Genomic diversity of bacteriophages infecting Microbacterium spp.

Deborah Jacobs-Sera; Lawrence A. Abad; Richard M. Alvey; Kirk R. Anders; Haley G. Aull; Suparna S. Bhalla; Lawrence S. Blumer; David W. Bollivar; J. Alfred Bonilla; Kristen A.  Butela; Roy J. Coomans; Steven G. Cresawn; Tom D'Elia; Arturo Diaz; Ashley M. Divens; Nicholas P. Edgington; Gregory D. Frederick; Maria D. Gainey; Rebecca A. Garlena; Kenneth W. Grant; Susan Margaret Robertson Gurney; Heather L. Hendrickson; Lee E. Hughes; Margaret A. Kenna; Karen K. Klyczek; Hari Kotturi; Travis N. Mavrich; Angela L. McKinney; Evan C. Merkhofer; Jordan Moberg Parker; Sally D. Molloy; Denise L. Monti; Dana A. Pape-Zambito; Richard S. Pollenz; Welkin H. Pope; Nathan S. Reyna; Claire A. Rinehart; Daniel A. Russell; Christopher D. Shaffer; Viknesh Sivanathan; Ty H. Stoner; Joseph Stukey; C. Nicole Sunnen; Sara S. Tolsma; Philippos K. Tsourkas; Jamie R. Wallen; Vassie C. Ware; Marcie H. Warner; Jacqueline M. Washington; Kristi M. Westover; JoAnn L. Whitefleet-Smith; Helen I. Wiersma-Koch; Daniel C. Williams; Kira M. Zack; Graham F. Hatfull

doi:10.1371/journal.pone.0234636

Genomic diversity of bacteriophages infecting Microbacterium spp.

Deborah Jacobs-Sera, Lawrence A. Abad, Richard M. Alvey, Kirk R. Anders, Haley G. Aull, Suparna S. Bhalla, Lawrence S. Blumer, David W. Bollivar, J. Alfred Bonilla, Kristen A. Butela, Roy J. Coomans, Steven G. Cresawn, Tom D'Elia, Arturo Diaz, Ashley M. Divens, Nicholas P. Edgington, Gregory D. Frederick, Maria D. Gainey, Rebecca A. Garlena, Kenneth W. GrantSusan Margaret Robertson Gurney, Heather L. Hendrickson, Lee E. Hughes, Margaret A. Kenna, Karen K. Klyczek, Hari Kotturi, Travis N. Mavrich, Angela L. McKinney, Evan C. Merkhofer, Jordan Moberg Parker, Sally D. Molloy, Denise L. Monti, Dana A. Pape-Zambito, Richard S. Pollenz, Welkin H. Pope, Nathan S. Reyna, Claire A. Rinehart, Daniel A. Russell, Christopher D. Shaffer, Viknesh Sivanathan, Ty H. Stoner, Joseph Stukey, C. Nicole Sunnen, Sara S. Tolsma, Philippos K. Tsourkas, Jamie R. Wallen, Vassie C. Ware, Marcie H. Warner, Jacqueline M. Washington, Kristi M. Westover, JoAnn L. Whitefleet-Smith, Helen I. Wiersma-Koch, Daniel C. Williams, Kira M. Zack, Graham F. Hatfull

School of Biology

Research output: Contribution to journal › Article › peer-review

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.

Original language	English
Article number	e0234636
Number of pages	41
Journal	PLoS One
Volume	15
Issue number	6
DOIs	https://doi.org/10.1371/journal.pone.0234636
Publication status	Published - 2020

Access to Document

10.1371/journal.pone.0234636Licence: CC BY

Cite this

Jacobs-Sera, D., Abad, L. A., Alvey, R. M., Anders, K. R., Aull, H. G., Bhalla, S. S., Blumer, L. S., Bollivar, D. W., Bonilla, J. A., Butela, K. A., Coomans, R. J., Cresawn, S. G., D'Elia, T., Diaz, A., Divens, A. M., Edgington, N. P., Frederick, G. D., Gainey, M. D., Garlena, R. A., ... Hatfull, G. F. (2020). Genomic diversity of bacteriophages infecting Microbacterium spp. PLoS One, 15(6), Article e0234636. https://doi.org/10.1371/journal.pone.0234636

@article{17e11f798ad34b098bbf53d8caa4cb2f,

title = "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.",

author = "Deborah Jacobs-Sera and Abad, {Lawrence A.} and Alvey, {Richard M.} and Anders, {Kirk R.} and Aull, {Haley G.} and Bhalla, {Suparna S.} and Blumer, {Lawrence S.} and Bollivar, {David W.} and Bonilla, {J. Alfred} and Butela, {Kristen A.} and Coomans, {Roy J.} and Cresawn, {Steven G.} and Tom D'Elia and Arturo Diaz and Divens, {Ashley M.} and Edgington, {Nicholas P.} and Frederick, {Gregory D.} and Gainey, {Maria D.} and Garlena, {Rebecca A.} and Grant, {Kenneth W.} and Gurney, {Susan Margaret Robertson} and Hendrickson, {Heather L.} and Hughes, {Lee E.} and Kenna, {Margaret A.} and Klyczek, {Karen K.} and Hari Kotturi and Mavrich, {Travis N.} and McKinney, {Angela L.} and Merkhofer, {Evan C.} and Parker, {Jordan Moberg} and Molloy, {Sally D.} and Monti, {Denise L.} and Pape-Zambito, {Dana A.} and Pollenz, {Richard S.} and Pope, {Welkin H.} and Reyna, {Nathan S.} and Rinehart, {Claire A.} and Russell, {Daniel A.} and Shaffer, {Christopher D.} and Viknesh Sivanathan and Stoner, {Ty H.} and Joseph Stukey and Sunnen, {C. Nicole} and Tolsma, {Sara S.} and Tsourkas, {Philippos K.} and Wallen, {Jamie R.} and Ware, {Vassie C.} and Warner, {Marcie H.} and Washington, {Jacqueline M.} and Westover, {Kristi M.} and Whitefleet-Smith, {JoAnn L.} and Wiersma-Koch, {Helen I.} and Williams, {Daniel C.} and Zack, {Kira M.} and Hatfull, {Graham F.}",

note = "Funding: This work was supported by grants from the National Institutes of Health (GM116884 and GM131729; https://www.nih.gov/) and Howard Hughes Medical Institute (54308198 and GT12053; https://www.hhmi.org) to GFH. Work performed by M.D.G and J.R.W was supported by a Provost Internal Support grant from Western Carolina University. HHMI supported the SEA-PHAGES program that generated the data and analyses (data collection and analysis), and supported a workshop where genomic data was analyzed for manuscript preparation.",

year = "2020",

doi = "10.1371/journal.pone.0234636",

language = "English",

volume = "15",

journal = "PLoS One",

issn = "1932-6203",

publisher = "Public Library of Science",

number = "6",

}

Jacobs-Sera, D, Abad, LA, Alvey, RM, Anders, KR, Aull, HG, Bhalla, SS, Blumer, LS, Bollivar, DW, Bonilla, JA, Butela, KA, Coomans, RJ, Cresawn, SG, D'Elia, T, Diaz, A, Divens, AM, Edgington, NP, Frederick, GD, Gainey, MD, Garlena, RA, Grant, KW, Gurney, SMR, Hendrickson, HL, Hughes, LE, Kenna, MA, Klyczek, KK, Kotturi, H, Mavrich, TN, McKinney, AL, Merkhofer, EC, Parker, JM, Molloy, SD, Monti, DL, Pape-Zambito, DA, Pollenz, RS, Pope, WH, Reyna, NS, Rinehart, CA, Russell, DA, Shaffer, CD, Sivanathan, V, Stoner, TH, Stukey, J, Sunnen, CN, Tolsma, SS, Tsourkas, PK, Wallen, JR, Ware, VC, Warner, MH, Washington, JM, Westover, KM, Whitefleet-Smith, JL, Wiersma-Koch, HI, Williams, DC, Zack, KM & Hatfull, GF 2020, 'Genomic diversity of bacteriophages infecting Microbacterium spp.', PLoS One, vol. 15, no. 6, e0234636. https://doi.org/10.1371/journal.pone.0234636

TY - JOUR

T1 - Genomic diversity of bacteriophages infecting Microbacterium spp.

AU - Jacobs-Sera, Deborah

AU - Abad, Lawrence A.

AU - Alvey, Richard M.

AU - Anders, Kirk R.

AU - Aull, Haley G.

AU - Bhalla, Suparna S.

AU - Blumer, Lawrence S.

AU - Bollivar, David W.

AU - Bonilla, J. Alfred

AU - Butela, Kristen A.

AU - Coomans, Roy J.

AU - Cresawn, Steven G.

AU - D'Elia, Tom

AU - Diaz, Arturo

AU - Divens, Ashley M.

AU - Edgington, Nicholas P.

AU - Frederick, Gregory D.

AU - Gainey, Maria D.

AU - Garlena, Rebecca A.

AU - Grant, Kenneth W.

AU - Gurney, Susan Margaret Robertson

AU - Hendrickson, Heather L.

AU - Hughes, Lee E.

AU - Kenna, Margaret A.

AU - Klyczek, Karen K.

AU - Kotturi, Hari

AU - Mavrich, Travis N.

AU - McKinney, Angela L.

AU - Merkhofer, Evan C.

AU - Parker, Jordan Moberg

AU - Molloy, Sally D.

AU - Monti, Denise L.

AU - Pape-Zambito, Dana A.

AU - Pollenz, Richard S.

AU - Pope, Welkin H.

AU - Reyna, Nathan S.

AU - Rinehart, Claire A.

AU - Russell, Daniel A.

AU - Shaffer, Christopher D.

AU - Sivanathan, Viknesh

AU - Stoner, Ty H.

AU - Stukey, Joseph

AU - Sunnen, C. Nicole

AU - Tolsma, Sara S.

AU - Tsourkas, Philippos K.

AU - Wallen, Jamie R.

AU - Ware, Vassie C.

AU - Warner, Marcie H.

AU - Washington, Jacqueline M.

AU - Westover, Kristi M.

AU - Whitefleet-Smith, JoAnn L.

AU - Wiersma-Koch, Helen I.

AU - Williams, Daniel C.

AU - Zack, Kira M.

AU - Hatfull, Graham F.

N1 - Funding: This work was supported by grants from the National Institutes of Health (GM116884 and GM131729; https://www.nih.gov/) and Howard Hughes Medical Institute (54308198 and GT12053; https://www.hhmi.org) to GFH. Work performed by M.D.G and J.R.W was supported by a Provost Internal Support grant from Western Carolina University. HHMI supported the SEA-PHAGES program that generated the data and analyses (data collection and analysis), and supported a workshop where genomic data was analyzed for manuscript preparation.

PY - 2020

Y1 - 2020

N2 - 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.

AB - 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.

U2 - 10.1371/journal.pone.0234636

DO - 10.1371/journal.pone.0234636

M3 - Article

SN - 1932-6203

VL - 15

JO - PLoS One

JF - PLoS One

IS - 6

M1 - e0234636

ER -

Genomic diversity of bacteriophages infecting Microbacterium spp.

Abstract

Access to Document

Fingerprint

Cite this