Expanding the diversity of mycobacteriophages: Insights into genome architecture and evolution

Welkin H. Pope, Deborah Jacobs-Sera, Daniel A. Russel, Craig L. Peebles, Zein Al-Atrache, Turi A. Alcoser, Lisa M. Alexander, Matthew B. Alfano, Samantha T. Alford, Nichols E. Amy, Marie D. Anderson, Alexander G. Anderson, Andrew A.S. Ang, Ares Manuel, Amanda J. Barber, Lucia P. Barker, Jonathan M. Barrett, William D. Barshop, Cynthia M. Bauerle, Ian M. BaylesKatherine L. Belfield, Aaron A. Best, Borjon Agustin, Charles A. Bowman, Christine A. Boyer, Kevin W. Bradley, Victoria A. Bradley, Lauren N. Broadway, Keshav Budwal, Kayla N. Busby, Ian W. Campbell, Anne M. Campbell, Alyssa Carey, Steven M. Caruso, Rebekah D. Chew, Chelsea L. Cockburn, Lianne B. Cohen, Jeffrey M. Corajod, Steven G. Cresawn, Kimberly R. Davis, Lisa Deng, Dee R. Denver, Breyon R. Dixon, Sahrish Ekram, Sarah C.R. Elgin, Angela E. Engelsen, Belle E.V. English, Marcella L. Erb, Crystal Estrada, Laura Z. Filliger, Ann M. Findley, Lauren Forbes, Mark H. Forsyth, Tyler M. Fox, Melissa J. Fritz, Roberto Garcia, Zindzi D. George, Anne E. Georges, Christopher R. Gissendanner, Shannon Goff, Rebecca Goldstein, Kobie C. Gordon, Russell D. Green, Stephanie L. Guerra, Krysta R. Guiney-Olsen, Bridget G. Guiza, Leila Haghighat, Garrett V. Hagopian, Catherine J. Harmon, Jeremy S. Harmson, Grant A. Hartzog, Samuel E. Harvey, Siping He, Kevin J. He, Kaitlin E. Healy, Ellen R. Higinbotham, Erin N. Hildebrandt, Jason H. Ho, Gina M. Hogan, Victoria G. Hohenstein, Nathan A. Holz, Vincent J. Huang, Ericka L. Hufford, Peter M. Hynes, Arrykka S. Jackson, Erica C. Jansen, Jonathan Jarvik, Paul G. Jasinto, Tuajuanda C. Jordan, Tomas Kasza, Murray A. Katelyn, Jessica S. Kelsey, Larisa A. Kerrigan, Daryl Khaw, Junghee Kim, Justin Z. Knutter, Ching Chung Ko, Gail V. Larkin, Jennifer R. Laroche, Asma Latif, Kohana D. Leuba, Sequoia I. Leuba, Lynn O. Lewis, Kathryn E. Loesser-Casey, Courtney A. Long, A. Javier Lopez, Nicholas Lowery, Tina Q. Lu, Victor Mac, Isaac R. Masters, Jazmyn J. Mccloud, Molly J. Mcdonough, Andrew J. Medenbach, Anjali Menon, Rachel Miller, Brandon K. Morgan, Patrick C. Ng, Elvis Nguyen, Katrina T. Nguyen, Emilie T. Nguyen, Kaylee M. Nicholson, Lindsay A. Parnell, Caitlin E. Peirce, Allison M. Perz, Luke J. Peterson, Rachel E. Pferdehirt, Seegren V. Philip, Kit Pogliano, Joe Pogliano, Tamsen Polley, Erica J. Puopolo, Hannah S. Rabinowitz, Michael J. Resiss, Corwin N. Rhyan, Yetta M. Robinson, Lauren L. Rodriguez, Andrew C. Rose, Jeffrey D. Rubin, Jessica A. Ruby, Margaret S. Saha, James W. Sandoz, Judith Savitskaya, Dale J. Schipper, Christine E. Schnitzler, Amanda R. Schott, J. Bradley Segal, Christopher D. Shaffer, Kathryn E. Sheldon, Erica M. Shepard, Jonathan W. Shepardson, Madav K. Shroff, Jessica M. Simmons, Erika F. Simms, Brandy M. Simpson, Kathryn M. Sinclair, Robert L. Sjoholm, Ingrid J. Slette, Blaire C. Spaulding, Clark L. Straub, Joseph Stukey, Trevor Sughrue, Tin Yun Tang, Lyons M. Tatyana, Stephen B. Taylor, Barbara J. Taylor, Louise M. Temple, Jasper V. Thompson, Michael P. Tokarz, Stephanie E. Trapani, Alexander P. Troum, Jonathan Tsay, Anthony T. Tubbs, Jillian M. Walton, Danielle H. Wang, Hannah Wang, John R. Warner, Emilie G. Weisser, Samantha C. Wendler, Kathleen A. Weston-Hafer, Hilary M. Whelan, Kurt E. Williamson, Angelica N. Willis, Hannah S. Wirtshafter, Theresa W. Wong, Phillip Wu, Yun Jeong Yang, Brandon C. Yee, David A. Zaidins, Bo Zhang, Melina Y. Zúniga, Roger W. Hendrix, Graham F. Hatfull

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Abstract

Mycobacteriophages are viruses that infect mycobacterial hosts such as Mycobacterium smegmatis and Mycobacterium tuberculosis. All mycobacteriophages characterized to date are dsDNA tailed phages, and have either siphoviral or myoviral morphotypes. However, their genetic diversity is considerable, and although sixty-two genomes have been sequenced and comparatively analyzed, these likely represent only a small portion of the diversity of the mycobacteriophage population at large. Here we report the isolation, sequencing and comparative genomic analysis of 18 new mycobacteriophages isolated from geographically distinct locations within the United States. Although no clear correlation between location and genome type can be discerned, these genomes expand our knowledge of mycobacteriophage diversity and enhance our understanding of the roles of mobile elements in viral evolution. Expansion of the number of mycobacteriophages grouped within Cluster A provides insights into the basis of immune specificity in these temperate phages, and we also describe a novel example of apparent immunity theft. The isolation and genomic analysis of bacteriophages by freshman college students provides an example of an authentic research experience for novice scientists.

Original languageEnglish
Article numbere16329
JournalPloS one
Volume6
Issue number1
DOIs
StatePublished - Feb 7 2011

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    Pope, W. H., Jacobs-Sera, D., Russel, D. A., Peebles, C. L., Al-Atrache, Z., Alcoser, T. A., Alexander, L. M., Alfano, M. B., Alford, S. T., Amy, N. E., Anderson, M. D., Anderson, A. G., Ang, A. A. S., Manuel, A., Barber, A. J., Barker, L. P., Barrett, J. M., Barshop, W. D., Bauerle, C. M., ... Hatfull, G. F. (2011). Expanding the diversity of mycobacteriophages: Insights into genome architecture and evolution. PloS one, 6(1), [e16329]. https://doi.org/10.1371/journal.pone.0016329