Dataset Information

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

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.

SUBMITTER: Pope WH

PROVIDER: S-EPMC3029335 | biostudies-literature | 2011 Jan

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

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

Pope Welkin H WH Jacobs-Sera Deborah D Russell Daniel A DA Peebles Craig L CL Al-Atrache Zein Z Alcoser Turi A TA Alexander Lisa M LM Alfano Matthew B MB Alford Samantha T ST Amy Nichols E NE Anderson Marie D MD Anderson Alexander G AG Ang Andrew A S AA Ares Manuel M Barber Amanda J AJ Barker Lucia P LP Barrett Jonathan M JM Barshop William D WD Bauerle Cynthia M CM Bayles Ian M IM Belfield Katherine L KL Best Aaron A AA Borjon Agustin A Bowman Charles A CA Boyer Christine A CA Bradley Kevin W KW Bradley Victoria A VA Broadway Lauren N LN Budwal Keshav K Busby Kayla N KN Campbell Ian W IW Campbell Anne M AM Carey Alyssa A Caruso Steven M SM Chew Rebekah D RD Cockburn Chelsea L CL Cohen Lianne B LB Corajod Jeffrey M JM Cresawn Steven G SG Davis Kimberly R KR Deng Lisa L Denver Dee R DR Dixon Breyon R BR Ekram Sahrish S Elgin Sarah C R SC Engelsen Angela E AE English Belle E V BE Erb Marcella L ML Estrada Crystal C Filliger Laura Z LZ Findley Ann M AM Forbes Lauren L Forsyth Mark H MH Fox Tyler M TM Fritz Melissa J MJ Garcia Roberto R George Zindzi D ZD Georges Anne E AE Gissendanner Christopher R CR Goff Shannon S Goldstein Rebecca R Gordon Kobie C KC Green Russell D RD Guerra Stephanie L SL Guiney-Olsen Krysta R KR Guiza Bridget G BG Haghighat Leila L Hagopian Garrett V GV Harmon Catherine J CJ Harmson Jeremy S JS Hartzog Grant A GA Harvey Samuel E SE He Siping S He Kevin J KJ Healy Kaitlin E KE Higinbotham Ellen R ER Hildebrandt Erin N EN Ho Jason H JH Hogan Gina M GM Hohenstein Victoria G VG Holz Nathan A NA Huang Vincent J VJ Hufford Ericka L EL Hynes Peter M PM Jackson Arrykka S AS Jansen Erica C EC Jarvik Jonathan J Jasinto Paul G PG Jordan Tuajuanda C TC Kasza Tomas T Katelyn Murray A MA Kelsey Jessica S JS Kerrigan Larisa A LA Khaw Daryl D Kim Junghee J Knutter Justin Z JZ Ko Ching-Chung CC Larkin Gail V GV Laroche Jennifer R JR Latif Asma A Leuba Kohana D KD Leuba Sequoia I SI Lewis Lynn O LO Loesser-Casey Kathryn E KE Long Courtney A CA Lopez A Javier AJ Lowery Nicholas N Lu Tina Q TQ Mac Victor V Masters Isaac R IR McCloud Jazmyn J JJ McDonough Molly J MJ Medenbach Andrew J AJ Menon Anjali A Miller Rachel R Morgan Brandon K BK Ng Patrick C PC Nguyen Elvis E Nguyen Katrina T KT Nguyen Emilie T ET Nicholson Kaylee M KM Parnell Lindsay A LA Peirce Caitlin E CE Perz Allison M AM Peterson Luke J LJ Pferdehirt Rachel E RE Philip Seegren V SV Pogliano Kit K Pogliano Joe J Polley Tamsen T Puopolo Erica J EJ Rabinowitz Hannah S HS Resiss Michael J MJ Rhyan Corwin N CN Robinson Yetta M YM Rodriguez Lauren L LL Rose Andrew C AC Rubin Jeffrey D JD Ruby Jessica A JA Saha Margaret S MS Sandoz James W JW Savitskaya Judith J Schipper Dale J DJ Schnitzler Christine E CE Schott Amanda R AR Segal J Bradley JB Shaffer Christopher D CD Sheldon Kathryn E KE Shepard Erica M EM Shepardson Jonathan W JW Shroff Madav K MK Simmons Jessica M JM Simms Erika F EF Simpson Brandy M BM Sinclair Kathryn M KM Sjoholm Robert L RL Slette Ingrid J IJ Spaulding Blaire C BC Straub Clark L CL Stukey Joseph J Sughrue Trevor T Tang Tin-Yun TY Tatyana Lyons M LM Taylor Stephen B SB Taylor Barbara J BJ Temple Louise M LM Thompson Jasper V JV Tokarz Michael P MP Trapani Stephanie E SE Troum Alexander P AP Tsay Jonathan J Tubbs Anthony T AT Walton Jillian M JM Wang Danielle H DH Wang Hannah H Warner John R JR Weisser Emilie G EG Wendler Samantha C SC Weston-Hafer Kathleen A KA Whelan Hilary M HM Williamson Kurt E KE Willis Angelica N AN Wirtshafter Hannah S HS Wong Theresa W TW Wu Phillip P Yang Yun jeong Yj Yee Brandon C BC Zaidins David A DA Zhang Bo B Zúniga Melina Y MY Hendrix Roger W RW Hatfull Graham F GF

PloS one 20110127 1

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 ...[more]

PMID: 21298013

Similar Datasets

Project description:Temperate phages encode an immunity system to control lytic gene expression during lysogeny. This gene regulatory circuit consists of multiple interacting genetic elements, and although it is essential for controlling phage growth, it is subject to conflicting evolutionary pressures. During superinfection of a lysogen, the prophage's circuit interacts with the superinfecting phage's circuit and prevents lytic growth if the two circuits are closely related. The circuitry is advantageous since it provides the prophage with a defense mechanism, but the circuitry is also disadvantageous since it limits the phage's host range during superinfection. Evolutionarily related phages have divergent, orthogonal immunity systems that no longer interact and are heteroimmune, but we do not understand how immunity systems evolve new specificities. Here, we use a group of Cluster A mycobacteriophages that exhibit a spectrum of genetic diversity to examine how immunity system evolution impacts superinfection immunity. We show that phages with mesotypic (i.e., genetically related but distinct) immunity systems exhibit asymmetric and incomplete superinfection phenotypes. They form complex immunity networks instead of well-defined immunity groups, and mutations conferring escape (i.e., virulence) from homotypic or mesotypic immunity have various escape specificities. Thus, virulence and the evolution of new immune specificities are shaped by interactions with homotypic and mesotypic immunity systems.IMPORTANCE Many aspects regarding superinfection, immunity, virulence, and the evolution of immune specificities are poorly understood due to the lack of large collections of isolated and sequenced phages with a spectrum of genetic diversity. Using a genetically diverse collection of Cluster A phages, we show that the classical and relatively straightforward patterns of homoimmunity, heteroimmunity, and virulence result from interactions between homotypic and heterotypic phages at the extreme edges of an evolutionary continuum of immune specificities. Genetic interactions between mesotypic phages result in more complex mesoimmunity phenotypes and virulence profiles. These results highlight that the evolution of immune specificities can be shaped by homotypic and mesotypic interactions and may be more dynamic than previously considered.

Project description:Inteins are self-splicing protein elements that are mobile at the DNA level and are sporadically distributed across microbial genomes. Inteins appear to be horizontally transferred, and it has been speculated that phages may play a role in intein distribution. Our attention turns to mycobacteriophages, which infect mycobacteria, where both phage and host harbor inteins. Using bioinformatics, mycobacteriophage genomes were mined for inteins. This study reveals that these mobile elements are present across multiple mycobacteriophage clusters and are pervasive in certain genes, like the large terminase subunit TerL and a RecB-like nuclease, with the majority of intein-containing genes being phage specific. Strikingly, despite this phage specificity, inteins localize to functional motifs shared with bacteria, such that intein-containing genes have similar roles, like hydrolase activity and nucleic acid binding, indicating a global commonality among intein-hosting proteins. Additionally, there are multiple insertion points within active centers, implying independent invasion events, with regulatory implications. Several phage inteins were shown to be splicing competent and to encode functional homing endonucleases, important for mobility. Further, bioinformatic analysis supports the potential for phages as facilitators of intein movement among mycobacteria and related genera. Analysis of catalytic intein residues finds the highly conserved penultimate histidine inconsistently maintained among mycobacteriophages. Biochemical characterization of a noncanonical phage intein shows that this residue influences precursor accumulation, suggesting that splicing has been tuned in phages to modulate generation of important proteins. Together, this work expands our understanding of phage-based intein dissemination and evolution and implies that phages provide a context for evolution of splicing-based regulation. Inteins are mobile protein splicing elements found in critical genes across all domains of life. Mycobacterial inteins are of particular interest because of their occurrence in pathogenic species, such as Mycobacterium tuberculosis and Mycobacterium leprae, which harbor inteins in important proteins. We have discovered a similarity in activities of intein-containing proteins among mycobacteriophages and their intein-rich actinobacterial hosts, with implications for both posttranslational regulation by inteins and phages participating in horizontal intein transfer. Our demonstration of multiple insertion points within active centers of phage proteins implies independent invasion events, indicating the importance of intein maintenance at specific functional sites. The variable conservation of a catalytic splicing residue, leading to profoundly altered splicing rates, points to the regulatory potential of inteins and to mycobacteriophages playing a role in intein evolution. Collectively, these results suggest inteins as posttranslational regulators and mycobacteriophages as both vehicles for intein distribution and incubators for intein evolution.

Dataset Information

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

Publications

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

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets