1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

The Bacteriophages of

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • Authors: W. Michael McShan1, Kimberly A. McCullor2, Scott V. Nguyen3
  • Editors: Vincent A. Fischetti5, Richard P. Novick6, Joseph J. Ferretti7, Daniel A. Portnoy8, Miriam Braunstein9, Julian I. Rood10
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Pharmaceutical Sciences, College of Pharmacy, The University of Oklahoma Health Sciences Center, Oklahoma City, OK, 73117; 2: Department of Pharmaceutical Sciences, College of Pharmacy, The University of Oklahoma Health Sciences Center, Oklahoma City, OK, 73117; 3: Department of Pharmaceutical Sciences, College of Pharmacy, The University of Oklahoma Health Sciences Center, Oklahoma City, OK, 73117; 4: Current address: UCD-Centre for Food Safety, School of Public Health, Physiotherapy and Sports Science, University College Dublin, Dublin, Ireland; 5: The Rockefeller University, New York, NY; 6: Skirball Institute for Molecular Medicine, NYU Medical Center, New York, NY; 7: Department of Microbiology & Immunology, University of Oklahoma Health Science Center, Oklahoma City, OK; 8: Department of Molecular and Cellular Microbiology, University of California, Berkeley, Berkeley, CA; 9: Department of Microbiology and Immunology, University of North Carolina-Chapel Hill, Chapel Hill, NC; 10: Infection and Immunity Program, Monash Biomedicine Discovery Institute, Monash University, Melbourne, Australia
  • Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
  • Received 03 December 2018 Accepted 23 January 2019 Published 17 May 2019
  • W. Michael McShan, [email protected]
image of The Bacteriophages of <span class="jp-italic">Streptococcus pyogenes</span>
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    The Bacteriophages of , Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/7/3/GPP3-0059-2018-1.gif /docserver/preview/fulltext/microbiolspec/7/3/GPP3-0059-2018-2.gif
  • Abstract:

    The bacteriophages of (group A streptococcus) play a key role in population shaping, genetic transfer, and virulence of this bacterial pathogen. Lytic phages like A25 can alter population distributions through elimination of susceptible serotypes but also serve as key mediators for genetic transfer of virulence genes and antibiotic resistance via generalized transduction. The sequencing of multiple genomes has uncovered a large and diverse population of endogenous prophages that are vectors for toxins and other virulence factors and occupy multiple attachment sites in the bacterial genomes. Some of these sites for integration appear to have the potential to alter the bacterial phenotype through gene disruption. Remarkably, the phage-like chromosomal islands (SpyCI), which share many characteristics with endogenous prophages, have evolved to mediate a growth-dependent mutator phenotype while acting as global transcriptional regulators. The diverse population of prophages appears to share a large pool of genetic modules that promotes novel combinations that may help disseminate virulence factors to different subpopulations of . The study of the bacteriophages of this pathogen, both lytic and lysogenic, will continue to be an important endeavor for our understanding of how continues to be a significant cause of human disease.

  • Citation: McShan W, McCullor K, Nguyen S. 2019. The Bacteriophages of . Microbiol Spectrum 7(3):GPP3-0059-2018. doi:10.1128/microbiolspec.GPP3-0059-2018.

References

1. Twort FW. 1915. An investigation on the nature of ultra-microscopic viruses. Lancet 186:1241–1243 http://dx.doi.org/10.1016/S0140-6736(01)20383-3.
2. Cantacuzene J, Boncieu O. 1926. Modifications subies pare des streptococques d’origine non-scarlatineuse qu contact des produits scarlatineux filtres. C R Acad Sci 182:1185.
3. Frobisher M, Brown JH. 1927. Transmissible toxicogenicity of streptococci. Bull Johns Hopkins Hosp 41:167–173.
4. Evans AC. 1933. Inactivation of antistreptococcus bacteriophage by animal fluids. Public Health Rep 48:411–426 http://dx.doi.org/10.2307/4580757.
5. Evans AC. 1934. Streptococcus bacteriophage: a study of four serological types. Public Health Rep 49:1386–1401 http://dx.doi.org/10.2307/4581377.
6. Evans AC. 1934. The prevalence of Streptococcus bacteriophage. Science 80:40–41 http://dx.doi.org/10.1126/science.80.2063.40. [PubMed]
7. Evans AC. 1940. The potency of nascent Streptococcus bacteriophage B. J Bacteriol 39:597–604.
8. Evans AC, Sockrider EM. 1942. Another serologic type of streptococcic bacteriophage. J Bacteriol 44:211–214.
9. Kjems E. 1960. Studies on streptococcal bacteriophages. 4. The occurrence of lysogenic strains among group A haemolytic streptococci. Acta Pathol Microbiol Scand 49:199–204 http://dx.doi.org/10.1111/j.1699-0463.1960.tb01130.x.
10. Krause RM. 1957. Studies on bacteriophages of hemolytic streptococci. I. Factors influencing the interaction of phage and susceptible host cell. J Exp Med 106:365–384 http://dx.doi.org/10.1084/jem.106.3.365. [PubMed]
11. Maxted WR. 1952. Enhancement of streptococcal bacteriophage lysis by hyaluronidase. Nature 170:1020–1021 http://dx.doi.org/10.1038/1701020b0. [PubMed]
12. Maxted WR. 1955. The influence of bacteriophage on Streptococcus pyogenes. J Gen Microbiol 12:484–495 http://dx.doi.org/10.1099/00221287-12-3-484. [PubMed]
13. Kjems E. 1958. Studies on streptococcal bacteriophages. 3. Hyaluronidase produced by the streptococcal phage-host cell system. Acta Pathol Microbiol Scand 44:429–439 http://dx.doi.org/10.1111/j.1699-0463.1958.tb01094.x.
14. Kjems E. 1955. Studies on streptococcal bacteriophages. I. Technique of isolating phage-producing strains. Acta Pathol Microbiol Scand 36:433–440 http://dx.doi.org/10.1111/j.1699-0463.1955.tb04638.x.
15. Maxted W. 1964. Streptococcal bacteriophages, p 25–52. In Uhr J (ed), Streptococci, Rheumatic Fever, and Glomerulonephritis. Williams and Wilkins Co, Baltimore, MD.
16. Zabriskie JB. 1964. The role of temperate bacteriophage in the production of erythrogenic toxin by group A streptococci. J Exp Med 119:761–780 http://dx.doi.org/10.1084/jem.119.5.761. [PubMed]
17. Weeks CR, Ferretti JJ. 1984. The gene for type A streptococcal exotoxin (erythrogenic toxin) is located in bacteriophage T12. Infect Immun 46:531–536.
18. Weeks CR, Ferretti JJ. 1986. Nucleotide sequence of the type A streptococcal exotoxin (erythrogenic toxin) gene from Streptococcus pyogenes bacteriophage T12. Infect Immun 52:144–150.
19. Johnson LP, Schlievert PM. 1984. Group A streptococcal phage T12 carries the structural gene for pyrogenic exotoxin type A. Mol Gen Genet 194:52–56 http://dx.doi.org/10.1007/BF00383496.
20. Ferretti J, Köhler W. History of streptococcal research. In Ferretti J, Stevens D, Fischetti V (ed), Streptococcus pyogenes : Basic Biology to Clinical Manifestations. University of Oklahoma Health Sciences Center, Oklahoma City, OK. https://www.ncbi.nlm.nih.gov/pubmed/26866232.
21. Mashburn-Warren L, Morrison DA, Federle MJ. 2012. The cryptic competence pathway in Streptococcus pyogenes is controlled by a peptide pheromone. J Bacteriol 194:4589–4600 http://dx.doi.org/10.1128/JB.00830-12. [PubMed]
22. Leonard CG, Colón AE, Cole RM. 1968. Transduction in group A streptococcus. Biochem Biophys Res Commun 30:130–135 http://dx.doi.org/10.1016/0006-291X(68)90459-2.
23. Pomrenke ME, Ferretti JJ. 1989. Physical maps of the streptococcal bacteriophage A25 and C1 genomes. J Basic Microbiol 29:395–398 http://dx.doi.org/10.1002/jobm.3620290621. [PubMed]
24. Moynet DJ, Colon-Whitt AE, Calandra GB, Cole RM. 1985. Structure of eight streptococcal bacteriophages. Virology 142:263–269 http://dx.doi.org/10.1016/0042-6822(85)90334-4.
25. Malke H. 1970. Characteristics of transducing group A streptococcal bacteriophages A 5 and A 25. Arch Gesamte Virusforsch 29:44–49 http://dx.doi.org/10.1007/BF01253879. [PubMed]
26. Zabriskie JB, Read SE, Fischetti VA. 1972. Lysogeny in streptococci, p 99–118. In Wannamaker LW, Matsen JM (ed), Streptococci and Streptococcal Diseases: Recognition, Understanding, and Management. Academic Press, New York, NY.
27. Read SE, Reed RW. 1972. Electron microscopy of the replicative events of A25 bacteriophages in group A streptococci. Can J Microbiol 18:93–96 http://dx.doi.org/10.1139/m72-015. [PubMed]
28. Hill JE, Wannamaker LW. 1981. Identification of a lysin associated with a bacteriophage (A25) virulent for group A streptococci. J Bacteriol 145:696–703.
29. Malke H. 1969. Transduction of Streptococcus pyogenes K 56 by temperature-sensitive mutants of the transducing phage A 25. Z Naturforsch B 24:1556–1561 http://dx.doi.org/10.1515/znb-1969-1214.
30. Fischetti VA, Barron B, Zabriskie JB. 1968. Studies on streptococcal bacteriophages. I. Burst size and intracellular growth of group A and group C streptococcal bacteriophages. J Exp Med 127:475–488 http://dx.doi.org/10.1084/jem.127.3.475. [PubMed]
31. Cleary PP, Wannamaker LW, Fisher M, Laible N. 1977. Studies of the receptor for phage A25 in group A streptococci: the role of peptidoglycan in reversible adsorption. J Exp Med 145:578–593 http://dx.doi.org/10.1084/jem.145.3.578. [PubMed]
32. McCullor K, Postoak B, Rahman M, King C, McShan WM. 2018. Genomic sequencing of high-efficiency transducing streptococcal bacteriophage A25: consequences of escape from lysogeny. J Bacteriol 200:e00358-18. [PubMed]
33. Wannamaker LW, Almquist S, Skjold S. 1973. Intergroup phage reactions and transduction between group C and group A streptococci. J Exp Med 137:1338–1353 http://dx.doi.org/10.1084/jem.137.6.1338. [PubMed]
34. Casjens SR, Gilcrease EB. 2009. Determining DNA packaging strategy by analysis of the termini of the chromosomes in tailed-bacteriophage virions. Methods Mol Biol 502:91–111 http://dx.doi.org/10.1007/978-1-60327-565-1_7. [PubMed]
35. Marks LR, Mashburn-Warren L, Federle MJ, Hakansson AP. 2014. Streptococcus pyogenes biofilm growth in vitro and in vivo and its role in colonization, virulence, and genetic exchange. J Infect Dis 210:25–34 http://dx.doi.org/10.1093/infdis/jiu058. [PubMed]
36. Crater DL, van de Rijn I. 1995. Hyaluronic acid synthesis operon ( has) expression in group A streptococci. J Biol Chem 270:18452–18458 http://dx.doi.org/10.1074/jbc.270.31.18452. [PubMed]
37. Henningham A, Yamaguchi M, Aziz RK, Kuipers K, Buffalo CZ, Dahesh S, Choudhury B, Van Vleet J, Yamaguchi Y, Seymour LM, Ben Zakour NL, He L, Smith HV, Grimwood K, Beatson SA, Ghosh P, Walker MJ, Nizet V, Cole JN. 2014. Mutual exclusivity of hyaluronan and hyaluronidase in invasive group A Streptococcus. J Biol Chem 289:32303–32315 http://dx.doi.org/10.1074/jbc.M114.602847. [PubMed]
38. Malke H. 1972. Linkage relationships of mutations endowing Streptococcus pyogenes with resistance to antibiotics that affect the ribosome. Mol Gen Genet 116:299–308 http://dx.doi.org/10.1007/BF00270087.
39. Colón AE, Cole RM, Leonard CG. 1970. Transduction in group A streptococci by ultraviolet-irradiated bacteriophages. Can J Microbiol 16:201–202 http://dx.doi.org/10.1139/m70-034. [PubMed]
40. Malke H. 1969. Transduction of Streptococcus pyogenes K 56 by temperature-sensitive mutants of the transducing phage A 25. Z Naturforsch B 24:1556–1561 http://dx.doi.org/10.1515/znb-1969-1214.
41. Hyder SL, Streitfeld MM. 1978. Transfer of erythromycin resistance from clinically isolated lysogenic strains of Streptococcus pyogenes via their endogenous phage. J Infect Dis 138:281–286 http://dx.doi.org/10.1093/infdis/138.3.281. [PubMed]
42. Colón AE, Cole RM, Leonard CG. 1972. Intergroup lysis and transduction by streptococcal bacteriophages. J Virol 9:551–553.
43. Bessen DE, McShan WM, Nguyen SV, Agarwal S, Shetty A, Tettelin H. 2015. Molecular epidemiology and genomics of group A Streptococcus. Infect Genet Evol 33:393–418. [PubMed]
44. Chaussee MS, Liu J, Stevens DL, Ferretti JJ. 1996. Genetic and phenotypic diversity among isolates of Streptococcus pyogenes from invasive infections. J Infect Dis 173:901–908 http://dx.doi.org/10.1093/infdis/173.4.901. [PubMed]
45. Hynes WL, Hancock L, Ferretti JJ. 1995. Analysis of a second bacteriophage hyaluronidase gene from Streptococcus pyogenes: evidence for a third hyaluronidase involved in extracellular enzymatic activity. Infect Immun 63:3015–3020.
46. Wannamaker LW, Skjold S, Maxted WR. 1970. Characterization of bacteriophages from nephritogenic group A streptococci. J Infect Dis 121:407–418 http://dx.doi.org/10.1093/infdis/121.4.407. [PubMed]
47. Yu C-E, Ferretti JJ. 1989. Molecular epidemiologic analysis of the type A streptococcal exotoxin (erythrogenic toxin) gene ( speA) in clinical Streptococcus pyogenes strains. Infect Immun 57:3715–3719.
48. Campbell AM. 1992. Chromosomal insertion sites for phages and plasmids. J Bacteriol 174:7495–7499 http://dx.doi.org/10.1128/jb.174.23.7495-7499.1992. [PubMed]
49. Groth AC, Calos MP. 2004. Phage integrases: biology and applications. J Mol Biol 335:667–678 http://dx.doi.org/10.1016/j.jmb.2003.09.082. [PubMed]
50. Fouts DE. 2006. Phage_Finder: automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Res 34:5839–5851 http://dx.doi.org/10.1093/nar/gkl732. [PubMed]
51. McShan WM, Ferretti JJ. 2007. Bacteriophages and the host phenotype, p 229–250. In McGrath S (ed), Bacteriophages: genetics and molecular biology. Horizon Scientific Press, Hethersett, Norwich, UK.
52. Nguyen SV, McShan WM. 2014. Chromosomal islands of Streptococcus pyogenes and related streptococci: molecular switches for survival and virulence. Front Cell Infect Microbiol 4:109 http://dx.doi.org/10.3389/fcimb.2014.00109. [PubMed]
53. Scott J, Nguyen S, King CJ, Hendrickson C, McShan WM. 2012. Mutator phenotype prophages in the genome strains of Streptococcus pyogenes: control by growth state and by a cryptic prophage-encoded promoter. Front Microbiol 3:317.
54. Scott J, Thompson-Mayberry P, Lahmamsi S, King CJ, McShan WM. 2008. Phage-associated mutator phenotype in group A Streptococcus. J Bacteriol 190:6290–6301 http://dx.doi.org/10.1128/JB.01569-07. [PubMed]
55. D’Ercole S, Petrelli D, Prenna M, Zampaloni C, Catania MR, Ripa S, Vitali LA. 2005. Distribution of mef(A)-containing genetic elements in erythromycin-resistant isolates of Streptococcus pyogenes from Italy. Clin Microbiol Infect 11:927–930 http://dx.doi.org/10.1111/j.1469-0691.2005.01250.x. [PubMed]
56. Claverys J-P, Martin B. 1998. Competence regulons, genomics and streptococci. Mol Microbiol 29:1126–1127 http://dx.doi.org/10.1046/j.1365-2958.1998.01005.x. [PubMed]
57. McShan WM, Tang Y-F, Ferretti JJ. 1997. Bacteriophage T12 of Streptococcus pyogenes integrates into the gene encoding a serine tRNA. Mol Microbiol 23:719–728 http://dx.doi.org/10.1046/j.1365-2958.1997.2591616.x. [PubMed]
58. Williams KP. 2002. Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic Acids Res 30:866–875 http://dx.doi.org/10.1093/nar/30.4.866. [PubMed]
59. Brüssow H, Hendrix RW. 2002. Phage genomics: small is beautiful. Cell 108:13–16 http://dx.doi.org/10.1016/S0092-8674(01)00637-7.
60. Ackermann HW. 2006. Classification of bacteriophages, p 8–16. In Calendar R (ed), The Bacteriophages, 2nd ed. Oxford University Press, New York, NY.
61. Ackermann H-W, DuBow MS. 1987. Viruses of Prokaryotes: General Properties of Bacteriophages, vol 1. CRC Press, Boca Raton, FL.
62. Smith NL, Taylor EJ, Lindsay AM, Charnock SJ, Turkenburg JP, Dodson EJ, Davies GJ, Black GW. 2005. Structure of a group A streptococcal phage-encoded virulence factor reveals a catalytically active triple-stranded beta-helix. Proc Natl Acad Sci U S A 102:17652–17657 http://dx.doi.org/10.1073/pnas.0504782102. [PubMed]
63. Nelson D, Schuch R, Zhu S, Tscherne DM, Fischetti VA. 2003. Genomic sequence of C1, the first streptococcal phage. J Bacteriol 185:3325–3332 http://dx.doi.org/10.1128/JB.185.11.3325-3332.2003. [PubMed]
64. Desiere F, McShan WM, van Sinderen D, Ferretti JJ, Brüssow H. 2001. Comparative genomics reveals close genetic relationships between phages from dairy bacteria and pathogenic streptococci: evolutionary implications for prophage-host interactions. Virology 288:325–341 http://dx.doi.org/10.1006/viro.2001.1085. [PubMed]
65. Canchaya C, Desiere F, McShan WM, Ferretti JJ, Parkhill J, Brüssow H. 2002. Genome analysis of an inducible prophage and prophage remnants integrated in the Streptococcus pyogenes strain SF370. Virology 302:245–258 http://dx.doi.org/10.1006/viro.2002.1570. [PubMed]
66. Ptashne M. 2004. A Genetic Switch: Phage Lambda Revisited, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
67. Campbell A, del-Campillo-Campbell A, Ginsberg ML. 2002. Specificity in DNA recognition by phage integrases. Gene 300:13–18 http://dx.doi.org/10.1016/S0378-1119(02)00846-6.
68. Argos P, Landy A, Abremski K, Egan JB, Haggard-Ljungquist E, Hoess RH, Kahn ML, Kalionis B, Narayana SV, Pierson LS. 1986. The integrase family of site-specific recombinases: regional similarities and global diversity. EMBO J 5:433–440 http://dx.doi.org/10.1002/j.1460-2075.1986.tb04229.x. [PubMed]
69. Bruttin A, Desiere F, Lucchini S, Foley S, Brüssow H. 1997. Characterization of the lysogeny DNA module from the temperate Streptococcus thermophilus bacteriophage phi Sfi21. Virology 233:136–148 http://dx.doi.org/10.1006/viro.1997.8603. [PubMed]
70. Breüner A, Brøndsted L, Hammer K. 1999. Novel organization of genes involved in prophage excision identified in the temperate lactococcal bacteriophage TP901-1. J Bacteriol 181:7291–7297.
71. Lewis JA, Hatfull GF. 2001. Control of directionality in integrase-mediated recombination: examination of recombination directionality factors (RDFs) including Xis and Cox proteins. Nucleic Acids Res 29:2205–2216 http://dx.doi.org/10.1093/nar/29.11.2205. [PubMed]
72. Hynes WL, Ferretti JJ. 1989. Sequence analysis and expression in Escherichia coli of the hyaluronidase gene of Streptococcus pyogenes bacteriophage H4489A. Infect Immun 57:533–539.
73. Barksdale L, Arden SB. 1974. Persisting bacteriophage infections, lysogeny, and phage conversions. Annu Rev Microbiol 28:265–299 http://dx.doi.org/10.1146/annurev.mi.28.100174.001405. [PubMed]
74. Proft T, Sriskandan S, Yang L, Fraser JD. 2003. Superantigens and streptococcal toxic shock syndrome. Emerg Infect Dis 9:1211–1218 http://dx.doi.org/10.3201/eid0910.030042. [PubMed]
75. Proft T, Moffatt SL, Berkahn CJ, Fraser JD. 1999. Identification and characterization of novel superantigens from Streptococcus pyogenes. J Exp Med 189:89–102 http://dx.doi.org/10.1084/jem.189.1.89. [PubMed]
76. Ochman H, Lawrence JG, Groisman EA. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304 http://dx.doi.org/10.1038/35012500. [PubMed]
77. Brüssow H, Canchaya C, Hardt WD. 2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68:560–602 http://dx.doi.org/10.1128/MMBR.68.3.560-602.2004. [PubMed]
78. Botstein D. 1980. A theory of modular evolution for bacteriophages. Ann N Y Acad Sci 354:484–490 http://dx.doi.org/10.1111/j.1749-6632.1980.tb27987.x. [PubMed]
79. 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 http://dx.doi.org/10.1006/jmbi.1997.1610. [PubMed]
80. Lucchini S, Desiere F, Brüssow H. 1999. Similarly organized lysogeny modules in temperate Siphoviridae from low GC content gram-positive bacteria. Virology 263:427–435 http://dx.doi.org/10.1006/viro.1999.9959. [PubMed]
81. Monod C, Repoila F, Kutateladze M, Tétart F, Krisch HM. 1997. The genome of the pseudo T-even bacteriophages, a diverse group that resembles T4. J Mol Biol 267:237–249 http://dx.doi.org/10.1006/jmbi.1996.0867. [PubMed]
82. Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, Hendrix RW. 2000. Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299:27–51 http://dx.doi.org/10.1006/jmbi.2000.3729. [PubMed]
83. Aziz RK, Edwards RA, Taylor WW, Low DE, McGeer A, Kotb M. 2005. Mosaic prophages with horizontally acquired genes account for the emergence and diversification of the globally disseminated M1T1 clone of Streptococcus pyogenes. J Bacteriol 187:3311–3318 http://dx.doi.org/10.1128/JB.187.10.3311-3318.2005. [PubMed]
84. Marciel AM, Kapur V, Musser JM. 1997. Molecular population genetic analysis of a Streptococcus pyogenes bacteriophage-encoded hyaluronidase gene: recombination contributes to allelic variation. Microb Pathog 22:209–217 http://dx.doi.org/10.1006/mpat.1996.9999. [PubMed]
85. Mylvaganam H, Bjorvatn B, Hofstad T, Osland A. 2000. Molecular characterization and allelic distribution of the phage-mediated hyaluronidase genes hylP and hylP2 among group A streptococci from western Norway. Microb Pathog 29:145–153 http://dx.doi.org/10.1006/mpat.2000.0378. [PubMed]
86. Martinez-Fleites C, Smith NL, Turkenburg JP, Black GW, Taylor EJ. 2009. Structures of two truncated phage-tail hyaluronate lyases from Streptococcus pyogenes serotype M1. Acta Crystallogr Sect F Struct Biol Cryst Commun 65:963–966 http://dx.doi.org/10.1107/S1744309109032813. [PubMed]
87. Holden MT, Heather Z, Paillot R, Steward KF, Webb K, Ainslie F, Jourdan T, Bason NC, Holroyd NE, Mungall K, Quail MA, Sanders M, Simmonds M, Willey D, Brooks K, Aanensen DM, Spratt BG, Jolley KA, Maiden MC, Kehoe M, Chanter N, Bentley SD, Robinson C, Maskell DJ, Parkhill J, Waller AS. 2009. Genomic evidence for the evolution of Streptococcus equi: host restriction, increased virulence, and genetic exchange with human pathogens. PLoS Pathog 5:e1000346 http://dx.doi.org/10.1371/journal.ppat.1000346. [PubMed]
88. Bai Q, Zhang W, Yang Y, Tang F, Nguyen X, Liu G, Lu C. 2013. Characterization and genome sequencing of a novel bacteriophage infecting Streptococcus agalactiae with high similarity to a phage from Streptococcus pyogenes. Arch Virol 158:1733–1741 http://dx.doi.org/10.1007/s00705-013-1667-x. [PubMed]
89. Obregón V, García JL, García E, López R, García P. 2003. Genome organization and molecular analysis of the temperate bacteriophage MM1 of Streptococcus pneumoniae. J Bacteriol 185:2362–2368 http://dx.doi.org/10.1128/JB.185.7.2362-2368.2003. [PubMed]
90. Siboo IR, Bensing BA, Sullam PM. 2003. Genomic organization and molecular characterization of SM1, a temperate bacteriophage of Streptococcus mitis. J Bacteriol 185:6968–6975 http://dx.doi.org/10.1128/JB.185.23.6968-6975.2003. [PubMed]
91. van Sinderen D, Karsens H, Kok J, Terpstra P, Ruiters MHJ, Venema G, Nauta A. 1996. Sequence analysis and molecular characterization of the temperate lactococcal bacteriophage r1t. Mol Microbiol 19:1343–1355 http://dx.doi.org/10.1111/j.1365-2958.1996.tb02478.x. [PubMed]
92. Venturini C, Ong CL, Gillen CM, Ben-Zakour NL, Maamary PG, Nizet V, Beatson SA, Walker MJ. 2013. Acquisition of the Sda1-encoding bacteriophage does not enhance virulence of the serotype M1 Streptococcus pyogenes strain SF370. Infect Immun 81:2062–2069 http://dx.doi.org/10.1128/IAI.00192-13. [PubMed]
93. Anbalagan S, Chaussee MS. 2013. Transcriptional regulation of a bacteriophage encoded extracellular DNase (Spd-3) by Rgg in Streptococcus pyogenes. PLoS One 8:e61312 http://dx.doi.org/10.1371/journal.pone.0061312. [PubMed]
94. Broudy TB, Pancholi V, Fischetti VA. 2001. Induction of lysogenic bacteriophage and phage-associated toxin from group a streptococci during coculture with human pharyngeal cells. Infect Immun 69:1440–1443 http://dx.doi.org/10.1128/IAI.69.3.1440-1443.2001. [PubMed]
95. Broudy TB, Pancholi V, Fischetti VA. 2002. The in vitro interaction of Streptococcus pyogenes with human pharyngeal cells induces a phage-encoded extracellular DNase. Infect Immun 70:2805–2811 http://dx.doi.org/10.1128/IAI.70.6.2805-2811.2002. [PubMed]
96. Banks DJ, Lei B, Musser JM. 2003. Prophage induction and expression of prophage-encoded virulence factors in group A Streptococcus serotype M3 strain MGAS315. Infect Immun 71:7079–7086 http://dx.doi.org/10.1128/IAI.71.12.7079-7086.2003. [PubMed]
97. Broudy TB, Fischetti VA. 2003. In vivo lysogenic conversion of Tox(-) Streptococcus pyogenes to Tox(+) with lysogenic streptococci or free phage. Infect Immun 71:3782–3786 http://dx.doi.org/10.1128/IAI.71.7.3782-3786.2003. [PubMed]
98. Aziz RK, Pabst MJ, Jeng A, Kansal R, Low DE, Nizet V, Kotb M. 2004. Invasive M1T1 group A Streptococcus undergoes a phase-shift in vivo to prevent proteolytic degradation of multiple virulence factors by SpeB. Mol Microbiol 51:123–134 http://dx.doi.org/10.1046/j.1365-2958.2003.03797.x.
99. Brenciani A, Bacciaglia A, Vignaroli C, Pugnaloni A, Varaldo PE, Giovanetti E. 2010. Phim46.1, the main Streptococcus pyogenes element carrying mef(A) and tet(O) genes. Antimicrob Agents Chemother 54:221–229 http://dx.doi.org/10.1128/AAC.00499-09. [PubMed]
100. Banks DJ, Porcella SF, Barbian KD, Beres SB, Philips LE, Voyich JM, DeLeo FR, Martin JM, Somerville GA, Musser JM. 2004. Progress toward characterization of the group A Streptococcus metagenome: complete genome sequence of a macrolide-resistant serotype M6 strain. J Infect Dis 190:727–738 http://dx.doi.org/10.1086/422697. [PubMed]
101. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, Deboy RT, Davidsen TM, Mora M, Scarselli M, Margarit y Ros I, Peterson JD, Hauser CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou L, Zafar N, Khouri H, Radune D, Dimitrov G, Watkins K, O’Connor KJ, Smith S, Utterback TR, White O, Rubens CE, Grandi G, Madoff LC, Kasper DL, Telford JL, Wessels MR, Rappuoli R, Fraser CM. 2005. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial “pan-genome”. Proc Natl Acad Sci U S A 102:13950–13955 http://dx.doi.org/10.1073/pnas.0506758102. [PubMed]
102. Giovanetti E, Brenciani A, Morroni G, Tiberi E, Pasquaroli S, Mingoia M, Varaldo PE. 2015. Transduction of the Streptococcus pyogenes bacteriophage Φm46.1, carrying resistance genes mef(A) and tet(O), to other Streptococcus species. Front Microbiol 5:746 http://dx.doi.org/10.3389/fmicb.2014.00746.
103. Di Luca MC, D’Ercole S, Petrelli D, Prenna M, Ripa S, Vitali LA. 2010. Lysogenic transfer of mef(A) and tet(O) genes carried by Phim46.1 among group A streptococci. Antimicrob Agents Chemother 54:4464–4466 http://dx.doi.org/10.1128/AAC.01318-09. [PubMed]
104. Anbalagan S, McShan WM, Dunman PM, Chaussee MS. 2011. Identification of Rgg binding sites in the Streptococcus pyogenes chromosome. J Bacteriol 193:4933–4942 http://dx.doi.org/10.1128/JB.00429-11. [PubMed]
105. Brown L, Kim JH, Cho KH. 2016. Presence of a prophage determines temperature-dependent capsule production in Streptococcus pyogenes. Genes (Basel) 7:E74 http://dx.doi.org/10.3390/genes7100074. [PubMed]
106. Novick RP, Christie GE, Penadés JR. 2010. The phage-related chromosomal islands of Gram-positive bacteria. Nat Rev Microbiol 8:541–551 http://dx.doi.org/10.1038/nrmicro2393. [PubMed]
107. Hendrickson C, Euler CW, Nguyen SV, Rahman M, McCullor KA, King CJ, Fischetti VA, McShan WM. 2015. Elimination of chromosomal island SpyCIM1 from Streptococcus pyogenes strain SF370 reverses the mutator phenotype and alters global transcription. PLoS One 10:e0145884 http://dx.doi.org/10.1371/journal.pone.0145884. [PubMed]
108. Bao YJ, Liang Z, Mayfield JA, McShan WM, Lee SW, Ploplis VA, Castellino FJ. 2016. Novel genomic rearrangements mediated by multiple genetic elements in Streptococcus pyogenes M23ND confer potential for evolutionary persistence. Microbiology 162:1346–1359 http://dx.doi.org/10.1099/mic.0.000326. [PubMed]
109. Bao Y, Liang Z, Booyjzsen C, Mayfield JA, Li Y, Lee SW, Ploplis VA, Song H, Castellino FJ. 2014. Unique genomic arrangements in an invasive serotype M23 strain of Streptococcus pyogenes identify genes that induce hypervirulence. J Bacteriol 196:4089–4102 http://dx.doi.org/10.1128/JB.02131-14. [PubMed]
110. Reese MG, Eeckman FH. 1995. Novel neural network algorithms for improved eukaryotic promoter site recognition. The 7th International Genome Sequencing and Analysis Conference, Hilton Head Island, SC.
111. Stöver BC, Müller KF. 2010. TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11:7 http://dx.doi.org/10.1186/1471-2105-11-7. [PubMed]
112. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539 http://dx.doi.org/10.1038/msb.2011.75. [PubMed]
113. Ferretti JJ, McShan WM, Ajdic D, Savic DJ, Savic G, Lyon K, Primeaux C, Sezate S, Suvorov AN, Kenton S, Lai HS, Lin SP, Qian Y, Jia HG, Najar FZ, Ren Q, Zhu H, Song L, White J, Yuan X, Clifton SW, Roe BA, McLaughlin R. 2001. Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci U S A 98:4658–4663 http://dx.doi.org/10.1073/pnas.071559398. [PubMed]
114. Sumby P, Porcella SF, Madrigal AG, Barbian KD, Virtaneva K, Ricklefs SM, Sturdevant DE, Graham MR, Vuopio-Varkila J, Hoe NP, Musser JM. 2005. Evolutionary origin and emergence of a highly successful clone of serotype M1 group a Streptococcus involved multiple horizontal gene transfer events. J Infect Dis 192:771–782 http://dx.doi.org/10.1086/432514. [PubMed]
115. Miyoshi-Akiyama T, Watanabe S, Kirikae T. 2012. Complete genome sequence of Streptococcus pyogenes M1 476, isolated from a patient with streptococcal toxic shock syndrome. J Bacteriol 194:5466 http://dx.doi.org/10.1128/JB.01265-12. [PubMed]
116. Zheng PX, Chung KT, Chiang-Ni C, Wang SY, Tsai PJ, Chuang WJ, Lin YS, Liu CC, Wu JJ. 2013. Complete genome sequence of emm1Streptococcus pyogenes A20, a strain with an intact two-component system, CovRS, isolated from a patient with necrotizing fasciitis. Genome Announc 1:e00149-12 http://dx.doi.org/10.1128/genomeA.00149-12. [PubMed]
117. Beres SB, Richter EW, Nagiec MJ, Sumby P, Porcella SF, DeLeo FR, Musser JM. 2006. Molecular genetic anatomy of inter- and intraserotype variation in the human bacterial pathogen group A Streptococcus. Proc Natl Acad Sci U S A 103:7059–7064 http://dx.doi.org/10.1073/pnas.0510279103. [PubMed]
118. Beres SB, Sylva GL, Barbian KD, Lei B, Hoff JS, Mammarella ND, Liu MY, Smoot JC, Porcella SF, Parkins LD, Campbell DS, Smith TM, McCormick JK, Leung DY, Schlievert PM, Musser JM. 2002. Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc Natl Acad Sci U S A 99:10078–10083 http://dx.doi.org/10.1073/pnas.152298499. [PubMed]
119. Nakagawa I, Kurokawa K, Yamashita A, Nakata M, Tomiyasu Y, Okahashi N, Kawabata S, Yamazaki K, Shiba T, Yasunaga T, Hayashi H, Hattori M, Hamada S. 2003. Genome sequence of an M3 strain of Streptococcus pyogenes reveals a large-scale genomic rearrangement in invasive strains and new insights into phage evolution. Genome Res 13(6A) :1042–1055 http://dx.doi.org/10.1101/gr.1096703. [PubMed]
120. Holden MT, Scott A, Cherevach I, Chillingworth T, Churcher C, Cronin A, Dowd L, Feltwell T, Hamlin N, Holroyd S, Jagels K, Moule S, Mungall K, Quail MA, Price C, Rabbinowitsch E, Sharp S, Skelton J, Whitehead S, Barrell BG, Kehoe M, Parkhill J. 2007. Complete genome of acute rheumatic fever-associated serotype M5 Streptococcus pyogenes strain manfredo. J Bacteriol 189:1473–1477 http://dx.doi.org/10.1128/JB.01227-06. [PubMed]
121. Tse H, Bao JY, Davies MR, Maamary P, Tsoi HW, Tong AH, Ho TC, Lin CH, Gillen CM, Barnett TC, Chen JH, Lee M, Yam WC, Wong CK, Ong CL, Chan YW, Wu CW, Ng T, Lim WW, Tsang TH, Tse CW, Dougan G, Walker MJ, Lok S, Yuen KY. 2012. Molecular characterization of the 2011 Hong Kong scarlet fever outbreak. J Infect Dis 206:341–351 http://dx.doi.org/10.1093/infdis/jis362. [PubMed]
122. Port GC, Paluscio E, Caparon MG. 2013. Complete genome sequence of emm type 14 Streptococcus pyogenes strain HSC5. Genome Announc 1:e00612-13 http://dx.doi.org/10.1128/genomeA.00612-13. [PubMed]
123. Smoot JC, Barbian KD, Van Gompel JJ, Smoot LM, Chaussee MS, Sylva GL, Sturdevant DE, Ricklefs SM, Porcella SF, Parkins LD, Beres SB, Campbell DS, Smith TM, Zhang Q, Kapur V, Daly JA, Veasy LG, Musser JM. 2002. Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc Natl Acad Sci U S A 99:4668–4673 http://dx.doi.org/10.1073/pnas.062526099. [PubMed]
124. Green NM, Zhang S, Porcella SF, Nagiec MJ, Barbian KD, Beres SB, LeFebvre RB, Musser JM. 2005. Genome sequence of a serotype M28 strain of group a Streptococcus: potential new insights into puerperal sepsis and bacterial disease specificity. J Infect Dis 192:760–770 http://dx.doi.org/10.1086/430618. [PubMed]
125. McShan WM, Ferretti JJ, Karasawa T, Suvorov AN, Lin S, Qin B, Jia H, Kenton S, Najar F, Wu H, Scott J, Roe BA, Savic DJ. 2008. Genome sequence of a nephritogenic and highly transformable M49 strain of Streptococcus pyogenes. J Bacteriol 190:7773–7785 http://dx.doi.org/10.1128/JB.00672-08. [PubMed]
126. Bessen DE, Kumar N, Hall GS, Riley DR, Luo F, Lizano S, Ford CN, McShan WM, Nguyen SV, Dunning Hotopp JC, Tettelin H. 2011. Whole-genome association study on tissue tropism phenotypes in group A Streptococcus. J Bacteriol 193:6651–6663 http://dx.doi.org/10.1128/JB.05263-11. [PubMed]
127. Fittipaldi N, Beres SB, Olsen RJ, Kapur V, Shea PR, Watkins ME, Cantu CC, Laucirica DR, Jenkins L, Flores AR, Lovgren M, Ardanuy C, Liñares J, Low DE, Tyrrell GJ, Musser JM. 2012. Full-genome dissection of an epidemic of severe invasive disease caused by a hypervirulent, recently emerged clone of group A Streptococcus. Am J Pathol 180:1522–1534 http://dx.doi.org/10.1016/j.ajpath.2011.12.037. [PubMed]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.GPP3-0059-2018
2019-05-17
2019-08-21

Abstract:

The bacteriophages of (group A streptococcus) play a key role in population shaping, genetic transfer, and virulence of this bacterial pathogen. Lytic phages like A25 can alter population distributions through elimination of susceptible serotypes but also serve as key mediators for genetic transfer of virulence genes and antibiotic resistance via generalized transduction. The sequencing of multiple genomes has uncovered a large and diverse population of endogenous prophages that are vectors for toxins and other virulence factors and occupy multiple attachment sites in the bacterial genomes. Some of these sites for integration appear to have the potential to alter the bacterial phenotype through gene disruption. Remarkably, the phage-like chromosomal islands (SpyCI), which share many characteristics with endogenous prophages, have evolved to mediate a growth-dependent mutator phenotype while acting as global transcriptional regulators. The diverse population of prophages appears to share a large pool of genetic modules that promotes novel combinations that may help disseminate virulence factors to different subpopulations of . The study of the bacteriophages of this pathogen, both lytic and lysogenic, will continue to be an important endeavor for our understanding of how continues to be a significant cause of human disease.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

The genome of bacteriophage A25 reveals an escape from lysogeny. The 33,900-bp generalized transducing phage A25 is shown. The portion of the chromosome included in the shaded box is the high homology region that contains the remnant lysogeny module and other genes that A25 shares with prophages from genome strains MGAS10270 (M2), MGAS315 (M3), MGAS10570 (M4), and STAB902 (M4). Unlike these complete lysogens, A25 only has the operator and antirepressor from the lysogeny module (shown in expanded view below the map), apparently having lost the integrase and repressor for lysogeny some time in the past. This A25 expanded region is compared to the homologous region from genome prophage MGAS10270.2, which contains these elements as well as the upstream genes including the -like repressor. Promoters are shown as directional arrows. Introduction of the MGAS10270.2 repressor into an A25-sensitive strain results in its conversion to a high level of A25 resistance ( 32 ). The genome follows a typical modular arrangement, with the predicted function for A25 genes indicated by color: regulation, dark red; DNA replication, pink; encode endonucleases, dark blue; genome packaging, light blue; structural, green; and lysis, yellow. The figure is redrawn from McCullor et al. ( 32 ).

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Prophage attachment sites in the genome. The locations of the genome prophages are shown as a generalized chromosome backbone based on the SF370 M1 genome; each diamond represents a genome prophage identified at that site. The M type of the host for each prophage is indicated by the number within the diamond, and the circled letter is the identifier linked to Table 2 for gene identification, the integration target within that gene (5′ or 3′), and associated prophage virulence genes. The rRNA operons are indicated as green blocks, and the hypervariable regions containing virulence genes associated with or are hatched. The origin of replication is indicated (OriC).

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Integration of prophage SF370.1 may provide an alternative promoter for dipeptidase Spy0713. In strains lacking an integrated prophage at this site, the native promoter for dipeptidase Spy0713 is downstream of the uncharacterized gene Spy0654; the predicted sequence is shown above. Integration of phage SF370.1 into Spy0713 separates this gene from that of the native promoter, and a predicted promoter encoded by the prophage is now positioned in front of the dipeptidase ORF. This phage-encoded promoter is preceded also by a canonical CinA box ( 56 ), which is not part of the native promoter. Transcription of prophage virulence genes and is from the opposite strand and should not influence transcription of Spy0713. Promoter predictions were done using the online tool at http://www.fruitfly.org/seq_tools/promoter.html ( 110 ).

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

Morphology of streptococcal lysogenic phages. Prophages SF370.1 and T12 release typical virions following induction. The SF370.1 head is about 55 nm across and the tail is 168 nm in length in this micrograph. In this image, the tail fibers that contain hyaluronate lyase (hyaluronidase) are visible. The T12 capsid has similar dimensions, with the head being about 66 nm and the tail length 196 nm. Electron micrographs provided by W.M. McShan and S.V. Nguyen.

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5
FIGURE 5

The genetic structure of streptococcal prophages and phage-like chromosomal islands. The prophages found in the genomes of follow a typical lambdoid pattern in their organization with genetic modules for lysogeny, DNA replication, regulation, head morphogenesis, head-tail joining, tails and tail fibers, lysis, and virulence.

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 6
FIGURE 6

Phylogenetic relationships of prophages. An unrooted phylogenetic tree was created by DNA alignment of the genome prophages. Prophages MGAS10394.2, HKU16.1, NZ131.1, m46.1, and MGAS10394.4 were so dissimilar from the other prophages that each occupied an independent branch; consequently, for clarity, they are not shown on the tree. The alignment organized the remaining prophages into six major branches, and the encircled letter identifier by each prophage refers to its associated attachment site () described in Table 2 ; each identifier is colored to facilitate viewing. The groups are defined by shared modules for structural genes ( Table 3 ). The tree was created using the software packages Clustal-omega and TreeGraph 2 ( 111 , 112 ).

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 7
FIGURE 7

Shared genetic modules of the T12-related prophage family. The top line is the simplified genetic map of bacteriophage T12 colored by gene or genetic module for the integrase, repressor-antirepressor, DNA replication, DNA modification, DNA packaging, capsid proteins, lysis, and virulence (). Regions of unknown or uncertain function are colored gray. Beneath T12 is shown the genetic maps of the other genome prophages that share the extended region dedicated to packaging, capsid proteins, and lysis. DNA regions that are divergent from T12 are not shown. The figure illustrates that a structural gene module can be associated with divergent attachment sites or virulence genes. The alignment was derived from the phylogenetic tree presented in Fig. 5 .

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 8
FIGURE 8

Identity matrix of genome prophages grouped by M type. The identity matrix presents the Clustal-omega DNA alignment from Fig. 5 as the percentage identity between genome prophages, which are grouped by the M type of their host streptococcus. The numbers within each cell represent the identity rounded to the nearest whole number, and the cell colors show the range into which each identity falls by increasing percentages of 10.

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 9
FIGURE 9

SpyCIM1 regulation of the MMR operon through dynamic site-specific excision and integration. The MMR operon of groups the genes encoding DNA MMR ( and ), multidrug efflux (), Holliday-junction resolvase (), and base excision repair glycosylase (). The orientation of this chromosomal region is shown here from the lagging strand to emphasize the MMR operon transcription. During exponential phase, SpyCIM1 excises from the chromosome, circularizes, and replicates as an episome, restoring transcription of the entire DNA MMR operon (WT). Excision and mobilization occur early in logarithmic growth in response to as yet unknown cellular signals (insert; adapted from Scott et al. [ 53 ]). As logarithmic growth continues, SpyCIM1 reintegrates into at , and by the time the culture reaches the stationary phase, the integration process has completed, again blocking transcription of the MMR operon. WT, wild-type phenotype associated with unimpeded expression of the MMR operon. Reproduced from ( 52 ) under the Creative Commons Attribution License (CC-BY 4.0). The phylogenetic tree of the SpyCI DNA sequences is presented. The tree was created with TreeGraph 2 ( 111 ) using previously analyzed data ( 52 ).

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Generic image for table
TABLE 1

Assembled and annotated genomes of that are hosts to prophages

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
Generic image for table
TABLE 2

Prophages of and their integration sites and associated virulence genes

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018
Generic image for table
TABLE 3

prophages grouped by shared structural modules

Source: microbiolspec May 2019 vol. 7 no. 3 doi:10.1128/microbiolspec.GPP3-0059-2018

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error