What Does the Talking?: Quorum Sensing Signalling Genes Discovered in a Bacteriophage Genome

The transfer of novel genetic material into the genomes of bacterial viruses (phages) has been widely documented in several host-phage systems. Bacterial genes are incorporated into the phage genome and, if retained, subsequently evolve within them. The expression of these phage genes can subvert or...

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Vydáno v:	PloS one Ročník 9; číslo 1; s. e85131
Hlavní autoři:	Hargreaves, Katherine R., Kropinski, Andrew M., Clokie, Martha R. J.
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	United States Public Library of Science 24.01.2014 Public Library of Science (PLoS)
Témata:	Amino Acid Sequence Analysis Annotations Antibiotics Bacteria Bacteriophages - classification Bacteriophages - physiology Bacteriophages - ultrastructure Biological evolution Biology Cladistic analysis Clostridium difficile Clostridium difficile - virology Communication Deoxyribonucleic acid DNA DNA sequencing Evolution Evolution, Molecular Gene expression Gene Order Gene sequencing Gene transfer Gene Transfer, Horizontal Genes Genes, Viral Genetic engineering Genetic Variation Genome, Viral Genomes Genomics Health aspects Histidine Histidine kinase Homology Host-Pathogen Interactions Infection Infections Loci Molecular Sequence Data Nosocomial infection Pathogenicity Pathogens Phages Phylogeny Pseudomonas Quorum Sensing - genetics Sequence Alignment Signal Transduction Signaling Strains (organisms) Transcription, Genetic Viruses
ISSN:	1932-6203, 1932-6203
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Abstract	The transfer of novel genetic material into the genomes of bacterial viruses (phages) has been widely documented in several host-phage systems. Bacterial genes are incorporated into the phage genome and, if retained, subsequently evolve within them. The expression of these phage genes can subvert or bolster bacterial processes, including altering bacterial pathogenicity. The phage phiCDHM1 infects Clostridium difficile, a pathogenic bacterium that causes nosocomial infections and is associated with antibiotic treatment. Genome sequencing and annotation of phiCDHM1 shows that despite being closely related to other C. difficile myoviruses, it has several genes that have not been previously reported in any phage genomes. Notably, these include three homologs of bacterial genes from the accessory gene regulator (agr) quorum sensing (QS) system. These are; a pre-peptide (AgrD) of an autoinducing peptide (AIP), an enzyme which processes the pre-peptide (AgrB) and a histidine kinase (AgrC) that detects the AIP to activate a response regulator. Phylogenetic analysis of the phage and C. difficile agr genes revealed that there are three types of agr loci in this species. We propose that the phage genes belonging to a third type, agr3, and have been horizontally transferred from the host. AgrB and AgrC are transcribed during the infection of two different strains. In addition, the phage agrC appears not to be confined to the phiCDHM1 genome as it was detected in genetically distinct C. difficile strains. The discovery of QS gene homologs in a phage genome presents a novel way in which phages could influence their bacterial hosts, or neighbouring bacterial populations. This is the first time that these QS genes have been reported in a phage genome and their distribution both in C. difficile and phage genomes suggests that the agr3 locus undergoes horizontal gene transfer within this species.
AbstractList	The transfer of novel genetic material into the genomes of bacterial viruses (phages) has been widely documented in several host-phage systems. Bacterial genes are incorporated into the phage genome and, if retained, subsequently evolve within them. The expression of these phage genes can subvert or bolster bacterial processes, including altering bacterial pathogenicity. The phage phiCDHM1 infects Clostridium difficile, a pathogenic bacterium that causes nosocomial infections and is associated with antibiotic treatment. Genome sequencing and annotation of phiCDHM1 shows that despite being closely related to other C. difficile myoviruses, it has several genes that have not been previously reported in any phage genomes. Notably, these include three homologs of bacterial genes from the accessory gene regulator (agr) quorum sensing (QS) system. These are; a pre-peptide (AgrD) of an autoinducing peptide (AIP), an enzyme which processes the pre-peptide (AgrB) and a histidine kinase (AgrC) that detects the AIP to activate a response regulator. Phylogenetic analysis of the phage and C. difficile agr genes revealed that there are three types of agr loci in this species. We propose that the phage genes belonging to a third type, agr3, and have been horizontally transferred from the host. AgrB and AgrC are transcribed during the infection of two different strains. In addition, the phage agrC appears not to be confined to the phiCDHM1 genome as it was detected in genetically distinct C. difficile strains. The discovery of QS gene homologs in a phage genome presents a novel way in which phages could influence their bacterial hosts, or neighbouring bacterial populations. This is the first time that these QS genes have been reported in a phage genome and their distribution both in C. difficile and phage genomes suggests that the agr3 locus undergoes horizontal gene transfer within this species. The transfer of novel genetic material into the genomes of bacterial viruses (phages) has been widely documented in several host-phage systems. Bacterial genes are incorporated into the phage genome and, if retained, subsequently evolve within them. The expression of these phage genes can subvert or bolster bacterial processes, including altering bacterial pathogenicity. The phage phiCDHM1 infects Clostridium difficile, a pathogenic bacterium that causes nosocomial infections and is associated with antibiotic treatment. Genome sequencing and annotation of phiCDHM1 shows that despite being closely related to other C. difficile myoviruses, it has several genes that have not been previously reported in any phage genomes. Notably, these include three homologs of bacterial genes from the accessory gene regulator (agr) quorum sensing (QS) system. These are; a pre-peptide (AgrD) of an autoinducing peptide (AIP), an enzyme which processes the pre-peptide (AgrB) and a histidine kinase (AgrC) that detects the AIP to activate a response regulator. Phylogenetic analysis of the phage and C. difficile agr genes revealed that there are three types of agr loci in this species. We propose that the phage genes belonging to a third type, agr3, and have been horizontally transferred from the host. AgrB and AgrC are transcribed during the infection of two different strains. In addition, the phage agrC appears not to be confined to the phiCDHM1 genome as it was detected in genetically distinct C. difficile strains. The discovery of QS gene homologs in a phage genome presents a novel way in which phages could influence their bacterial hosts, or neighbouring bacterial populations. This is the first time that these QS genes have been reported in a phage genome and their distribution both in C. difficile and phage genomes suggests that the agr3 locus undergoes horizontal gene transfer within this species.The transfer of novel genetic material into the genomes of bacterial viruses (phages) has been widely documented in several host-phage systems. Bacterial genes are incorporated into the phage genome and, if retained, subsequently evolve within them. The expression of these phage genes can subvert or bolster bacterial processes, including altering bacterial pathogenicity. The phage phiCDHM1 infects Clostridium difficile, a pathogenic bacterium that causes nosocomial infections and is associated with antibiotic treatment. Genome sequencing and annotation of phiCDHM1 shows that despite being closely related to other C. difficile myoviruses, it has several genes that have not been previously reported in any phage genomes. Notably, these include three homologs of bacterial genes from the accessory gene regulator (agr) quorum sensing (QS) system. These are; a pre-peptide (AgrD) of an autoinducing peptide (AIP), an enzyme which processes the pre-peptide (AgrB) and a histidine kinase (AgrC) that detects the AIP to activate a response regulator. Phylogenetic analysis of the phage and C. difficile agr genes revealed that there are three types of agr loci in this species. We propose that the phage genes belonging to a third type, agr3, and have been horizontally transferred from the host. AgrB and AgrC are transcribed during the infection of two different strains. In addition, the phage agrC appears not to be confined to the phiCDHM1 genome as it was detected in genetically distinct C. difficile strains. The discovery of QS gene homologs in a phage genome presents a novel way in which phages could influence their bacterial hosts, or neighbouring bacterial populations. This is the first time that these QS genes have been reported in a phage genome and their distribution both in C. difficile and phage genomes suggests that the agr3 locus undergoes horizontal gene transfer within this species.
Audience	Academic
Author	Hargreaves, Katherine R. Clokie, Martha R. J. Kropinski, Andrew M.
AuthorAffiliation	1 Department of Infection, Immunity and Inflammation, University of Leicester, Leicester, Leicestershire, United Kingdom 2 Laboratory for Foodborne Zoonoses, Public Health Agency of Canada, West Guelph, Ontario, Canada 3 Department of Molecular and Cellular Biology, University of Guelph, Guelph, Ontario, Canada The Scripps Research Institute and Sorrento Therapeutics, Inc., United States of America
AuthorAffiliation_xml	– name: 1 Department of Infection, Immunity and Inflammation, University of Leicester, Leicester, Leicestershire, United Kingdom – name: The Scripps Research Institute and Sorrento Therapeutics, Inc., United States of America – name: 2 Laboratory for Foodborne Zoonoses, Public Health Agency of Canada, West Guelph, Ontario, Canada – name: 3 Department of Molecular and Cellular Biology, University of Guelph, Guelph, Ontario, Canada
Author_xml	– sequence: 1 givenname: Katherine R. surname: Hargreaves fullname: Hargreaves, Katherine R. – sequence: 2 givenname: Andrew M. surname: Kropinski fullname: Kropinski, Andrew M. – sequence: 3 givenname: Martha R. J. surname: Clokie fullname: Clokie, Martha R. J.
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24475037$$D View this record in MEDLINE/PubMed
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Copyright	COPYRIGHT 2014 Public Library of Science 2014 Hargreaves 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. 2014 Hargreaves et al 2014 Hargreaves et al
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Competing Interests: Phage CDHM1 is included as part of a patent application no 1215184.1. The full patent name is Therapeutic phage No. PCT/GB2013/052245. This does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials. Conceived and designed the experiments: KRH MRJC AMK. Performed the experiments: KRH AMK. Analyzed the data: KRH MRJC AMK. Contributed reagents/materials/analysis tools: KRH MRJC AMK. Wrote the paper: KRH MRJC AMK.
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Snippet	The transfer of novel genetic material into the genomes of bacterial viruses (phages) has been widely documented in several host-phage systems. Bacterial genes...
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SubjectTerms	Amino Acid Sequence Analysis Annotations Antibiotics Bacteria Bacteriophages - classification Bacteriophages - physiology Bacteriophages - ultrastructure Biological evolution Biology Cladistic analysis Clostridium difficile Clostridium difficile - virology Communication Deoxyribonucleic acid DNA DNA sequencing Evolution Evolution, Molecular Gene expression Gene Order Gene sequencing Gene transfer Gene Transfer, Horizontal Genes Genes, Viral Genetic engineering Genetic Variation Genome, Viral Genomes Genomics Health aspects Histidine Histidine kinase Homology Host-Pathogen Interactions Infection Infections Loci Molecular Sequence Data Nosocomial infection Pathogenicity Pathogens Phages Phylogeny Pseudomonas Quorum Sensing - genetics Sequence Alignment Signal Transduction Signaling Strains (organisms) Transcription, Genetic Viruses
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Title	What Does the Talking?: Quorum Sensing Signalling Genes Discovered in a Bacteriophage Genome
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Volume	9
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