Characterization of Five Novel Brevibacillus Bacteriophages and Genomic Comparison of Brevibacillus Phages
Brevibacillus laterosporus is a spore-forming bacterium that causes a secondary infection in beehives following European Foulbrood disease. To better understand the contributions of Brevibacillus bacteriophages to the evolution of their hosts, five novel phages (Jenst, Osiris, Powder, SecTim467, and...
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| creator | Berg, Jordan A Merrill, Bryan D Crockett, Justin T Esplin, Kyle P Evans, Marlee R Heaton, Karli E Hilton, Jared A Hyde, Jonathan R McBride, Morgan S Schouten, Jordan T Simister, Austin R Thurgood, Trever L Ward, Andrew T Breakwell, Donald P Hope, Sandra Grose, Julianne H |
| description | Brevibacillus laterosporus is a spore-forming bacterium that causes a secondary infection in beehives following European Foulbrood disease. To better understand the contributions of Brevibacillus bacteriophages to the evolution of their hosts, five novel phages (Jenst, Osiris, Powder, SecTim467, and Sundance) were isolated and characterized. When compared with the five Brevibacillus phages currently in NCBI, these phages were assigned to clusters based on whole genome and proteome synteny. Powder and Osiris, both myoviruses, were assigned to the previously described Jimmer-like cluster. SecTim467 and Jenst, both siphoviruses, formed a novel phage cluster. Sundance, a siphovirus, was assigned as a singleton phage along with the previously isolated singleton, Emery. In addition to characterizing the basic relationships between these phages, several genomic features were observed. A motif repeated throughout phages Jenst and SecTim467 was frequently upstream of genes predicted to function in DNA replication, nucleotide metabolism, and transcription, suggesting transcriptional co-regulation. In addition, paralogous gene pairs that encode a putative transcriptional regulator were identified in four Brevibacillus phages. These paralogs likely evolved to bind different DNA sequences due to variation at amino acid residues predicted to bind specific nucleotides. Finally, a putative transposable element was identified in SecTim467 and Sundance that carries genes homologous to those found in Brevibacillus chromosomes. Remnants of this transposable element were also identified in phage Jenst. These discoveries provide a greater understanding of the diversity of phages, their behavior, and their evolutionary relationships to one another and to their host. In addition, they provide a foundation with which further Brevibacillus phages can be compared. |
| doi_str_mv | 10.1371/journal.pone.0156838 |
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To better understand the contributions of Brevibacillus bacteriophages to the evolution of their hosts, five novel phages (Jenst, Osiris, Powder, SecTim467, and Sundance) were isolated and characterized. When compared with the five Brevibacillus phages currently in NCBI, these phages were assigned to clusters based on whole genome and proteome synteny. Powder and Osiris, both myoviruses, were assigned to the previously described Jimmer-like cluster. SecTim467 and Jenst, both siphoviruses, formed a novel phage cluster. Sundance, a siphovirus, was assigned as a singleton phage along with the previously isolated singleton, Emery. In addition to characterizing the basic relationships between these phages, several genomic features were observed. A motif repeated throughout phages Jenst and SecTim467 was frequently upstream of genes predicted to function in DNA replication, nucleotide metabolism, and transcription, suggesting transcriptional co-regulation. In addition, paralogous gene pairs that encode a putative transcriptional regulator were identified in four Brevibacillus phages. These paralogs likely evolved to bind different DNA sequences due to variation at amino acid residues predicted to bind specific nucleotides. Finally, a putative transposable element was identified in SecTim467 and Sundance that carries genes homologous to those found in Brevibacillus chromosomes. Remnants of this transposable element were also identified in phage Jenst. These discoveries provide a greater understanding of the diversity of phages, their behavior, and their evolutionary relationships to one another and to their host. In addition, they provide a foundation with which further Brevibacillus phages can be compared.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0156838</identifier><identifier>PMID: 27304881</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino Acid Sequence ; Amino acids ; Bacillus subtilis ; Bacteria ; Bacteriophages - classification ; Bacteriophages - genetics ; Bacteriophages - metabolism ; Base Sequence ; Beehives ; Bees ; Biological evolution ; Biology and Life Sciences ; Brevibacillus ; Brevibacillus - virology ; Brevibacillus laterosporus ; Chromosomes ; Clusters ; Deoxyribonucleic acid ; DNA ; DNA biosynthesis ; DNA Replication ; DNA, Viral - genetics ; E coli ; Escherichia coli ; European foulbrood ; Gene expression ; Gene Expression Regulation, Viral ; Gene regulation ; Gene sequencing ; Genes ; Genetic engineering ; Genetic Variation ; Genome, Viral - genetics ; Genomes ; Genomics - methods ; Homology ; Infections ; Metabolism ; Microscopy, Electron, Transmission ; Molecular biology ; Mutation ; Nucleotide sequence ; Nucleotides ; Phages ; Phylogeny ; Powder ; Proteins ; Proteomes ; Proteomics - methods ; Secondary infection ; Sequence Analysis, DNA ; Sequence Homology, Amino Acid ; Synteny ; Transcription ; Transposons ; Vibrio cholerae ; Viral Proteins - genetics ; Viral Proteins - metabolism ; Virion - genetics ; Virion - metabolism ; Virion - ultrastructure ; Virology</subject><ispartof>PloS one, 2016-06, Vol.11 (6), p.e0156838-e0156838</ispartof><rights>2016 Berg 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. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2016 Berg et al 2016 Berg et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c559t-65f3c8e297433300d299b9e3e05605544db23dbd5c0609be75934c862fe1fb563</citedby><cites>FETCH-LOGICAL-c559t-65f3c8e297433300d299b9e3e05605544db23dbd5c0609be75934c862fe1fb563</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4909266/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4909266/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27304881$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Schuch, Raymond</contributor><creatorcontrib>Berg, Jordan A</creatorcontrib><creatorcontrib>Merrill, Bryan D</creatorcontrib><creatorcontrib>Crockett, Justin T</creatorcontrib><creatorcontrib>Esplin, Kyle P</creatorcontrib><creatorcontrib>Evans, Marlee R</creatorcontrib><creatorcontrib>Heaton, Karli E</creatorcontrib><creatorcontrib>Hilton, Jared A</creatorcontrib><creatorcontrib>Hyde, Jonathan R</creatorcontrib><creatorcontrib>McBride, Morgan S</creatorcontrib><creatorcontrib>Schouten, Jordan T</creatorcontrib><creatorcontrib>Simister, Austin R</creatorcontrib><creatorcontrib>Thurgood, Trever L</creatorcontrib><creatorcontrib>Ward, Andrew T</creatorcontrib><creatorcontrib>Breakwell, Donald P</creatorcontrib><creatorcontrib>Hope, Sandra</creatorcontrib><creatorcontrib>Grose, Julianne H</creatorcontrib><title>Characterization of Five Novel Brevibacillus Bacteriophages and Genomic Comparison of Brevibacillus Phages</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Brevibacillus laterosporus is a spore-forming bacterium that causes a secondary infection in beehives following European Foulbrood disease. To better understand the contributions of Brevibacillus bacteriophages to the evolution of their hosts, five novel phages (Jenst, Osiris, Powder, SecTim467, and Sundance) were isolated and characterized. When compared with the five Brevibacillus phages currently in NCBI, these phages were assigned to clusters based on whole genome and proteome synteny. Powder and Osiris, both myoviruses, were assigned to the previously described Jimmer-like cluster. SecTim467 and Jenst, both siphoviruses, formed a novel phage cluster. Sundance, a siphovirus, was assigned as a singleton phage along with the previously isolated singleton, Emery. In addition to characterizing the basic relationships between these phages, several genomic features were observed. A motif repeated throughout phages Jenst and SecTim467 was frequently upstream of genes predicted to function in DNA replication, nucleotide metabolism, and transcription, suggesting transcriptional co-regulation. In addition, paralogous gene pairs that encode a putative transcriptional regulator were identified in four Brevibacillus phages. These paralogs likely evolved to bind different DNA sequences due to variation at amino acid residues predicted to bind specific nucleotides. Finally, a putative transposable element was identified in SecTim467 and Sundance that carries genes homologous to those found in Brevibacillus chromosomes. Remnants of this transposable element were also identified in phage Jenst. These discoveries provide a greater understanding of the diversity of phages, their behavior, and their evolutionary relationships to one another and to their host. In addition, they provide a foundation with which further Brevibacillus phages can be compared.</description><subject>Amino Acid Sequence</subject><subject>Amino acids</subject><subject>Bacillus subtilis</subject><subject>Bacteria</subject><subject>Bacteriophages - classification</subject><subject>Bacteriophages - genetics</subject><subject>Bacteriophages - metabolism</subject><subject>Base Sequence</subject><subject>Beehives</subject><subject>Bees</subject><subject>Biological evolution</subject><subject>Biology and Life Sciences</subject><subject>Brevibacillus</subject><subject>Brevibacillus - virology</subject><subject>Brevibacillus laterosporus</subject><subject>Chromosomes</subject><subject>Clusters</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA biosynthesis</subject><subject>DNA Replication</subject><subject>DNA, Viral - genetics</subject><subject>E coli</subject><subject>Escherichia coli</subject><subject>European foulbrood</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Viral</subject><subject>Gene regulation</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genetic engineering</subject><subject>Genetic Variation</subject><subject>Genome, Viral - genetics</subject><subject>Genomes</subject><subject>Genomics - methods</subject><subject>Homology</subject><subject>Infections</subject><subject>Metabolism</subject><subject>Microscopy, Electron, Transmission</subject><subject>Molecular biology</subject><subject>Mutation</subject><subject>Nucleotide sequence</subject><subject>Nucleotides</subject><subject>Phages</subject><subject>Phylogeny</subject><subject>Powder</subject><subject>Proteins</subject><subject>Proteomes</subject><subject>Proteomics - methods</subject><subject>Secondary infection</subject><subject>Sequence Analysis, DNA</subject><subject>Sequence Homology, Amino Acid</subject><subject>Synteny</subject><subject>Transcription</subject><subject>Transposons</subject><subject>Vibrio cholerae</subject><subject>Viral Proteins - genetics</subject><subject>Viral Proteins - metabolism</subject><subject>Virion - genetics</subject><subject>Virion - metabolism</subject><subject>Virion - 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Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Berg, Jordan A</au><au>Merrill, Bryan D</au><au>Crockett, Justin T</au><au>Esplin, Kyle P</au><au>Evans, Marlee R</au><au>Heaton, Karli E</au><au>Hilton, Jared A</au><au>Hyde, Jonathan R</au><au>McBride, Morgan S</au><au>Schouten, Jordan T</au><au>Simister, Austin R</au><au>Thurgood, Trever L</au><au>Ward, Andrew T</au><au>Breakwell, Donald P</au><au>Hope, Sandra</au><au>Grose, Julianne H</au><au>Schuch, Raymond</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Characterization of Five Novel Brevibacillus Bacteriophages and Genomic Comparison of Brevibacillus Phages</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2016-06-01</date><risdate>2016</risdate><volume>11</volume><issue>6</issue><spage>e0156838</spage><epage>e0156838</epage><pages>e0156838-e0156838</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Brevibacillus laterosporus is a spore-forming bacterium that causes a secondary infection in beehives following European Foulbrood disease. To better understand the contributions of Brevibacillus bacteriophages to the evolution of their hosts, five novel phages (Jenst, Osiris, Powder, SecTim467, and Sundance) were isolated and characterized. When compared with the five Brevibacillus phages currently in NCBI, these phages were assigned to clusters based on whole genome and proteome synteny. Powder and Osiris, both myoviruses, were assigned to the previously described Jimmer-like cluster. SecTim467 and Jenst, both siphoviruses, formed a novel phage cluster. Sundance, a siphovirus, was assigned as a singleton phage along with the previously isolated singleton, Emery. In addition to characterizing the basic relationships between these phages, several genomic features were observed. A motif repeated throughout phages Jenst and SecTim467 was frequently upstream of genes predicted to function in DNA replication, nucleotide metabolism, and transcription, suggesting transcriptional co-regulation. In addition, paralogous gene pairs that encode a putative transcriptional regulator were identified in four Brevibacillus phages. These paralogs likely evolved to bind different DNA sequences due to variation at amino acid residues predicted to bind specific nucleotides. Finally, a putative transposable element was identified in SecTim467 and Sundance that carries genes homologous to those found in Brevibacillus chromosomes. Remnants of this transposable element were also identified in phage Jenst. These discoveries provide a greater understanding of the diversity of phages, their behavior, and their evolutionary relationships to one another and to their host. In addition, they provide a foundation with which further Brevibacillus phages can be compared.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>27304881</pmid><doi>10.1371/journal.pone.0156838</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2016-06, Vol.11 (6), p.e0156838-e0156838 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1797243345 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS); EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Amino Acid Sequence Amino acids Bacillus subtilis Bacteria Bacteriophages - classification Bacteriophages - genetics Bacteriophages - metabolism Base Sequence Beehives Bees Biological evolution Biology and Life Sciences Brevibacillus Brevibacillus - virology Brevibacillus laterosporus Chromosomes Clusters Deoxyribonucleic acid DNA DNA biosynthesis DNA Replication DNA, Viral - genetics E coli Escherichia coli European foulbrood Gene expression Gene Expression Regulation, Viral Gene regulation Gene sequencing Genes Genetic engineering Genetic Variation Genome, Viral - genetics Genomes Genomics - methods Homology Infections Metabolism Microscopy, Electron, Transmission Molecular biology Mutation Nucleotide sequence Nucleotides Phages Phylogeny Powder Proteins Proteomes Proteomics - methods Secondary infection Sequence Analysis, DNA Sequence Homology, Amino Acid Synteny Transcription Transposons Vibrio cholerae Viral Proteins - genetics Viral Proteins - metabolism Virion - genetics Virion - metabolism Virion - ultrastructure Virology |
| title | Characterization of Five Novel Brevibacillus Bacteriophages and Genomic Comparison of Brevibacillus Phages |
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