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Volume 167, Issue 9

Wildy Prize Lecture, 2020–2021: Who wouldn’t want to discover a new virus? Open Access

Abstract

Innovations in science education are desperately needed to find ways to engage and interest students early in their undergraduate careers. Exposing students to authentic research experiences is highly beneficial, but finding ways to include all types of students and to do this at large scale is especially challenging. An attractive solution is the concept of an inclusive research education community (iREC) in which centralized research leadership and administration supports multiple institutions, including diverse groups of schools and universities, faculty and students. The Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Sciences (SEA-PHAGES) programme is an excellent example of an iREC, in which students explore viral diversity and evolution through discovery and genomic analysis of novel bacteriophages. The SEA-PHAGES programme has proven to be sustainable, to be implemented at large scale, and to enhance student persistence in science, as well as to produce substantial research advances. Discovering a new virus with the potential for new biological insights and clinical applications is inherently exciting. Who wouldn’t want to discover a new virus?

  • Received:
  • Accepted:
  • Published Online:
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. The Microbiology Society waived the open access fees for this article.
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2021-09-01
2024-05-06
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References

  1. Brewer C, Smith D. eds Vision and Change in Undergraduate Biology Education: A Call to Action Washington, DC: American Association for the Advancement of Science; 2011
     [Google Scholar]
  2. Asai DJ. Race matters. Cell 2020; 181:754–757 [View Article] [PubMed]
     [Google Scholar]
  3. Technology PsCoSa Report To The President. Engage To Excel: Producing One Million Additional College Graduates With Degrees In Science, Technology, Engineering, And Mathematics Washington, DC: U.S. Government Office of Science and Technology; 2012
     [Google Scholar]
  4. Gentile J, Brenner K, Stephens A. Undergraduate Research Experiences for STEM Students: Successes, Challenges, and Opportunities Washington, DC: The National Academies; 2017
     [Google Scholar]
  5. Wei CA, Woodin T. Undergraduate research experiences in biology: alternatives to the apprenticeship model. CBE Life Sci Educ 2011; 10:123–131 [View Article] [PubMed]
     [Google Scholar]
  6. Hanauer DI, Graham MJ. SEA-PHAGES Betancur L, Bobrownicki A et al. An inclusive research education community (IREC): Impact of the SEA-PHAGES program on research outcomes and student learning. Proc Natl Acad Sci U S A 2017; 114:13531–13536 [View Article] [PubMed]
     [Google Scholar]
  7. Elgin SCR, Hauser C, Holzen TM, Jones C, Kleinschmit A et al. The GEP: Crowd-sourcing big data analysis with undergraduates. Trends Genet 2017; 33:81–85 [View Article] [PubMed]
     [Google Scholar]
  8. Jordan TC, Burnett SH, Carson S, Caruso SM, Clase K et al. A broadly implementable research course in phage discovery and genomics for first-year undergraduate students. mBio 2014; 5:e01051-01013 [View Article] [PubMed]
     [Google Scholar]
  9. Hatfull GF. Innovations in undergraduate science education: going viral. J Virol 2015; 89:8111–8113 [View Article] [PubMed]
     [Google Scholar]
  10. Hatfull GF. Bacteriophage research: gateway to learning science. Microbe 2010243–250
     [Google Scholar]
  11. Hatfull GF, Pedulla ML, Jacobs-Sera D, Cichon PM, Foley A et al. Exploring the mycobacteriophage metaproteome: Phage Genomics as an educational platform. PLoS Genet 2006; 2:e92 [View Article] [PubMed]
     [Google Scholar]
  12. Hendrix RW. The long evolutionary reach of viruses. Curr Biol 1999; 9:914–917
     [Google Scholar]
  13. Hendrix RW. Bacteriophages: evolution of the majority. Theor Popul Biol 2002; 61:471–480 [View Article] [PubMed]
     [Google Scholar]
  14. Hendrix RW. Bacteriophage genomics. Curr Opin Microbiol 2003; 6:506–511 [View Article] [PubMed]
     [Google Scholar]
  15. Hatfull GF, Hendrix RW. Bacteriophages and their genomes. Curr Opin Virol 2011; 1:298–303
     [Google Scholar]
  16. Salmond GPC, Fineran PC. A century of the phage: past, present and future. Nat Rev Microbiol 2015; 13:777–786 [View Article] [PubMed]
     [Google Scholar]
  17. Hanauer DI, Dolan EL. The project ownership survey: measuring differences in scientific inquiry experiences. CBE Life Sci Educ 2014; 13:149–158 [View Article] [PubMed]
     [Google Scholar]
  18. Hanauer DI, Frederick J, Fotinakes B, Strobel SA. Linguistic analysis of project ownership for undergraduate research experiences. CBE Life Sci Educ 2012; 11:378–385 [View Article] [PubMed]
     [Google Scholar]
  19. Hanauer DI, Graham MJ, Hatfull GF. n.d A measure of college student persistence in the sciences (pits). CBE Life Sci Educ 15: [View Article] [PubMed]
     [Google Scholar]
  20. Hatfull GF. Actinobacteriophages: genomics, dynamics, and applications. Annu Rev Virol 2020; 7:37–61 [View Article] [PubMed]
     [Google Scholar]
  21. Russell DA, Hatfull GF. PhagesDB: the actinobacteriophage database. Bioinformatics 2017; 33:784–786 [View Article] [PubMed]
     [Google Scholar]
  22. Hatfull GF, Sarkis GJ. DNA sequence, structure and gene expression of mycobacteriophage L5: a phage system for mycobacterial genetics. Mol Microbiol 1993; 7:395–405 [View Article] [PubMed]
     [Google Scholar]
  23. Cresawn SG, Bogel M, Day N, Jacobs-Sera D, Hendrix RW et al. Phamerator: A bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics 2011; 12:395 [View Article] [PubMed]
     [Google Scholar]
  24. Mavrich TN, Gauthier C, Abad L, Bowman CA, Cresawn SG et al. Pdm_utils: A SEA-PHAGES MYSQL Phage database management Toolkit. Bioinformatics 2020 [View Article] [PubMed]
     [Google Scholar]
  25. Hatfull GF, Jacobs-Sera D, Lawrence JG, Pope WH, Russell DA et al. Comparative genomic analysis of 60 mycobacteriophage genomes: Genome clustering, gene acquisition, and gene size. J Mol Biol 2010; 397:119–143 [View Article] [PubMed]
     [Google Scholar]
  26. Pope WH, Mavrich TN, Garlena RA, Guerrero-Bustamante CA, Jacobs-Sera D et al. Bacteriophages of Gordonia spp. display a spectrum of diversity and genetic relationships. mBio 2017; 8: [View Article]
     [Google Scholar]
  27. Pedulla ML, Ford ME, Houtz JM, Karthikeyan T, Wadsworth C et al. Origins of highly mosaic mycobacteriophage genomes. Cell 2003; 113:171–182 [View Article] [PubMed]
     [Google Scholar]
  28. Hatfull GF. Mycobacteriophages: genes and genomes. Annu Rev Microbiol 2010; 64:331–356 [View Article] [PubMed]
     [Google Scholar]
  29. Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF. Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc Natl Acad Sci U S A 1999; 96:2192–2197 [View Article] [PubMed]
     [Google Scholar]
  30. Hampton HG, Watson BNJ, Fineran PC. The arms race between bacteria and their phage foes. Nature 2020; 577:327–336 [View Article] [PubMed]
     [Google Scholar]
  31. Dedrick RM, Jacobs-Sera D, Bustamante CAG, Garlena RA, Mavrich TN et al. Prophage-mediated defence against viral attack and viral counter-defence. Nat Microbiol 2017; 2:16251 [View Article] [PubMed]
     [Google Scholar]
  32. Gentile GM, Wetzel KS, Dedrick RM, Montgomery MT, Garlena RA et al. More evidence of collusion: A new prophage-mediated viral defense system encoded by mycobacteriophage Sbash. mBio 2019; 10: [View Article] [PubMed]
     [Google Scholar]
  33. Montgomery MT, Guerrero Bustamante CA, Dedrick RM, Jacobs-Sera D, Hatfull GF. Yet more evidence of collusion: a new viral defense system encoded by gordonia phage CarolAnn. mBio 2019; 10: [View Article]
     [Google Scholar]
  34. Bondy-Denomy J, Pawluk A, Maxwell KL, Davidson AR. Bacteriophage genes that inactivate the CRISPR/Cas bacterial immune system. Nature 2013; 493:429–432 [View Article] [PubMed]
     [Google Scholar]
  35. Gao Y, Cao D, Zhu J, Feng H, Luo X et al. Structural insights into assembly, operation and inhibition of a type I restriction-modification system. Nat Microbiol 2020; 5:1107–1118 [View Article] [PubMed]
     [Google Scholar]
  36. CC K, Hatfull GF. Mycobacteriophage Fruitloop gp52 inactivates Wag31 (DivIVA) to prevent heterotypic superinfection. Mol Microbiol 2018
     [Google Scholar]
  37. Ko C-C, Hatfull GF. Identification of mycobacteriophage toxic genes reveals new features of mycobacterial physiology and morphology. Sci Rep 2020; 10:14670 [View Article] [PubMed]
     [Google Scholar]
  38. Rybniker J, Krumbach K, van Gumpel E, Plum G, Eggeling L et al. The cytotoxic early protein 77 of mycobacteriophage L5 interacts with MSMEG_3532, an L-serine dehydratase of Mycobacterium smegmatis. J Basic Microbiol 2011; 51:515–522 [View Article] [PubMed]
     [Google Scholar]
  39. Rybniker J, Plum G, Robinson N, Small PL, Hartmann P. Identification of three cytotoxic early proteins of mycobacteriophage L5 leading to growth inhibition in Mycobacterium smegmatis. Microbiology (Reading) 2008; 154:2304–2314 [View Article] [PubMed]
     [Google Scholar]
  40. Lee MH, Pascopella L, Jacobs WR, Hatfull GF. Site-specific integration of mycobacteriophage L5: integration-proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and bacille Calmette-Guérin. Proc Natl Acad Sci U S A 1991; 88:3111–3115 [View Article] [PubMed]
     [Google Scholar]
  41. Pham TT, Jacobs-Sera D, Pedulla ML, Hendrix RW, Hatfull GF. Comparative genomic analysis of mycobacteriophage Tweety: evolutionary insights and construction of compatible site-specific integration vectors for mycobacteria. Microbiology (Reading) 2007; 153:2711–2723 [View Article] [PubMed]
     [Google Scholar]
  42. Morris P, Marinelli LJ, Jacobs-Sera D, Hendrix RW, Hatfull GF. Genomic characterization of mycobacteriophage Giles: evidence for phage acquisition of host DNA by illegitimate recombination. J Bacteriol 2008; 190:2172–2182 [View Article] [PubMed]
     [Google Scholar]
  43. Bibb LA, Hancox MI, Hatfull GF. Integration and excision by the large serine recombinase phiRv1 integrase. Mol Microbiol 2005; 55:1896–1910 [View Article] [PubMed]
     [Google Scholar]
  44. Donnelly-Wu MK, Jacobs WR, Hatfull GF. Superinfection immunity of mycobacteriophage L5: applications for genetic transformation of mycobacteria. Mol Microbiol 1993; 7:407–417 [View Article] [PubMed]
     [Google Scholar]
  45. Petrova ZO, Broussard GW, Hatfull GF. Mycobacteriophage-repressor-mediated immunity as a selectable genetic marker: Adephagia and BPs repressor selection. Microbiology (Reading) 2015; 161:1539–1551 [View Article] [PubMed]
     [Google Scholar]
  46. Wetzel KS, Aull HG, Zack KM, Garlena RA, Hatfull GF. Protein-Mediated and RNA-based origins of replication of extrachromosomal mycobacterial prophages. mBio 2020; 11: [View Article] [PubMed]
     [Google Scholar]
  47. van Kessel JC, Hatfull GF. Recombineering in Mycobacterium tuberculosis. Nat Methods 2007; 4:147–152 [View Article] [PubMed]
     [Google Scholar]
  48. van Kessel JC, Hatfull GF. Efficient point mutagenesis in mycobacteria using single-stranded DNA recombineering: characterization of antimycobacterial drug targets. Mol Microbiol 2008; 67:1094–1107 [View Article] [PubMed]
     [Google Scholar]
  49. van Kessel JC, Hatfull GF. Mycobacterial recombineering. Methods Mol Biol 2008; 435:203–215 [View Article] [PubMed]
     [Google Scholar]
  50. van Kessel JC, Marinelli LJ, Hatfull GF. Recombineering mycobacteria and their phages. Nat Rev Microbiol 2008; 6:851–857 [View Article] [PubMed]
     [Google Scholar]
  51. Bardarov S, Bardarov S, Pavelka MS, Sambandamurthy V, Larsen M et al. Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology (Reading) 2002; 148:3007–3017 [View Article] [PubMed]
     [Google Scholar]
  52. Bardarov S Jr, Dou H, Eisenach K, Banaiee N, Ya S u et al. Detection and drug-susceptibility testing of M. tuberculosis from sputum samples using luciferase reporter phage: comparison with the Mycobacteria Growth Indicator Tube (MGIT) system. Diagn Microbiol Infect Dis 2003; 45:53–61 [View Article] [PubMed]
     [Google Scholar]
  53. Bardarov S, Kriakov J, Carriere C, Yu S, Vaamonde C et al. Conditionally replicating mycobacteriophages: a system for transposon delivery to Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 1997; 94:10961–10966 [View Article] [PubMed]
     [Google Scholar]
  54. Jacobs WR Jr, Barletta RG, Udani R, Chan J, Kalkut G et al. Rapid assessment of drug susceptibilities of Mycobacterium tuberculosis by means of luciferase reporter phages. Science 1993; 260:819–822 [View Article] [PubMed]
     [Google Scholar]
  55. Marinelli LJ, Hatfull GF, Piuri M. Recombineering: A powerful tool for modification of bacteriophage genomes. Bacteriophage 2012; 2:5–14 [View Article] [PubMed]
     [Google Scholar]
  56. Marinelli LJ, Piuri M, Hatfull GF. Genetic manipulation of lytic bacteriophages with BRED: bacteriophage recombineering of electroporated DNA. Methods Mol Biol 2019; 1898:69–80 [View Article] [PubMed]
     [Google Scholar]
  57. Marinelli LJ, Piuri M, Swigonová Z, Balachandran A, Oldfield LM et al. BRED: a simple and powerful tool for constructing mutant and recombinant bacteriophage genomes. PLoS One 2008; 3:e3957 [View Article]
     [Google Scholar]
  58. Wetzel KS, Guerrero-Bustamante CA, Dedrick RM, Ko C-C, Freeman KG et al. Crispy-bred and CRISPY-BRIP: Efficient bacteriophage engineering. Sci Rep 2021; 11:6796 [View Article] [PubMed]
     [Google Scholar]
  59. Dedrick RM, Guerrero-Bustamante CA, Garlena RA, Russell DA, Ford K et al. Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus. Nat Med 2019; 25:730–733 [View Article] [PubMed]
     [Google Scholar]
  60. Jacobs-Sera D, Marinelli LJ, Bowman C, Broussard GW, Guerrero Bustamante C et al. On the nature of mycobacteriophage diversity and host preference. Virology 2012; 434:187–201 [View Article] [PubMed]
     [Google Scholar]
  61. Dedrick RM, Aull HG, Jacobs-Sera D, Garlena RA, Russell DA et al. The prophage and plasmid mobilome as a likely driver of Mycobacterium abscessus diversity. mBio 2021; 12:
     [Google Scholar]
  62. Dedrick RM, Smith BE, Garlena RA, Russell DA, Aull HG et al. Mycobacterium abscessus strain morphotype determines phage susceptibility, the repertoire of therapeutically useful phages, and phage resistance. mBio 2021; 12: [View Article]
     [Google Scholar]
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Wildy Prize Lecture, 2020–2021: Who wouldn’t want to discover a new virus?
Microbiology 167, 001094 (2021); https://doi.org/10.1099/mic.0.001094
/content/journal/micro/10.1099/mic.0.001094
/content/journal/micro/10.1099/mic.0.001094
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