000-0001-8891-6053</orcidid></search><sort><creationdate>20240507</creationdate><title>A genome-wide cytotoxicity screen of cluster F1 mycobacteriophage Girr reveals novel inhibitors of Mycobacterium smegmatis growth</title><author>Pollenz, Richard S ; 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Over the past decade, thousands of bacteriophage genomes have been sequenced and annotated. A striking observation from this work is that known structural features and functions cannot be assigned for >65% of the encoded proteins. One approach to begin experimentally elucidating the function of these uncharacterized gene products is genome-wide screening to identify phage genes that confer phenotypes of interest like inhibition of host growth. This study describes the results of a screen evaluating the effects of overexpressing each gene encoded by the temperate Cluster F1 mycobacteriophage Girr on the growth of the host bacterium Mycobacterium smegmatis. Overexpression of 29 of the 102 Girr genes (~28% of the genome) resulted in mild to severe cytotoxicity. Of the 29 toxic genes described, 12 have no known function and are predominately small proteins of <125 amino acids. Overexpression of the majority of these 12 cytotoxic no known functions proteins resulted in moderate to severe growth reduction and represent novel antimicrobial products. The remaining 17 toxic genes have predicted functions, encoding products involved in phage structure, DNA replication/modification, DNA binding/gene regulation, or other enzymatic activity. Comparison of this dataset with prior genome-wide cytotoxicity screens of mycobacteriophages Waterfoul and Hammy reveals some common functional themes, though several of the predicted Girr functions associated with cytotoxicity in our report, including genes involved in lysogeny, have not been described previously. This study, completed as part of the HHMI-supported SEA-GENES project, highlights the power of parallel, genome-wide overexpression screens to identify novel interactions between phages and their hosts.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>38456318</pmid><doi>10.1093/g3journal/jkae049</doi><orcidid>https://orcid.org/0000-0002-6581-1256</orcidid><orcidid>https://orcid.org/0000-0001-8891-6053</orcidid><oa>free_for_read</oa></addata></record> |
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| source | Oxford Journals Open Access Collection; MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central |
| subjects | Genome, Viral Mutant Screen Report Mycobacteriophages - genetics Mycobacterium smegmatis - virology Viral Proteins - genetics Viral Proteins - metabolism |
| title | A genome-wide cytotoxicity screen of cluster F1 mycobacteriophage Girr reveals novel inhibitors of Mycobacterium smegmatis growth |
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