Novel Cluster AZ Arthrobacter phages Powerpuff, Lego, and YesChef exhibit close functional relationships with Microbacterium phages

Bacteriophages exhibit a vast spectrum of relatedness and there is increasing evidence of close genomic relationships independent of host genus. The variability in phage similarity at the nucleotide, amino acid, and gene content levels confounds attempts at quantifying phage relatedness, especially...

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Published in:PloS one Vol. 17; no. 1; p. e0262556
Main Authors: Kapinos, Andrew, Aghamalian, Pauline, Capehart, Erika, Alag, Anya, Angel, Heather, Briseno, Eddie, Corado Perez, Byron, Farag, Emily, Foster, Hilory, Hakim, Abbas, Hernandez-Casas, Daisy, Huang, Calvin, Lam, Derek, Mendez, Maya, Min, Ashley, Nguyen, Nikki, Omholt, Alexa L, Ortiz, Emily, Saldivar, Lizbeth Shelly, Shannon, Jack Arthur, Smith, Rachel, Sridhar, Mihika V, Ta, An, Theophilus, Malavika C, Ngo, Ryan, Torres, Canela, Reddi, Krisanavane, Freise, Amanda C, Moberg Parker, Jordan
Format: Journal Article
Language:English
Published: United States Public Library of Science 13-01-2022
Public Library of Science (PLoS)
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Summary:Bacteriophages exhibit a vast spectrum of relatedness and there is increasing evidence of close genomic relationships independent of host genus. The variability in phage similarity at the nucleotide, amino acid, and gene content levels confounds attempts at quantifying phage relatedness, especially as more novel phages are isolated. This study describes three highly similar novel Arthrobacter globiformis phages-Powerpuff, Lego, and YesChef-which were assigned to Cluster AZ using a nucleotide-based clustering parameter. Phages in Cluster AZ, Microbacterium Cluster EH, and the former Microbacterium singleton Zeta1847 exhibited low nucleotide similarity. However, their gene content similarity was in excess of the recently adopted Microbacterium clustering parameter, which ultimately resulted in the reassignment of Zeta1847 to Cluster EH. This finding further highlights the importance of using multiple metrics to capture phage relatedness. Additionally, Clusters AZ and EH phages encode a shared integrase indicative of a lysogenic life cycle. In the first experimental verification of a Cluster AZ phage's life cycle, we show that phage Powerpuff is a true temperate phage. It forms stable lysogens that exhibit immunity to superinfection by related phages, despite lacking identifiable repressors typically required for lysogenic maintenance and superinfection immunity. The ability of phage Powerpuff to undergo and maintain lysogeny suggests that other closely related phages may be temperate as well. Our findings provide additional evidence of significant shared phage genomic content spanning multiple actinobacterial host genera and demonstrate the continued need for verification and characterization of life cycles in newly isolated phages.
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Competing Interests: The authors have declared that no competing interests exist.
Current address: Department of Biomedical Science, Kaiser Permanente Bernard J. Tyson School of Medicine, Pasadena, CA, United States of America
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0262556