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Genomic diversity of bacteriophages infecting Microbacterium spp.

ABSTRACT: The bacteriophage population is vast, dynamic, old, and genetically diverse. The genomics of phages that infect bacterial hosts in the phylum Actinobacteria show them to not only be diverse but also pervasively mosaic, and replete with genes of unknown function. To further explore this broad group of bacteriophages, we describe here the isolation and genomic characterization of 116 phages that infect Microbacterium spp. Most of the phages are lytic, and can be grouped into twelve clusters according to their overall relatedness; seven of the phages are singletons with no close relatives. Genome sizes vary from 17.3 kbp to 97.7 kbp, and their G+C% content ranges from 51.4% to 71.4%, compared to ~67% for their Microbacterium hosts. The phages were isolated on five different Microbacterium species, but typically do not efficiently infect strains beyond the one on which they were isolated. These Microbacterium phages contain many novel features, including very large viral genes (13.5 kbp) and unusual fusions of structural proteins, including a fusion of VIP2 toxin and a MuF-like protein into a single gene. These phages and their genetic components such as integration systems, recombineering tools, and phage-mediated delivery systems, will be useful resources for advancing Microbacterium genetics.

SUBMITTER: Jacobs-Sera D

PROVIDER: S-EPMC7302621 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Genomic diversity of bacteriophages infecting Microbacterium spp.

Jacobs-Sera Deborah D Abad Lawrence A LA Alvey Richard M RM Anders Kirk R KR Aull Haley G HG Bhalla Suparna S SS Blumer Lawrence S LS Bollivar David W DW Bonilla J Alfred JA Butela Kristen A KA Coomans Roy J RJ Cresawn Steven G SG D'Elia Tom T Diaz Arturo A Divens Ashley M AM Edgington Nicholas P NP Frederick Gregory D GD Gainey Maria D MD Garlena Rebecca A RA Grant Kenneth W KW Gurney Susan M R SMR Hendrickson Heather L HL Hughes Lee E LE Kenna Margaret A MA Klyczek Karen K KK Kotturi Hari H Mavrich Travis N TN McKinney Angela L AL Merkhofer Evan C EC Moberg Parker Jordan J Molloy Sally D SD Monti Denise L DL Pape-Zambito Dana A DA Pollenz Richard S RS Pope Welkin H WH Reyna Nathan S NS Rinehart Claire A CA Russell Daniel A DA Shaffer Christopher D CD Sivanathan Viknesh V Stoner Ty H TH Stukey Joseph J Sunnen C Nicole CN Tolsma Sara S SS Tsourkas Philippos K PK Wallen Jamie R JR Ware Vassie C VC Warner Marcie H MH Washington Jacqueline M JM Westover Kristi M KM Whitefleet-Smith JoAnn L JL Wiersma-Koch Helen I HI Williams Daniel C DC Zack Kira M KM Hatfull Graham F GF

PloS one 20200618 6

The bacteriophage population is vast, dynamic, old, and genetically diverse. The genomics of phages that infect bacterial hosts in the phylum Actinobacteria show them to not only be diverse but also pervasively mosaic, and replete with genes of unknown function. To further explore this broad group of bacteriophages, we describe here the isolation and genomic characterization of 116 phages that infect Microbacterium spp. Most of the phages are lytic, and can be grouped into twelve clusters accord ...[more]

PMID: 32555720

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Project description:BackgroundBacteriophages are bacterial parasites and are considered the most abundant and diverse biological entities on the planet. Previously we identified 154 prophages from 151 serovars of Salmonella enterica subsp. enterica. A detailed analysis of Salmonella prophage genomics is required given the influence of phages on their bacterial hosts and should provide a broader understanding of Salmonella biology and virulence and contribute to the practical applications of phages as vectors and antibacterial agents.ResultsHere we provide a comparative analysis of the full genome sequences of 142 prophages of Salmonella enterica subsp. enterica which is the full complement of the prophages that could be retrieved from public databases. We discovered extensive variation in genome sizes (ranging from 6.4 to 358.7 kb) and guanine plus cytosine (GC) content (ranging from 35.5 to 65.4%) and observed a linear correlation between the genome size and the number of open reading frames (ORFs). We used three approaches to compare the phage genomes. The NUCmer/MUMmer genome alignment tool was used to evaluate linkages and correlations based on nucleotide identity between genomes. Multiple sequence alignment was performed to calculate genome average nucleotide identity using the Kalgin program. Finally, genome synteny was explored using dot plot analysis. We found that 90 phage genome sequences grouped into 17 distinct clusters while the remaining 52 genomes showed no close relationships with the other phage genomes and are identified as singletons. We generated genome maps using nucleotide and amino acid sequences which allowed protein-coding genes to be sorted into phamilies (phams) using the Phamerator software. Out of 5796 total assigned phamilies, one phamily was observed to be dominant and was found in 49 prophages, or 34.5% of the 142 phages in our collection. A majority of the phamilies, 4330 out of 5796 (74.7%), occurred in just one prophage underscoring the high degree of diversity among Salmonella bacteriophages.ConclusionsBased on nucleotide and amino acid sequences, a high diversity was found among Salmonella bacteriophages which validate the use of prophage sequence analysis as a highly discriminatory subtyping tool for Salmonella. Thorough understanding of the conservation and variation of prophage genomic characteristics will facilitate their rational design and use as tools for bacterial strain construction, vector development and as anti-bacterial agents.

Dataset Information

Genomic diversity of bacteriophages infecting Microbacterium spp.

Publications

Genomic diversity of bacteriophages infecting Microbacterium spp.

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