Bacteriophages of Gordonia spp. Display a spectrum of diversity and genetic relationships

mBio

Volumn 8, Issue 4, 2017, Pages

  Pope, Welkin H ^a   Mavrich, Travis N ^a   Garlena, Rebecca A ^a   Guerrero Bustamante, Carlos A ^a   Jacobs Sera, Deborah ^a   Montgomery, Matthew T ^a   Russell, Daniel A ^a   Warner, Marcie H ^a   Hatfull, Graham F ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Bacteriophage genetics; Bacteriophages; Gordonia

Indexed keywords

ACTINOBACTERIA; ARTICLE; BACTERIAL GENOME; BACTERIOPHAGE; CONTROLLED STUDY; GENETIC SIMILARITY; GENETIC VARIABILITY; GENOME ANALYSIS; GORDONIA; GORDONIA ALKANIVORANS; GORDONIA MALAQUAE; GORDONIA NEOFELIFAECIS; GORDONIA RUBROPERTINCTA; GORDONIA SPUTI; GORDONIA TERRAE; LONG TERMINAL REPEAT; MICROBIAL DIVERSITY; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SEQUENCE ANALYSIS; SIPHOVIRIDAE; VIRION; CLASSIFICATION; DNA BASE COMPOSITION; DNA SEQUENCE; GENETIC VARIATION; GENETICS; GENOMICS; ISOLATION AND PURIFICATION; MYCOBACTERIOPHAGE; VIROLOGY; VIRUS GENOME;

VIRUS DNA;

BACTERIOPHAGES; BASE COMPOSITION; DNA, VIRAL; GENETIC VARIATION; GENOME, VIRAL; GENOMICS; GORDONIA BACTERIUM; MYCOBACTERIOPHAGES; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 85029158292     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01069-17     Document Type: Article

References (61)

1. Hatfull GF, Hendrix RW. 2011. Bacteriophages and their genomes. Curr Opin Virol 1:298–303. https://doi.org/10.1016/j.coviro.2011.06.009.
2. Pedulla ML, Ford ME, Houtz JM, Karthikeyan T, Wadsworth C, Lewis JA, Jacobs-Sera D, Falbo J, Gross J, Pannunzio NR, Brucker W, Kumar V, Kandasamy J, Keenan L, Bardarov S, Kriakov J, Lawrence JG, Jacobs WR, Jr, Hendrix RW, Hatfull GF. 2003. Origins of highly mosaic mycobacteriophage genomes. Cell 113:171–182. https://doi.org/10.1016/S0092-8674(03)00233-2.
3. Hendrix RW, Smith MC, Burns RN, Ford ME, Hatfull GF. 1999. Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc Natl Acad Sci U S A 96:2192–2197. https://doi.org/10.1073/pnas.96.5.2192.
4. Pope WH, Bowman CA, Russell DA, Jacobs-Sera D, Asai DJ, Cresawn SG, Jacobs WR, Hendrix RW, Lawrence JG, Hatfull GF, Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Science, Phage Hunters Integrating Research and Education, Mycobacterial Genetics Course. 2015. Whole genome comparison of a large collection of mycobacteriophages reveals a continuum of phage genetic diversity. eLife 4:e06416. https://doi.org/10.7554/eLife.06416.
5. Grose JH, Casjens SR. 2014. Understanding the enormous diversity of bacteriophages: the tailed phages that infect the bacterial family Enterobacteriaceae. Virology 468–470:421–443. https://doi.org/10.1016/j.virol.2014.08.024.
6. Kwan T, Liu J, DuBow M, Gros P, Pelletier J. 2005. The complete genomes and proteomes of 27 Staphylococcus aureus bacteriophages. Proc Natl Acad Sci U S A 102:5174–5179. https://doi.org/10.1073/pnas.0501140102.
7. Kwan T, Liu J, Dubow M, Gros P, Pelletier J. 2006. Comparative genomic analysis of 18 Pseudomonas aeruginosa bacteriophages. J Bacteriol 188: 1184–1187. https://doi.org/10.1128/JB.188.3.1184-1187.2006.
8. Gregory AC, Solonenko SA, Ignacio-Espinoza JC, LaButti K, Copeland A, Sudek S, Maitland A, Chittick L, Dos Santos F, Weitz JS, Worden AZ, Woyke T, Sullivan MB. 2016. Genomic differentiation among wild cyanophages despite widespread horizontal gene transfer. BMC Genomics 17:930. https://doi.org/10.1186/s12864-016-3286-x.
9. Hatfull GF, Jacobs-Sera D, Lawrence JG, Pope WH, Russell DA, Ko CC, Weber RJ, Patel MC, Germane KL, Edgar RH, Hoyte NN, Bowman CA, Tantoco AT, Paladin EC, Myers MS, Smith AL, Grace MS, Pham TT, O’Brien MB, Vogelsberger AM, Hryckowian AJ, Wynalek JL, Donis-Keller H, Bogel MW, Peebles CL, Cresawn SG, Hendrix RW. 2010. Comparative genomic analysis of 60 mycobacteriophage genomes: genome clustering, gene acquisition, and gene size. J Mol Biol 397:119–143. https://doi.org/10.1016/j.jmb.2010.01.011.
10. Deng L, Ignacio-Espinoza JC, Gregory AC, Poulos BT, Weitz JS, Hugenholtz P, Sullivan MB. 2014. Viral tagging reveals discrete populations in Synechococcus viral genome sequence space. Nature 513:242–245. https://doi.org/10.1038/nature13459.
11. Jacobs-Sera D, Marinelli LJ, Bowman C, Broussard GW, Guerrero Bustamante C, Boyle MM, Petrova ZO, Dedrick RM, Pope WH, Science Education Alliance Phage Hunters Advancing Genomics and Evolutionary Science Sea-Phages Program, Modlin RL, Hendrix RW, Hatfull GF. 2012. On the nature of mycobacteriophage diversity and host preference. Virology 434:187–201. https://doi.org/10.1016/j.virol.2012.09.026.
12. Pope WH, Jacobs-Sera D, Russell DA, Rubin DH, Kajee A, Msibi ZN, Larsen MH, Jacobs WR, Jr, Lawrence JG, Hendrix RW, Hatfull GF. 2014. Genomics and proteomics of mycobacteriophage patience, an accidental tourist in the Mycobacterium neighborhood. mBio 5:e02145. https://doi.org/10.1128/mBio.02145-14.
13. Dyson ZA, Tucci J, Seviour RJ, Petrovski S. 2015. Lysis to kill: evaluation of the lytic abilities, and genomics of nine bacteriophages infective for Gordonia spp. and their potential use in activated sludge foam biocontrol. PLoS One 10:e0134512. https://doi.org/10.1371/journal.pone.0134512.
14. Liu M, Gill JJ, Young R, Summer EJ. 2015. Bacteriophages of wastewater foaming-associated filamentous Gordonia reduce host levels in raw activated sludge. Sci Rep 5:13754. https://doi.org/10.1038/srep13754.
15. Montgomery MT, Pope WH, Arnold ZM, Basina A, Iyer AM, Stoner TH, Kasturiarachi NS, Pressimone CA, Schiebel JG, Furbee EC, Grubb SR, Warner MH, Garlena RA, Russell DA, Jacobs-Sera D, Hatfull GF. 2016. Genome sequences of Gordonia phages Bowser and Schwabeltier. Genome Announc 4:e00596-16. https://doi.org/10.1128/genomeA.00596-16.
16. Petrovski S, Seviour RJ, Tillett D. 2011. Characterization of the genome of the polyvalent lytic bacteriophage GTE2, which has potential for biocontrol of Gordonia-, Rhodococcus-, and Nocardia-stabilized foams in activated sludge plants. Appl Environ Microbiol 77:3923–3929. https://doi.org/10.1128/AEM.00025-11.
17. Petrovski S, Tillett D, Seviour RJ. 2012. Genome sequences and characterization of the related Gordonia phages GTE5 and GRU1 and their use as potential biocontrol agents. Appl Environ Microbiol 78:42–47. https://doi.org/10.1128/AEM.05584-11.
18. Pope WH, Akbar AF, Ayers TN, Belohoubek SG, Chung CF, Hartman AC, Kayiti T, Kessler CM, Koman PI, Kotovskiy GA, Morgan TM, Rohac RM, Silva GM, Willis CE, III, Milliken KA, Shedlock KA, Stanton AC, Toner CL, Furbee EC, Grubb SR, Warner MH, Montgomery MT, Garlena RA, Russell DA, Jacobs-Sera D, Hatfull GF. 2016. Genome sequences of Gordonia bacteriophages Obliviate, UmaThurman, and Guacamole. Genome Announc 4:e00595-16. https://doi.org/10.1128/genomeA.00595-16.
19. Pope WH, Anderson KC, Arora C, Bortz ME, Burnet G, Conover DH, D’Incau GM, Ghobrial JA, Jonas AL, Migdal EJ, Rote NL, German BA, McDonnell JE, Mezghani N, Schafer CE, Thompson PK, Ulbrich MC, Yu VJ, Furbee EC, Grubb SR, Warner MH, Montgomery MT, Garlena RA, Russell DA, Jacobs-Sera D, Hatfull GF. 2016. Genome sequences of Gordonia terrae bacteriophages Phinally and Vivi2. Genome Announc 4:e00599-16. https://doi.org/10.1128/genomeA.00599-16.
20. Pope WH, Bandla S, Colbert AK, Eichinger FG, Gamburg MB, Horiates SG, Jamison JM, Julian DR, Moore WA, Murthy P, Powell MC, Smith SV, Mezghani N, Milliken KA, Thompson PK, Toner CL, Ulbrich MC, Furbee EC, Grubb SR, Warner MH, Montgomery MT, Garlena RA, Russell DA, Jacobs-Sera D, Hatfull GF. 2016. Genome sequences of Gordonia phages BaxterFox, Kita, Nymphadora, and Yeezy. Genome Announc 4:e00600-16. https://doi.org/10.1128/genomeA.00600-16.
21. Pope WH, Bandyopadhyay A, Carlton ML, Kane MT, Panchal NJ, Pham YC, Reynolds ZJ, Sapienza MS, German BA, McDonnell JE, Schafer CE, Yu VJ, Furbee EC, Grubb SR, Warner MH, Montgomery MT, Garlena RA, Russell DA, Jacobs-Sera D, Hatfull GF. 2016. Genome sequence of Gordonia phage Yvonnetastic. Genome Announc 4:e00594-16. https://doi.org/10.1128/genomeA.00594-16.
22. Pope WH, Benczkowski MS, Green DE, Hwang M, Kennedy B, Kocak B, Kruczek E, Lin L, Moretti ML, Onelangsy FL, Mezghani N, Milliken KA, Toner CL, Thompson PK, Ulbrich MC, Furbee EC, Grubb SR, Warner MH, Montgomery MT, Garlena RA, Russell DA, Jacobs-Sera D, Hatfull GF. 2016. Genome sequences of Gordonia terrae phages Benczkowski14 and Katyusha. Genome Announc 4:e00578-16. https://doi.org/10.1128/genomeA.00578-16.
23. Pope WH, Berryman EN, Forrest KM, McHale L, Wertz AT, Zhuang Z, Kasturiarachi NS, Pressimone CA, Schiebel JG, Furbee EC, Grubb SR, Warner MH, Montgomery MT, Garlena RA, Russell DA, Jacobs-Sera D, Hatfull GF. 2016. Genome sequence of Gordonia phage BetterKatz. Genome Announc 4:e00590-16. https://doi.org/10.1128/genomeA.00590-16.
24. Pope WH, Biery DN, Huff ZT, Huynh AB, McFadden WM, Mouat JS, Schneiderman SE, Song H, Szpak LE, Umbaugh MS, German BA, McDonnell JE, Mezghani N, Schafer CE, Thompson PK, Ulbrich MC, Yu VJ, Furbee EC, Grubb SR, Warner MH, Montgomery MT, Garlena RA, Russell DA, Jacobs- Sera D, Hatfull GF. 2016. Genome sequences of Gordonia terrae phages Attis and SoilAssassin. Genome Announc 4:e00591-16. https://doi.org/10.1128/genomeA.00591-16.
25. Pope WH, Brown AK, Fisher DJ, Okwiya NH, Savage KA, German BA, McDonnell JE, Schafer CE, Yu VJ, Furbee EC, Grubb SR, Warner MH, Montgomery MT, Garlena RA, Russell DA, Jacobs-Sera D, Hatfull GF. 2016. Genome sequence of Gordonia bacteriophage Lucky10. Genome Announc 4:e00580-16. https://doi.org/10.1128/genomeA.00580-16.
26. Pope WH, Davis JP, O’Shea S, Pfeiffer AC, Rich AN, Xue JC, Shedlock KA, Stanton AC, Furbee EC, Grubb SR, Warner MH, Montgomery MT, Garlena RA, Russell DA, Jacobs-Sera D, Hatfull GF. 2016. Genome sequences of Gordonia phages Hotorobo, Woes, and Monty. Genome Announc 4:e00598-16. https://doi.org/10.1128/genomeA.00598-16.
27. Pope WH, Guido MJ, Iyengar P, Nigra JT, Serbin MB, Kasturiarachi NS, Pressimone CA, Schiebel JG, Furbee EC, Grubb SR, Warner MH, Montgomery MT, Garlena RA, Russell DA, Jacobs-Sera D, Hatfull GF. 2016. Genome sequence of Gordonia phage Emalyn. Genome Announc 4:e00597-16. https://doi.org/10.1128/genomeA.00597-16.
28. Pope WH, Montgomery MT, Bonilla JA, Dejong R, Garlena RA, Guerrero Bustamante C, Klyczek KK, Russell DA, Wertz JT, Jacobs-Sera D, Hatfull GF. 2017. Complete genome sequences of 38 Gordonia sp. bacteriophages. Genome Announc 5:e01143-16. https://doi.org/10.1128/genomeA.01143-16.
29. Dyson ZA, Brown TL, Farrar B, Doyle SR, Tucci J, Seviour RJ, Petrovski S. 2016. Locating and activating molecular “time bombs”: induction of Mycolata prophages. PLoS One 11:e0159957. https://doi.org/10.1371/journal.pone.0159957.
30. Petrovski S, Seviour RJ, Tillett D. 2011. Prevention of Gordonia and Nocardia stabilized foam formation by using bacteriophage GTE7. Appl Environ Microbiol 77:7864–7867. https://doi.org/10.1128/AEM.05692-11.
31. Arenskötter M, Bröker D, Steinbüchel A. 2004. Biology of the metabolically diverse genus Gordonia. Appl Environ Microbiol 70:3195–3204. https://doi.org/10.1128/AEM.70.6.3195-3204.2004.
32. Jordan TC, Burnett SH, Carson S, Caruso SM, Clase K, DeJong RJ, Dennehy JJ, Denver DR, Dunbar D, Elgin SC, Findley AM, Gissendanner CR, Golebiewska UP, Guild N, Hartzog GA, Grillo WH, Hollowell GP, Hughes LE, Johnson A, King RA, Lewis LO, Li W, Rosenzweig F, Rubin MR, Saha MS, Sandoz J, Shaffer CD, Taylor B, Temple L, Vazquez E, Ware VC, Barker LP, Bradley KW, Jacobs-Sera D, Pope WH, Russell DA, Cresawn SG, Lopatto D, Bailey CP, Hatfull GF. 2014. A broadly implementable research course in phage discovery and genomics for first-year undergraduate students. mBio 5:e01051-13. https://doi.org/10.1128/mBio.01051-13.
33. Tsukamura M. 1971. Proposal of a new genus, Gordona, for slightly acid-fast organisms occurring in sputa of patients with pulmonary disease and in soil. J Gen Microbiol 68:15–26. https://doi.org/10.1099/00221287-68-1-15.
34. Russell DA, Guerrero Bustamante CA, Garlena RA, Hatfull GF. 2016. Complete genome sequence of Gordonia terrae 3612. Genome Announc 4:e01058-16. https://doi.org/10.1128/genomeA.01058-16.
35. Cresawn SG, Bogel M, Day N, Jacobs-Sera D, Hendrix RW, Hatfull GF. 2011. Phamerator: a bioinformatic tool for comparative bacteriophage genomics. BMC Bioinformatics 12:395. https://doi.org/10.1186/1471-2105-12-395.
36. Pope WH, Jacobs-Sera D, Russell DA, Peebles CL, Al-Atrache Z, Alcoser TA, Alexander LM, Alfano MB, Alford ST, Amy NE, Anderson MD, Anderson AG, Ang AA, Ares M, Barber AJ, Barker LP, Barrett JM, Barshop WD, Bauerle CM, Bayles IM, Belfield KL, Best AA, Borjon A, Bowman CA, Boyer CA, Bradley KW, Bradley VA, Broadway LN, Budwal K, Busby KN, Campbell IW, Campbell AM, Carey A, Caruso SM, Chew RD, Cockburn CL, Cohen LB, Corajod JM, Cresawn SG, Davis KR. 2011. Expanding the diversity of mycobacteriophages: insights into genome architecture and evolution. PLoS One 6:e16329. https://doi.org/10.1371/journal.pone.0016329.
37. 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 49:237–248. https://doi.org/10.1016/j.molcel.2012.11.012.
38. Smith MC, Thorpe HM. 2002. Diversity in the serine recombinases. Mol Microbiol 44:299–307. https://doi.org/10.1046/j.1365-2958.2002.02891.x.
39. Payne K, Sun Q, Sacchettini J, Hatfull GF. 2009. Mycobacteriophage lysin B is a novel mycolylarabinogalactan esterase. Mol Microbiol 73:367–381. https://doi.org/10.1111/j.1365-2958.2009.06775.x.
40. Dedrick RM, Jacobs-Sera D, Bustamante CA, Garlena RA, Mavrich TN, Pope WH, Reyes JC, Russell DA, Adair T, Alvey R, Bonilla JA, Bricker JS, Brown BR, Byrnes D, Cresawn SG, Davis WB, Dickson LA, Edgington NP, Findley AM, Golebiewska U, Grose JH, Hayes CF, Hughes LE, Hutchison KW, Isern S, Johnson AA, Kenna MA, Klyczek KK, Mageeney CM, Michael SF, Molloy SD, Montgomery MT, Neitzel J, Page ST, Pizzorno MC, Poxleitner MK, Rinehart CA, Robinson CJ, Rubin MR, Teyim JN, Vazquez E, Ware VC, Washington J, Hatfull GF. 2017. Prophage-mediated defence against viral attack and viral counter-defence. Nat Microbiol 2:16251. https://doi.org/10.1038/nmicrobiol.2016.251.
41. Payne KM, Hatfull GF. 2012. Mycobacteriophage endolysins: diverse and modular enzymes with multiple catalytic activities. PLoS One 7:e34052. https://doi.org/10.1371/journal.pone.0034052.
42. Petrovski S, Dyson ZA, Seviour RJ, Tillett D. 2012. Small but sufficient: the Rhodococcus phage RRH1 has the smallest known Siphoviridae genome at 14.2 kilobases. J Virol 86:358–363. https://doi.org/10.1128/JVI.05460-11.
43. Brown KL, Sarkis GJ, Wadsworth C, Hatfull GF. 1997. Transcriptional silencing by the mycobacteriophage L5 repressor. EMBO J 16:5914–5921.
44. Lee MH, Pascopella L, Jacobs WR, Jr, Hatfull GF. 1991. Site-specific integration of mycobacteriophage L5: integration-proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and Bacille Calmette-Guerin. Proc Natl Acad Sci U S A 88:3111–3115. https://doi.org/10.1073/pnas.88.8.3111.
45. Kim AI, Ghosh P, Aaron MA, Bibb LA, Jain S, Hatfull GF. 2003. Mycobacteriophage Bxb1 integrates into the Mycobacterium smegmatis groEL1 gene. Mol Microbiol 50:463–473. https://doi.org/10.1046/j.1365-2958.2003.03723.x.
46. Dedrick RM, Mavrich TN, Ng WL, Cervantes Reyes JC, Olm MR, Rush RE, Jacobs-Sera D, Russell DA, Hatfull GF. 2016. Function, expression, specificity, diversity and incompatibility of actinobacteriophage parABS systems. Mol Microbiol 101:625–644. https://doi.org/10.1111/mmi.13414.
47. Stella EJ, Franceschelli JJ, Tasselli SE, Morbidoni HR. 2013. Analysis of novel mycobacteriophages indicates the existence of different strategies for phage inheritance in mycobacteria. PLoS One 8:e56384. https://doi.org/10.1371/journal.pone.0056384.
48. Ford ME, Sarkis GJ, Belanger AE, Hendrix RW, Hatfull GF. 1998. Genome structure of mycobacteriophage D29: implications for phage evolution. J Mol Biol 279:143–164. https://doi.org/10.1006/jmbi.1997.1610.
49. Mavrich TN, Hatfull GF. 2017. Bacteriophage evolution differs by host, lifestyle, and genome. Nat Microbiol 2:17112. https://doi.org/10.1038/nmicrobiol.2017.112.
50. Marinelli LJ, Fitz-Gibbon S, Hayes C, Bowman C, Inkeles M, Loncaric A, Russell DA, Jacobs-Sera D, Cokus S, Pellegrini M, Kim J, Miller JF, Hatfull GF, Modlin RL. 2012. Propionibacterium acnes bacteriophages display limited genetic diversity and broad killing activity against bacterial skin isolates. mBio 3:e00279-12. https://doi.org/10.1128/mBio.00279-12.
51. Jacobs WR, Jr, Snapper SB, Tuckman M, Bloom BR. 1989. Mycobacteriophage vector systems. Rev Infect Dis 11(Suppl 2):S404–S410. https://doi.org/10.1093/clinids/11.Supplement_2.S404.
52. Bardarov S, Kriakov J, Carriere C, Yu S, Vaamonde C, McAdam RA, Bloom BR, Hatfull GF, Jacobs WR, Jr. 1997. Conditionally replicating mycobacteriophages: a system for transposon delivery to Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 94:10961–10966. https://doi.org/10.1073/pnas.94.20.10961.
53. Besemer J, Borodovsky M. 2005. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res 33:W451–W454. https://doi.org/10.1093/nar/gki487.
54. Delcher AL, Bratke KA, Powers EC, Salzberg SL. 2007. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23:673–679. https://doi.org/10.1093/bioinformatics/btm009.
55. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2.
56. Laslett D, Canback B. 2004. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32:11–16. https://doi.org/10.1093/nar/gkh152.
57. Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964. https://doi.org/10.1093/nar/25.5.0955.
58. Söding J, Biegert A, Lupas AN. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244–W248. https://doi.org/10.1093/nar/gki408.
59. Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030.
60. Huson DH. 1998. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73. https://doi.org/10.1093/bioinformatics/14.1.68.
61. Klyczek KK, Bonilla JA, Jacobs-Sera D, Adair TL, Afram P, Allen KG, et al. 2017. Tales of diversity: Genomic and morphological characteristics of forty-six Arthrobacter phages. PLoS ONE 12:e0180517. https://doi.org/10.1371/journal.pone.0180517.