Closely Related Vibrio alginolyticus Strains Encode an Identical Repertoire of Caudovirales-Like Regions and Filamentous Phages
Many filamentous vibriophages encode virulence genes that lead to the emergence of pathogenic bacteria. Most genomes of filamentous vibriophages characterized up until today were isolated from human pathogens. Despite genome-based predictions that environmental Vibrios also contain filamentous phage...
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Published in | Viruses Vol. 12; no. 12; p. 1359 |
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Abstract | Many filamentous vibriophages encode virulence genes that lead to the emergence of pathogenic bacteria. Most genomes of filamentous vibriophages characterized up until today were isolated from human pathogens. Despite genome-based predictions that environmental Vibrios also contain filamentous phages that contribute to bacterial virulence, empirical evidence is scarce. This study aimed to characterize the bacteriophages of a marine pathogen, Vibrio alginolyticus (Kiel-alginolyticus ecotype) and to determine their role in bacterial virulence. To do so, we sequenced the phage-containing supernatant of eight different V. alginolyticus strains, characterized the phages therein and performed infection experiments on juvenile pipefish to assess their contribution to bacterial virulence. We were able to identify two actively replicating filamentous phages. Unique to this study was that all eight bacteria of the Kiel-alginolyticus ecotype have identical bacteriophages, supporting our previously established theory of a clonal expansion of the Kiel-alginolyticus ecotype. We further found that in one of the two filamentous phages, two phage-morphogenesis proteins (Zot and Ace) share high sequence similarity with putative toxins encoded on the Vibrio cholerae phage CTXΦ. The coverage of this filamentous phage correlated positively with virulence (measured in controlled infection experiments on the eukaryotic host), suggesting that this phage contributes to bacterial virulence. |
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AbstractList | Many filamentous vibriophages encode virulence genes that lead to the emergence of pathogenic bacteria. Most genomes of filamentous vibriophages characterized up until today were isolated from human pathogens. Despite genome-based predictions that environmental Vibrios also contain filamentous phages that contribute to bacterial virulence, empirical evidence is scarce. This study aimed to characterize the bacteriophages of a marine pathogen, Vibrio alginolyticus (Kiel-alginolyticus ecotype) and to determine their role in bacterial virulence. To do so, we sequenced the phage-containing supernatant of eight different V. alginolyticus strains, characterized the phages therein and performed infection experiments on juvenile pipefish to assess their contribution to bacterial virulence. We were able to identify two actively replicating filamentous phages. Unique to this study was that all eight bacteria of the Kiel-alginolyticus ecotype have identical bacteriophages, supporting our previously established theory of a clonal expansion of the Kiel-alginolyticus ecotype. We further found that in one of the two filamentous phages, two phage-morphogenesis proteins (Zot and Ace) share high sequence similarity with putative toxins encoded on the Vibrio cholerae phage CTXΦ. The coverage of this filamentous phage correlated positively with virulence (measured in controlled infection experiments on the eukaryotic host), suggesting that this phage contributes to bacterial virulence.Many filamentous vibriophages encode virulence genes that lead to the emergence of pathogenic bacteria. Most genomes of filamentous vibriophages characterized up until today were isolated from human pathogens. Despite genome-based predictions that environmental Vibrios also contain filamentous phages that contribute to bacterial virulence, empirical evidence is scarce. This study aimed to characterize the bacteriophages of a marine pathogen, Vibrio alginolyticus (Kiel-alginolyticus ecotype) and to determine their role in bacterial virulence. To do so, we sequenced the phage-containing supernatant of eight different V. alginolyticus strains, characterized the phages therein and performed infection experiments on juvenile pipefish to assess their contribution to bacterial virulence. We were able to identify two actively replicating filamentous phages. Unique to this study was that all eight bacteria of the Kiel-alginolyticus ecotype have identical bacteriophages, supporting our previously established theory of a clonal expansion of the Kiel-alginolyticus ecotype. We further found that in one of the two filamentous phages, two phage-morphogenesis proteins (Zot and Ace) share high sequence similarity with putative toxins encoded on the Vibrio cholerae phage CTXΦ. The coverage of this filamentous phage correlated positively with virulence (measured in controlled infection experiments on the eukaryotic host), suggesting that this phage contributes to bacterial virulence. Many filamentous vibriophages encode virulence genes that lead to the emergence of pathogenic bacteria. Most genomes of filamentous vibriophages characterized up until today were isolated from human pathogens. Despite genome-based predictions that environmental Vibrios also contain filamentous phages that contribute to bacterial virulence, empirical evidence is scarce. This study aimed to characterize the bacteriophages of a marine pathogen, (Kiel- ecotype) and to determine their role in bacterial virulence. To do so, we sequenced the phage-containing supernatant of eight different strains, characterized the phages therein and performed infection experiments on juvenile pipefish to assess their contribution to bacterial virulence. We were able to identify two actively replicating filamentous phages. Unique to this study was that all eight bacteria of the Kiel- ecotype have identical bacteriophages, supporting our previously established theory of a clonal expansion of the Kiel- ecotype. We further found that in one of the two filamentous phages, two phage-morphogenesis proteins (Zot and Ace) share high sequence similarity with putative toxins encoded on the phage CTXΦ. The coverage of this filamentous phage correlated positively with virulence (measured in controlled infection experiments on the eukaryotic host), suggesting that this phage contributes to bacterial virulence. Many filamentous vibriophages encode virulence genes that lead to the emergence of pathogenic bacteria. Most genomes of filamentous vibriophages characterized up until today were isolated from human pathogens. Despite genome-based predictions that environmental Vibrios also contain filamentous phages that contribute to bacterial virulence, empirical evidence is scarce. This study aimed to characterize the bacteriophages of a marine pathogen, Vibrio alginolyticus (Kiel-alginolyticus ecotype) and to determine their role in bacterial virulence. To do so, we sequenced the phage-containing supernatant of eight different V. alginolyticus strains, characterized the phages therein and performed infection experiments on juvenile pipefish to assess their contribution to bacterial virulence. We were able to identify two actively replicating filamentous phages. Unique to this study was that all eight bacteria of the Kiel-alginolyticus ecotype have identical bacteriophages, supporting our previously established theory of a clonal expansion of the Kiel-alginolyticus ecotype. We further found that in one of the two filamentous phages, two phage-morphogenesis proteins (Zot and Ace) share high sequence similarity with putative toxins encoded on the Vibrio cholerae phage CTXΦ. The coverage of this filamentous phage correlated positively with virulence (measured in controlled infection experiments on the eukaryotic host), suggesting that this phage contributes to bacterial virulence. Many filamentous vibriophages encode virulence genes that lead to the emergence of pathogenic bacteria. Most genomes of filamentous vibriophages characterized up until today were isolated from human pathogens. Despite genome-based predictions that environmental Vibrios also contain filamentous phages that contribute to bacterial virulence, empirical evidence is scarce. This study aimed to characterize the bacteriophages of a marine pathogen, Vibrio alginolyticus (Kiel- alginolyticus ecotype) and to determine their role in bacterial virulence. To do so, we sequenced the phage-containing supernatant of eight different V. alginolyticus strains, characterized the phages therein and performed infection experiments on juvenile pipefish to assess their contribution to bacterial virulence. We were able to identify two actively replicating filamentous phages. Unique to this study was that all eight bacteria of the Kiel- alginolyticus ecotype have identical bacteriophages, supporting our previously established theory of a clonal expansion of the Kiel- alginolyticus ecotype. We further found that in one of the two filamentous phages, two phage-morphogenesis proteins (Zot and Ace) share high sequence similarity with putative toxins encoded on the Vibrio cholerae phage CTXΦ. The coverage of this filamentous phage correlated positively with virulence (measured in controlled infection experiments on the eukaryotic host), suggesting that this phage contributes to bacterial virulence. |
Author | Hoppert, Michael Liesegang, Heiko Wendling, Carolin Charlotte Chibani, Cynthia Maria Hertel, Robert |
AuthorAffiliation | 2 Institute of Microbiology and Genetics, Department of Genomic and Applied Microbiology, Georg-August-University, 37077 Göttingen, Germany; hertel@b-tu.de (R.H.); hlieseg@gwdg.de (H.L.) 6 ETH Zürich, Institute of Integrative Biology, Universitätstrasse 16, CHN D 33, 8092 Zürich, Switzerland 1 Institut für Allgemeine Mikrobiologie, Christian-Albrechts-Universität zu Kiel, Am Botanischen Garten 1-9, 24118 Kiel, Germany; cchibani@ifam.uni-kiel.de 4 Institute for Microbiology and Genetics, University of Göttingen, 37077 Göttingen, Germany; mhopper@gwdg.de 5 GEOMAR, Helmholtz Centre for Ocean Research, Kiel, Düsternbrookerweg 20, 24105 Kiel, Germany 3 FG Synthetic Microbiology, Brandenburg University of Technology, 01968 Cottbus-Senftenberg, Germany |
AuthorAffiliation_xml | – name: 6 ETH Zürich, Institute of Integrative Biology, Universitätstrasse 16, CHN D 33, 8092 Zürich, Switzerland – name: 2 Institute of Microbiology and Genetics, Department of Genomic and Applied Microbiology, Georg-August-University, 37077 Göttingen, Germany; hertel@b-tu.de (R.H.); hlieseg@gwdg.de (H.L.) – name: 3 FG Synthetic Microbiology, Brandenburg University of Technology, 01968 Cottbus-Senftenberg, Germany – name: 1 Institut für Allgemeine Mikrobiologie, Christian-Albrechts-Universität zu Kiel, Am Botanischen Garten 1-9, 24118 Kiel, Germany; cchibani@ifam.uni-kiel.de – name: 4 Institute for Microbiology and Genetics, University of Göttingen, 37077 Göttingen, Germany; mhopper@gwdg.de – name: 5 GEOMAR, Helmholtz Centre for Ocean Research, Kiel, Düsternbrookerweg 20, 24105 Kiel, Germany |
Author_xml | – sequence: 1 givenname: Cynthia Maria orcidid: 0000-0003-2147-9375 surname: Chibani fullname: Chibani, Cynthia Maria – sequence: 2 givenname: Robert orcidid: 0000-0003-4982-6084 surname: Hertel fullname: Hertel, Robert – sequence: 3 givenname: Michael surname: Hoppert fullname: Hoppert, Michael – sequence: 4 givenname: Heiko orcidid: 0000-0003-1792-2047 surname: Liesegang fullname: Liesegang, Heiko – sequence: 5 givenname: Carolin Charlotte surname: Wendling fullname: Wendling, Carolin Charlotte |
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Keywords | prophages Vibrio virulence Inoviridae vibriophages zot filamentous phages |
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SubjectTerms | Animals Bacteria Bacterial Load bacteriophages Caudovirales - classification Caudovirales - genetics Caudovirales - isolation & purification Cholera Climate change Deoxyribonucleic acid DNA DNA, Viral ecotypes filamentous phages Fish Diseases - microbiology Genome, Bacterial Genomes High-Throughput Nucleotide Sequencing humans Inoviridae Inovirus - classification Inovirus - genetics Inovirus - isolation & purification juveniles Morphogenesis Pathogens Phages prophages sequence homology Strains (organisms) Vibrio alginolyticus Vibrio alginolyticus - classification Vibrio alginolyticus - genetics Vibrio alginolyticus - pathogenicity Vibrio alginolyticus - virology Vibrio cholerae Vibrio Infections - veterinary Vibrio virulence vibriophages Virulence zot |
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Title | Closely Related Vibrio alginolyticus Strains Encode an Identical Repertoire of Caudovirales-Like Regions and Filamentous Phages |
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