1932

Abstract

Research opportunities for undergraduate students are strongly advantageous, but implementation at a large scale presents numerous challenges. The enormous diversity of the bacteriophage population and a supportive programmatic structure provide opportunities to engage early-career undergraduates in phage discovery, genomics, and genetics. The Science Education Alliance (SEA) is an inclusive Research-Education Community (iREC) providing centralized programmatic support for students and faculty without prior experience in virology at institutions from community colleges to research-active universities to participate in two course-based projects, SEA-PHAGES (SEA Phage Hunters Advancing Genomic and Evolutionary Science) and SEA-GENES (SEA Gene-function Exploration by a Network of Emerging Scientists). Since 2008, the SEA has supported more than 50,000 undergraduate researchers who have isolated more than 23,000 bacteriophages of which more than 4,500 are fully sequenced and annotated. Students have functionally characterized hundreds of phage genes, and the phage collection has fueled the therapeutic use of phages for treatment of infections. Participation in the SEA promotes student persistence in science education, and its inclusivity promotes a more equitable scientific community.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-113023-110757
2024-09-26
2025-02-13
Loading full text...

Full text loading...

/deliver/fulltext/virology/11/1/annurev-virology-113023-110757.html?itemId=/content/journals/10.1146/annurev-virology-113023-110757&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Natl. Acad. Sci. Technol. Eng. Med. 2017.. Undergraduate Research Experiences for STEM Students: Successes, Challenges, and Opportunities. Washington, DC:: Natl. Acad. Press
    [Google Scholar]
  2. 2.
    Russell SH, Hancock MP, McCullough J. 2007.. Benefits of undergraduate research experiences. . Science 316:(5824):54849
    [Crossref] [Google Scholar]
  3. 3.
    Natl. Acad. Sci. Technol. Eng. Med. 2023.. Advancing Antiracism, Diversity, Equity, and Inclusion in STEMM Organizations: Beyond Broadening Participation. Washington, DC:: Natl. Acad. Press
    [Google Scholar]
  4. 4.
    Rodenbusch SE, Hernandez PR, Simmons SL, Dolan EL. 2016.. Early engagement in course-based research increases graduation rates and completion of science, engineering, and mathematics degrees. . CBE—Life Sci. Educ. 15:(2):ar20
    [Crossref] [Google Scholar]
  5. 5.
    Estrada M, Hernandez PR, Schultz PW. 2018.. A longitudinal study of how quality mentorship and research experience integrate underrepresented minorities into STEM careers. . CBE—Life Sci. Educ. 17:(1):ar9
    [Crossref] [Google Scholar]
  6. 6.
    Asai DJ. 2020.. Race matters. . Cell 181:(4):75457 6. A commentary emphasizing changing the culture of science by putting inclusive diversity at the center.
    [Crossref] [Google Scholar]
  7. 7.
    Eagan MK, Sharkness J, Hurtado S, Mosqueda CM, Chang MJ. 2011.. Engaging undergraduates in science research: not just about faculty willingness. . Res. High Educ. 52:(2):15177
    [Crossref] [Google Scholar]
  8. 8.
    Community Coll. Res. Cent. 2024.. Community college FAQs. . Community College Research Center. https://ccrc.tc.columbia.edu/community-college-faqs.html
    [Google Scholar]
  9. 9.
    Am. Assoc. Community Coll. 2023.. Fast facts 2023. . American Association of Community Colleges. https://www.aacc.nche.edu/wp-content/uploads/2023/03/AACC2023_FastFacts.pdf
    [Google Scholar]
  10. 10.
    Bangera G, Brownell SE. 2014.. Course-based undergraduate research experiences can make scientific research more inclusive. . CBE—Life Sci. Educ. 13:(4):6026
    [Crossref] [Google Scholar]
  11. 11.
    Jordan TC, Burnett SH, Carson S, Caruso SM, Clase K, et al. 2014.. A broadly implementable research course in phage discovery and genomics for first-year undergraduate students. . mBio 5:(1):e01051-13
    [Crossref] [Google Scholar]
  12. 12.
    Hanauer DI, Graham MJ, SEA-PHAGES, Betancur L, Bobrownicki A, et al. 2017.. An inclusive Research Education Community (iREC): impact of the SEA-PHAGES program on research outcomes and student learning. . PNAS 114:(51):1353136 12. Describes the SEA-PHAGES program, with evidence for scientific and educational effect.
    [Crossref] [Google Scholar]
  13. 13.
    Hatfull GF, Pedulla ML, Jacobs-Sera D, Cichon PM, Foley A, et al. 2006.. Exploring the mycobacteriophage metaproteome: phage genomics as an educational platform. . PLOS Genet. 2:(6 ). :e92 13. A description of phage genomics as an educational platform and seven key attributes of undergraduate research experiences.
    [Crossref] [Google Scholar]
  14. 14.
    Hanauer DI, Jacobs-Sera D, Pedulla ML, Cresawn SG, Hendrix RW, Hatfull GF. 2006.. Teaching scientific inquiry. . Science 314:(5807):188081
    [Crossref] [Google Scholar]
  15. 15.
    Hanauer DI, Graham MJ, Jacobs-Sera D, Garlena RA, Russell DA, et al. 2022.. Broadening access to STEM through the community college: investigating the role of course-based research experiences (CREs). . CBE—Life Sci. Educ. 21:(2):ar38
    [Crossref] [Google Scholar]
  16. 16.
    Hanauer DI, Graham MJ, Arnold RJ, Ayuk MA, Balish MF, et al. 2022.. Instructional models for course-based research experience (CRE) teaching. . CBE—Life Sci. Educ. 21:(1):ar8
    [Crossref] [Google Scholar]
  17. 17.
    DeChenne-Peters SE, Scheuermann NL. 2022.. Faculty experiences during the implementation of an introductory biology course-based undergraduate research experience (CURE). . CBE—Life Sci. Educ. 21:(4):ar70
    [Crossref] [Google Scholar]
  18. 18.
    Leonetti CT, Lindberg H, Schwake DO, Cotter RL. 2023.. A call to assess the impacts of course-based undergraduate research experiences for career and technical education, allied health, and underrepresented students at community colleges. . CBE—Life Sci. Educ. 22:(1):ar4
    [Crossref] [Google Scholar]
  19. 19.
    Lopatto D, Hauser C, Jones CJ, Paetkau D, Chandrasekaran V, et al. 2014.. A central support system can facilitate implementation and sustainability of a classroom-based undergraduate research experience (CURE) in genomics. . CBE—Life Sci. Educ. 13:(4):71123
    [Crossref] [Google Scholar]
  20. 20.
    Croonquist P, Falkenberg V, Minkovsky N, Sawa A, Skerritt M, et al. 2023.. The Genomics Education Partnership: first findings on genomics research in community colleges. . Scholarsh. Pr. Undergrad. Res. 6:(3):1728
    [Crossref] [Google Scholar]
  21. 21.
    Hurley A, Chevrette MG, Acharya DD, Lozano GL, Garavito M, et al. 2021.. Tiny Earth: a big idea for STEM education and antibiotic discovery. . mBio 12:(1):e03432-20
    [Crossref] [Google Scholar]
  22. 22.
    Shaffer CD, Alvarez C, Bailey C, Barnard D, Bhalla S, et al. 2010.. The Genomics Education Partnership: successful integration of research into laboratory classes at a diverse group of undergraduate institutions. . CBE—Life Sci. Educ. 9:(1):5569
    [Crossref] [Google Scholar]
  23. 23.
    Hatfull GF. 2015.. Dark matter of the biosphere: the amazing world of bacteriophage diversity. . J. Virol. 89:(16):810710
    [Crossref] [Google Scholar]
  24. 24.
    Hatfull GF, Racaniello V. 2014.. PHIRE and TWiV: experiences in bringing virology to new audiences. . Annu. Rev. Virol. 1::3753
    [Crossref] [Google Scholar]
  25. 25.
    Heller D, Sivanathan V. 2022.. Publishing student-led discoveries in genetics. . G3 12:(8):jkac141
    [Crossref] [Google Scholar]
  26. 26.
    Hendrix RW, Smith MCM, Burns RN, Ford ME, Hatfull GF. 1999.. Evolutionary relationships among diverse bacteriophages and prophages: All the world's a phage. . PNAS 96:(5):219297
    [Crossref] [Google Scholar]
  27. 27.
    Bar-On YM, Phillips R, Milo R. 2018.. The biomass distribution on Earth. . PNAS 115:(25):650611
    [Crossref] [Google Scholar]
  28. 28.
    Mushegian AR. 2020.. Are there 1031 virus particles on Earth, or more, or fewer?. J. Bacteriol. 202:(9):e0005220
    [Crossref] [Google Scholar]
  29. 29.
    Suttle CA. 2007.. Marine viruses—major players in the global ecosystem. . Nat. Rev. Microbiol. 5:(10):80112
    [Crossref] [Google Scholar]
  30. 30.
    Dion MB, Oechslin F, Moineau S. 2020.. Phage diversity, genomics and phylogeny. . Nat. Rev. Microbiol. 18:(3):12538
    [Crossref] [Google Scholar]
  31. 31.
    Ndela EO, Roux S, Henke C, Sczyrba A, Ngando TS, et al. 2022.. Reekeekee- and roodoodooviruses, two different Microviridae clades constituted by the smallest DNA phages. . Virus Evol. 9:(1):veac123
    [Crossref] [Google Scholar]
  32. 32.
    Devoto AE, Santini JM, Olm MR, Anantharaman K, Munk P, et al. 2019.. Megaphages infect Prevotella and variants are widespread in gut microbiomes. . Nat. Microbiol. 4:(4):693700
    [Crossref] [Google Scholar]
  33. 33.
    Al-Shayeb B, Sachdeva R, Chen L-X, Ward F, Munk P, et al. 2020.. Clades of huge phages from across Earth's ecosystems. . Nature 578:(7795):42531
    [Crossref] [Google Scholar]
  34. 34.
    Harding KR, Kyte N, Fineran PC. 2023.. Jumbo phages. . Curr. Biol. 33:(14):R75051
    [Crossref] [Google Scholar]
  35. 35.
    Turner D, Shkoporov AN, Lood C, Millard AD, Dutilh BE, et al. 2023.. Abolishment of morphology-based taxa and change to binomial species names: 2022 taxonomy update of the ICTV Bacterial Viruses Subcommittee. . Arch. Virol. 168:(2):74
    [Crossref] [Google Scholar]
  36. 36.
    Hatfull GF. 2020.. Actinobacteriophages: genomics, dynamics, and applications. . Annu. Rev. Virol. 7::3761
    [Crossref] [Google Scholar]
  37. 37.
    Brum JR, Sullivan MB. 2015.. Rising to the challenge: accelerated pace of discovery transforms marine virology. . Nat. Rev. Microbiol. 13:(3):14759
    [Crossref] [Google Scholar]
  38. 38.
    Mirzaei MK, Maurice CF. 2017.. Ménage à trois in the human gut: interactions between host, bacteria and phages. . Nat. Rev. Microbiol. 15:(7):397408
    [Crossref] [Google Scholar]
  39. 39.
    Pope WH, Mavrich TN, Garlena RA, Guerrero-Bustamante CA, Jacobs-Sera D, et al. 2017.. Bacteriophages of Gordonia spp. display a spectrum of diversity and genetic relationships. . mBio 8:(4):e01069-17
    [Crossref] [Google Scholar]
  40. 40.
    Pope WH, Bowman CA, Russell DA, Jacobs-Sera D, Asai DJ, et al. 2015.. Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity. . eLife 4::e06416
    [Crossref] [Google Scholar]
  41. 41.
    Jacobs-Sera D, Abad LA, Alvey RM, Anders KR, Aull HG, et al. 2020.. Genomic diversity of bacteriophages infecting Microbacterium spp. . PLOS ONE 15:(6):e0234636
    [Crossref] [Google Scholar]
  42. 42.
    Clokie MRJ, Millard AD, Letarov AV, Heaphy S. 2011.. Phages in nature. . Bacteriophage 1:(1):3145
    [Crossref] [Google Scholar]
  43. 43.
    Hampton HG, Watson BNJ, Fineran PC. 2020.. The arms race between bacteria and their phage foes. . Nature 577:(7790):32736
    [Crossref] [Google Scholar]
  44. 44.
    Georjon H, Bernheim A. 2023.. The highly diverse antiphage defence systems of bacteria. . Nat. Rev. Microbiol. 21:(10):686700
    [Crossref] [Google Scholar]
  45. 45.
    Hatfull GF, Dedrick RM, Schooley RT. 2021.. Phage therapy for antibiotic-resistant bacterial infections. . Annu. Rev. Med. 73::197211
    [Crossref] [Google Scholar]
  46. 46.
    Nagel T, Musila L, Muthoni M, Nikolich M, Nakavuma JL, Clokie MR. 2022.. Phage banks as potential tools to rapidly and cost-effectively manage antimicrobial resistance in the developing world. . Curr. Opin. Virol. 53::101208
    [Crossref] [Google Scholar]
  47. 47.
    Mirdita M, Schütze K, Moriwaki Y, Heo L, Ovchinnikov S, Steinegger M. 2022.. ColabFold: making protein folding accessible to all. . Nat. Methods 19:(6):67982
    [Crossref] [Google Scholar]
  48. 48.
    Meng EC, Goddard TD, Pettersen EF, Couch GS, Pearson ZJ, et al. 2023.. UCSF ChimeraX: tools for structure building and analysis. . Protein Sci. 32:(11):e4792
    [Crossref] [Google Scholar]
  49. 49.
    Hanauer DI, Graham MJ, Hatfull GF. 2016.. A measure of college student persistence in the sciences (PITS). . CBE—Life Sci. Educ. 15:(4):ar54
    [Crossref] [Google Scholar]
  50. 50.
    Hanauer DI, Zhang T, Graham MJ, Adams SD, Ahumada-Santos YP, et al. 2023.. Models of classroom assessment for course-based research experiences. . Front. Educ. 8::1279921
    [Crossref] [Google Scholar]
  51. 51.
    Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, et al. 2016.. Taxonomy, physiology, and natural products of Actinobacteria. . Microbiol. Mol. Biol. Rev. 80:(1):143
    [Crossref] [Google Scholar]
  52. 52.
    Russell DA, Hatfull GF. 2016.. PhagesDB: the actinobacteriophage database. . Bioinformatics 33:(5):78486
    [Crossref] [Google Scholar]
  53. 53.
    Cresawn SG, Bogel M, Day N, Jacobs-Sera D, Hendrix RW, Hatfull GF. 2011.. Phamerator: a bioinformatic tool for comparative bacteriophage genomics. . BMC Bioinform. 12:(1):395
    [Crossref] [Google Scholar]
  54. 54.
    Pollenz RS, Barnhill K, Biggs A, Bland J, Carter V, et al. 2023.. A genome-wide cytotoxicity screen of Cluster F1 mycobacteriophage Girr reveals novel inhibitors of Mycobacterium smegmatis growth. . bioRxiv 2023.08.04.552056. https://doi.org/10.1101/2023.08.04.552056
  55. 55.
    Amaya I, Edwards K, Wise BM, Bhattacharyya A, Pablo CHD, et al. 2023.. A genome-wide overexpression screen reveals Mycobacterium smegmatis growth inhibitors encoded by mycobacteriophage Hammy. . G3 12::jkad240
    [Crossref] [Google Scholar]
  56. 56.
    Heller D, Amaya I, Mohamed A, Ali I, Mavrodi D, et al. 2022.. Systematic overexpression of genes encoded by mycobacteriophage Waterfoul reveals novel inhibitors of mycobacterial growth. . G3 12:(8):jkac140 56. Describes the characterization of phage genes in the SEA-GENES program.
    [Crossref] [Google Scholar]
  57. 57.
    Hanauer DI, Hatfull G. 2015.. Measuring networking as an outcome variable in undergraduate research experiences. . CBE—Life Sci. Educ. 14:(4):ar38
    [Crossref] [Google Scholar]
  58. 58.
    Dulberger CL, Rubin EJ, Boutte CC. 2020.. The mycobacterial cell envelope—a moving target. . Nat. Rev. Microbiol. 18:(1):4759
    [Crossref] [Google Scholar]
  59. 59.
    Podgorski J, Calabrese J, Alexandrescu L, Jacobs-Sera D, Pope W, et al. 2020.. Structures of three actinobacteriophage capsids: roles of symmetry and accessory proteins. . Viruses 12:(3):294
    [Crossref] [Google Scholar]
  60. 60.
    Podgorski JM, Freeman K, Gosselin S, Huet A, Conway JF, et al. 2023.. A structural dendrogram of the actinobacteriophage major capsid proteins provides important structural insights into the evolution of capsid stability. . Structure 31:(3):28294.e5
    [Crossref] [Google Scholar]
  61. 61.
    Freeman KG, Robotham AC, Parks OB, Abad L, Jacobs-Sera D, et al. 2023.. Virion glycosylation influences mycobacteriophage immune recognition. . Cell Host Microbe 31:(7):121631.e6
    [Crossref] [Google Scholar]
  62. 62.
    Dulberger CL, Guerrero-Bustamante CA, Owen SV, Wilson S, Wuo MG, et al. 2023.. Mycobacterial nucleoid-associated protein Lsr2 is required for productive mycobacteriophage infection. . Nat. Microbiol. 8:(4):695710
    [Crossref] [Google Scholar]
  63. 63.
    Gordon BRG, Li Y, Wang L, Sintsova A, van Bakel H, et al. 2010.. Lsr2 is a nucleoid-associated protein that targets AT-rich sequences and virulence genes in Mycobacterium tuberculosis. . PNAS 107:(11):515459
    [Crossref] [Google Scholar]
  64. 64.
    Dedrick RM, Smith BE, Garlena RA, Russell DA, Aull HG, et al. 2021.. Mycobacterium abscessus strain morphotype determines phage susceptibility, the repertoire of therapeutically useful phages, and phage resistance. . mBio 12:(2):e03431-20
    [Google Scholar]
  65. 65.
    Wetzel KS, Illouz M, Abad L, Aull HG, Russell DA, et al. 2023.. Therapeutically useful mycobacteriophages BPs and Muddy require trehalose polyphleates. . Nat. Microbiol. 8:(9):171731
    [Crossref] [Google Scholar]
  66. 66.
    Gauthier CH, Cresawn SG, Hatfull GF. 2022.. PhaMMseqs: a new pipeline for constructing phage gene phamilies using MMseqs2. . G3 12:(11):jkac233
    [Crossref] [Google Scholar]
  67. 67.
    Pedulla ML, Ford ME, Houtz JM, Karthikeyan T, Wadsworth C, et al. 2003.. Origins of highly mosaic mycobacteriophage genomes. . Cell 113:(2):17182
    [Crossref] [Google Scholar]
  68. 68.
    Hatfull GF, Hendrix RW. 2011.. Bacteriophages and their genomes. . Curr. Opin. Virol. 1:(4):298303
    [Crossref] [Google Scholar]
  69. 69.
    Mavrich TN, Hatfull GF. 2017.. Bacteriophage evolution differs by host, lifestyle and genome. . Nat. Microbiol. 2:(9):17112
    [Crossref] [Google Scholar]
  70. 70.
    Gauthier CH, Hatfull GF. 2023.. PhamClust: a phage genome clustering tool using proteomic equivalence. . mSystems 8:(5):e00443-23
    [Crossref] [Google Scholar]
  71. 71.
    Payne KM, Hatfull GF. 2012.. Mycobacteriophage endolysins: diverse and modular enzymes with multiple catalytic activities. . PLOS ONE 7:(3):e34052
    [Crossref] [Google Scholar]
  72. 72.
    Pollenz RS, Bland J, Pope WH. 2022.. Bioinformatic characterization of endolysins and holin-like membrane proteins in the lysis cassette of phages that infect Gordonia rubripertincta. . PLOS ONE 17:(11):e0276603
    [Crossref] [Google Scholar]
  73. 73.
    Broussard GW, Oldfield LM, Villanueva VM, Lunt BL, Shine EE, Hatfull GF. 2013.. Integration-dependent bacteriophage immunity provides insights into the evolution of genetic switches. . Mol. Cell 49:(2):23748
    [Crossref] [Google Scholar]
  74. 74.
    Wetzel KS, Aull HG, Zack KM, Garlena RA, Hatfull GF. 2020.. Protein-mediated and RNA-based origins of replication of extrachromosomal mycobacterial prophages. . mBio 11:(2):e00385-20
    [Crossref] [Google Scholar]
  75. 75.
    Wetzel KS, Guerrero-Bustamante CA, Dedrick RM, Ko C-C, Freeman KG, et al. 2021.. CRISPY-BRED and CRISPY-BRIP: efficient bacteriophage engineering. . Sci. Rep. 11:(1):6796
    [Crossref] [Google Scholar]
  76. 76.
    Marinelli LJ, Piuri M, Swigoňová Z, Balachandran A, Oldfield LM, et al. 2008.. BRED: a simple and powerful tool for constructing mutant and recombinant bacteriophage genomes. . PLOS ONE 3:(12):e3957
    [Crossref] [Google Scholar]
  77. 77.
    Dedrick RM, Marinelli LJ, Newton GL, Pogliano K, Pogliano J, Hatfull GF. 2013.. Functional requirements for bacteriophage growth: gene essentiality and expression in mycobacteriophage Giles. . Mol. Microbiol. 88:(3):57789
    [Crossref] [Google Scholar]
  78. 78.
    Dedrick RM, Mavrich TN, Ng WL, Hatfull GF. 2017.. Expression and evolutionary patterns of mycobacteriophage D29 and its temperate close relatives. . BMC Microbiol. 17:(1):225
    [Crossref] [Google Scholar]
  79. 79.
    Dedrick RM, Bustamante CAG, Garlena RA, Pinches RS, Cornely K, Hatfull GF. 2019.. Mycobacteriophage ZoeJ: a broad host-range close relative of mycobacteriophage TM4. . Tuberculosis 115::1423
    [Crossref] [Google Scholar]
  80. 80.
    Dedrick RM, Jacobs-Sera D, Bustamante CAG, Garlena RA, Mavrich TN, et al. 2017.. Prophage-mediated defence against viral attack and viral counter-defence. . Nat. Microbiol. 2:(3):16251
    [Crossref] [Google Scholar]
  81. 81.
    Gentile GM, Wetzel KS, Dedrick RM, Montgomery MT, Garlena RA, et al. 2019.. More evidence of collusion: a new prophage-mediated viral defense system encoded by mycobacteriophage Sbash. . mBio 10:(2):e00196-19
    [Crossref] [Google Scholar]
  82. 82.
    Montgomery MT, Bustamante CAG, Dedrick RM, Jacobs-Sera D, Hatfull GF. 2019.. Yet more evidence of collusion: a new viral defense system encoded by Gordonia phage CarolAnn. . mBio 10:(2):e02417-18
    [Crossref] [Google Scholar]
  83. 83.
    Dedrick RM, Aull HG, Jacobs-Sera D, Garlena RA, Russell DA, et al. 2021.. The prophage and plasmid mobilome as a likely driver of Mycobacterium abscessus diversity. . mBio 12:(2):e03441-20
    [Google Scholar]
  84. 84.
    Ko C-C, Hatfull GF. 2020.. Identification of mycobacteriophage toxic genes reveals new features of mycobacterial physiology and morphology. . Sci. Rep. 10:(1):14670
    [Crossref] [Google Scholar]
  85. 85.
    Binsabaan SA, Freeman KG, Hatfull GF, VanDemark AP. 2023.. The cytotoxic mycobacteriophage protein Phaedrus gp82 interacts with and modulates the activity of the host ATPase, MoxR. . J. Mol. Biol. 435:(20):168261
    [Crossref] [Google Scholar]
  86. 86.
    Dedrick RM, Guerrero-Bustamante CA, Garlena RA, Russell DA, Ford K, et al. 2019.. Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus. . Nat. Med. 25:(5):73033 86. Reports the first therapeutic use of bacteriophages for a mycobacterial infection.
    [Crossref] [Google Scholar]
  87. 87.
    Petrova ZO, Broussard GW, Hatfull GF. 2015.. Mycobacteriophage-repressor-mediated immunity as a selectable genetic marker: Adephagia and BPs repressor selection. . Microbiology 161:(8):153951
    [Crossref] [Google Scholar]
  88. 88.
    Donnelly-Wu MK, Jacobs WR, Hatfull GF. 1993.. Superinfection immunity of mycobacteriophage L5: applications for genetic transformation of mycobacteria. . Mol. Microbiol. 7:(3):40717
    [Crossref] [Google Scholar]
  89. 89.
    McGinnis RJ, Brambley CA, Stamey B, Green WC, Gragg KN, et al. 2022.. A monomeric mycobacteriophage immunity repressor utilizes two domains to recognize an asymmetric DNA sequence. . Nat. Commun. 13:(1):4105
    [Crossref] [Google Scholar]
  90. 90.
    Little JS, Dedrick RM, Freeman KG, Cristinziano M, Smith BE, et al. 2022.. Bacteriophage treatment of disseminated cutaneous Mycobacterium chelonae infection. . Nat. Commun. 13:(1):2313
    [Crossref] [Google Scholar]
  91. 91.
    Nick JA, Dedrick RM, Gray AL, Vladar EK, Smith BE, et al. 2022.. Host and pathogen response to bacteriophage engineered against Mycobacterium abscessus lung infection. . Cell 185::186074
    [Crossref] [Google Scholar]
  92. 92.
    Dedrick RM, Smith BE, Cristinziano M, Freeman KG, Jacobs-Sera D, et al. 2022.. Phage therapy of Mycobacterium infections: compassionate-use of phages in twenty patients with drug-resistant mycobacterial disease. . Clin. Infect. Dis. 76:(1):10312
    [Crossref] [Google Scholar]
  93. 93.
    Gauthier CH, Abad L, Venbakkam AK, Malnak J, Russell DA, Hatfull GF. 2022.. DEPhT: a novel approach for efficient prophage discovery and precise extraction. . Nucleic Acids Res. 50:(13):e75
    [Crossref] [Google Scholar]
  94. 94.
    Abad L, Gauthier CH, Florian I, Jacobs-Sera D, Hatfull GF. 2023.. The heterogenous and diverse population of prophages in Mycobacterium genomes. . mSystems 8::e0044623
    [Crossref] [Google Scholar]
  95. 95.
    Huson DH. 1998.. SplitsTree: analyzing and visualizing evolutionary data. . Bioinformatics 14:(1):6873
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-virology-113023-110757
Loading
/content/journals/10.1146/annurev-virology-113023-110757
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error