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1. Cluster K mycobacteriophages: insights into the evolutionary origins of mycobacteriophage TM4.

Author

Welkin H Pope, Christina M Ferreira, Deborah Jacobs-Sera, Robert C Benjamin, Ariangela J Davis, Randall J DeJong, Sarah C R Elgin, Forrest R Guilfoile, Mark H Forsyth, Alexander D Harris, Samuel E Harvey, Lee E Hughes, Peter M Hynes, Arrykka S Jackson, Marilyn D Jalal, Elizabeth A MacMurray, Coreen M Manley, Molly J McDonough, Jordan L Mosier, Larissa J Osterbann, Hannah S Rabinowitz, Corwin N Rhyan, Daniel A Russell, Margaret S Saha, Christopher D Shaffer, Stephanie E Simon, Erika F Sims, Isabel G Tovar, Emilie G Weisser, John T Wertz, Kathleen A Weston-Hafer, Kurt E Williamson, Bo Zhang, Steven G Cresawn, Paras Jain, Mariana Piuri, William R Jacobs, Roger W Hendrix, and Graham F Hatfull

Subjects
Medicine, Science
Abstract

Five newly isolated mycobacteriophages--Angelica, CrimD, Adephagia, Anaya, and Pixie--have similar genomic architectures to mycobacteriophage TM4, a previously characterized phage that is widely used in mycobacterial genetics. The nucleotide sequence similarities warrant grouping these into Cluster K, with subdivision into three subclusters: K1, K2, and K3. Although the overall genome architectures of these phages are similar, TM4 appears to have lost at least two segments of its genome, a central region containing the integration apparatus, and a segment at the right end. This suggests that TM4 is a recent derivative of a temperate parent, resolving a long-standing conundrum about its biology, in that it was reportedly recovered from a lysogenic strain of Mycobacterium avium, but it is not capable of forming lysogens in any mycobacterial host. Like TM4, all of the Cluster K phages infect both fast- and slow-growing mycobacteria, and all of them--with the exception of TM4--form stable lysogens in both Mycobacterium smegmatis and Mycobacterium tuberculosis; immunity assays show that all five of these phages share the same immune specificity. TM4 infects these lysogens suggesting that it was either derived from a heteroimmune temperate parent or that it has acquired a virulent phenotype. We have also characterized a widely-used conditionally replicating derivative of TM4 and identified mutations conferring the temperature-sensitive phenotype. All of the Cluster K phages contain a series of well conserved 13 bp repeats associated with the translation initiation sites of a subset of the genes; approximately one half of these contain an additional sequence feature composed of imperfectly conserved 17 bp inverted repeats separated by a variable spacer. The K1 phages integrate into the host tmRNA and the Cluster K phages represent potential new tools for the genetics of M. tuberculosis and related species.

Published
2011
Full Text
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2. Expanding the diversity of mycobacteriophages: insights into genome architecture and evolution.

Author

Welkin H Pope, Deborah Jacobs-Sera, Daniel A Russell, 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, Manuel Ares, Amanda J Barber, Lucia P Barker, Jonathan M Barrett, William D Barshop, Cynthia M Bauerle, Ian M Bayles, Katherine L Belfield, Aaron A Best, Agustin Borjon, 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, and Graham F Hatfull

Subjects
Medicine, Science
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.

Published
2011
Full Text
View/download PDF

3. Cluster K Mycobacteriophages: Insights into the Evolutionary Origins of Mycobacteriophage TM4

Author

Paras Jain, Kurt E. Williamson, Welkin H. Pope, Marilyn D. Jalal, Sarah C. R. Elgin, Graham F. Hatfull, Daniel A. Russell, Emilie G. Weisser, Margaret S. Saha, John T. Wertz, Forrest R. Guilfoile, Randall J. DeJong, Bo Zhang, Mariana Piuri, Molly J. McDonough, Steven G. Cresawn, Arrykka S. Jackson, Christopher D. Shaffer, Samuel E. Harvey, Lee E. Hughes, Deborah Jacobs-Sera, Kathleen Weston-Hafer, Robert C. Benjamin, Mark H. Forsyth, Coreen M. Manley, Stephanie E. Simon, Christina M. Ferreira, Corwin N. Rhyan, Peter M. Hynes, H. S. Rabinowitz, Elizabeth A. MacMurray, Roger W. Hendrix, Alexander D. Harris, Ariangela J. Davis, William R. Jacobs, Erika Fieldman Sims, Larissa J. Osterbann, Jordan L. Mosier, and Isabel G. Tovar

Subjects
Bacterial Diseases, viruses, lcsh:Medicine, Virus Replication, Genome, Conserved sequence, purl.org/becyt/ford/1 [https], Lysogen, Viral classification, Cluster Analysis, Bacteriophages, Genome Sequencing, lcsh:Science, Genome Evolution, Conserved Sequence, Genetics, Multidisciplinary, Mycobacteriophages, biology, Mycobacteriophage, Mycobacterium smegmatis, Temperature, Chromosome Mapping, Genomics, Infectious Diseases, Medical Microbiology, Multigene Family, Attachment Sites, Microbiological, Medicine, CIENCIAS NATURALES Y EXACTAS, Research Article, Otras Ciencias Biológicas, Virus Integration, Molecular Sequence Data, Genome, Viral, Microbiology, Viral Evolution, Mycobacterium, Ciencias Biológicas, Evolution, Molecular, Viral Proteins, Lysogenic cycle, Virology, TM4, purl.org/becyt/ford/1.6 [https], Biology, Comparative genomics, Evolutionary Biology, Base Sequence, lcsh:R, Virion, Bacteriology, Molecular Sequence Annotation, Sequence Analysis, DNA, Comparative Genomics, biology.organism_classification, Mutation, Cluster K, lcsh:Q, DNA viruses, Gene Deletion
Abstract

Five newly isolated mycobacteriophages -Angelica, CrimD, Adephagia, Anaya, and Pixie - have similar genomic architectures to mycobacteriophage TM4, a previously characterized phage that is widely used in mycobacterial genetics. The nucleotide sequence similarities warrant grouping these into Cluster K, with subdivision into three subclusters: K1, K2, and K3. Although the overall genome architectures of these phages are similar, TM4 appears to have lost at least two segments of its genome, a central region containing the integration apparatus, and a segment at the right end. This suggests that TM4 is a recent derivative of a temperate parent, resolving a long-standing conundrum about its biology, in that it was reportedly recovered from a lysogenic strain of Mycobacterium avium, but it is not capable of forming lysogens in any mycobacterial host. Like TM4, all of the Cluster K phages infect both fast- and slow-growing mycobacteria, and all of them - with the exception of TM4 - form stable lysogens in both Mycobacterium smegmatis and Mycobacterium tuberculosis; immunity assays show that all five of these phages share the same immune specificity. TM4 infects these lysogens suggesting that it was either derived from a heteroimmune temperate parent or that it has acquired a virulent phenotype. We have also characterized a widely-used conditionally replicating derivative of TM4 and identified mutations conferring the temperature-sensitive phenotype. All of the Cluster K phages contain a series of well conserved 13 bp repeats associated with the translation initiation sites of a subset of the genes; approximately one half of these contain an additional sequence feature composed of imperfectly conserved 17 bp inverted repeats separated by a variable spacer. The K1 phages integrate into the host tmRNA and the Cluster K phages represent potential new tools for the genetics of M. tuberculosis and related species. © 2011 Pope et al. Fil: Pope, Welkin H.. University of Pittsburgh; Estados Unidos Fil: Ferreira, Christina M.. University of Pittsburgh; Estados Unidos Fil: Jacobs Sera, Deborah. University of Pittsburgh; Estados Unidos Fil: Benjamin, Robert C.. University of North Texas; Estados Unidos Fil: Davis, Ariangela J.. Calvin College; Estados Unidos Fil: DeJong, Randall J.. Calvin College; Estados Unidos Fil: Elgin, Sarah C. R.. Washington University in St. Louis; Estados Unidos Fil: Guilfoile, Forrest R.. University of Pittsburgh; Estados Unidos Fil: Forsyth, Mark H.. The College Of William And Mary; Estados Unidos Fil: Harris, Alexander D.. Calvin College; Estados Unidos Fil: Harvey, Samuel E.. The College Of William And Mary; Estados Unidos Fil: Hughes, Lee E.. University of North Texas; Estados Unidos Fil: Hynes, Peter M.. Washington University in St. Louis; Estados Unidos Fil: Jackson, Arrykka S.. The College Of William And Mary; Estados Unidos Fil: Jalal, Marilyn D.. University of North Texas; Estados Unidos Fil: MacMurray, Elizabeth A.. The College Of William And Mary; Estados Unidos Fil: Manley, Coreen M.. University of North Texas; Estados Unidos Fil: McDonough, Molly J.. The College Of William And Mary; Estados Unidos Fil: Mosier, Jordan L.. University of North Texas; Estados Unidos Fil: Osterbann, Larissa J.. Calvin College; Estados Unidos Fil: Rabinowitz, Hannah S.. Washington University in St. Louis; Estados Unidos Fil: Rhyan, Corwin N.. Washington University in St. Louis; Estados Unidos Fil: Russell, Daniel A.. University of Pittsburgh; Estados Unidos Fil: Saha, Margaret S.. The College Of William And Mary; Estados Unidos Fil: Shaffer, Christopher D.. Washington University in St. Louis; Estados Unidos Fil: Simon, Stephanie E.. University of North Texas; Estados Unidos Fil: Sims, Erika F.. Washington University in St. Louis; Estados Unidos Fil: Tovar, Isabel G.. University of North Texas; Estados Unidos Fil: Weisser, Emilie G.. Washington University in St. Louis; Estados Unidos Fil: Wertz, John T.. Calvin College; Estados Unidos Fil: Weston-Hafer, Kathleen A.. Washington University in St. Louis; Estados Unidos Fil: Williamson, Kurt E.. The College Of William And Mary; Estados Unidos Fil: Zhang, Bo. Washington University in St. Louis; Estados Unidos Fil: Cresawn, Steven G.. James Madison University; Estados Unidos Fil: Jain, Paras. Albert Einstein College Of Medicine Of Yeshiva University; Estados Unidos Fil: Piuri, Mariana. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. University of Pittsburgh; Estados Unidos Fil: Jacobs, William R.. Albert Einstein College Of Medicine Of Yeshiva University; Estados Unidos Fil: Hendrix, Roger W.. University of Pittsburgh; Estados Unidos Fil: Hatfull, Graham F.. University of Pittsburgh; Estados Unidos

Published
2011

4. Expanding the diversity of mycobacteriophages: insights into genome architecture and evolution

Author

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

Subjects
Genome evolution, Science Policy, Mycobacteriophage, Population, lcsh:Medicine, Genome, Viral, Biology, Microbiology, Genome, 03 medical and health sciences, Virology, education, lcsh:Science, Genome Evolution, 030304 developmental biology, Genetics, Comparative genomics, 0303 health sciences, education.field_of_study, Multidisciplinary, Base Sequence, Geography, Mycobacteriophages, 030306 microbiology, lcsh:R, Genetic Variation, Sequence Analysis, DNA, Genomics, Comparative Genomics, Biological Evolution, United States, 3. Good health, Science Education, Evolutionary biology, Viral evolution, DNA, Viral, lcsh:Q, Mobile genetic elements, Research Article
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.

Published
2011

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