Importance of Prophages to Evolution and Virulence of Bacterial Pathogens

Overview

Journal Virulence

Specialty Microbiology

Date 2013 Apr 25

PMID 23611873

Citations 253

Authors

Louis-Charles Fortier

Ognjen Sekulovic

Affiliations

Soon will be listed here.

Abstract

Bacteriophages, or simply phages, are viruses infecting bacteria. With an estimated 10 ( 31) particles in the biosphere, phages outnumber bacteria by a factor of at least 10 and not surprisingly, they influence the evolution of most bacterial species, sometimes in unexpected ways. "Temperate" phages have the ability to integrate into the chromosome of their host upon infection, where they can reside as "quiescent" prophages until conditions favor their reactivation. Lysogenic conversion resulting from the integration of prophages encoding powerful toxins is probably the most determinant contribution of prophages to the evolution of pathogenic bacteria. We currently grasp only a small fraction of the total phage diversity. Phage biologists keep unraveling novel mechanisms developed by phages to parasitize their host. The purpose of this review is to give an overview of some of the various ways by which prophages change the lifestyle and boost virulence of some of the most dangerous bacterial pathogens.

Citing Articles

Global phylogenomic analysis of reveals genomic and prophage diversity in multidrug-resistant lineages.

Grist L, Brown A, Fitzpatrick N, Mariano G, La Ragione R, Van Vliet A Microb Genom. 2025; 11(3).

PMID: 40042988 PMC: 11883136. DOI: 10.1099/mgen.0.001369.

Comparative Genomic Analysis of 66 Bacteriophages Infecting Morganella morganii Strains.

Mahamud S, Oishy S, Roy S, Pal K, Rubaiyat R, Ansary M Curr Microbiol. 2025; 82(4):137.

PMID: 39955358 DOI: 10.1007/s00284-025-04110-7.

Recent Discovery of Diverse Prophages Located in Genomes of spp. and Their Implications for Bacterial Pathogenicity, Environmental Fitness, Genome Evolution, Food Safety, and Public Health.

Ou Y, Yan J, Wang Y, Chen L Foods. 2025; 14(3).

PMID: 39941999 PMC: 11817191. DOI: 10.3390/foods14030403.

Urinary bacteriophage cooperation with bacterial pathogens during human urinary tract infections supports lysogenic phage therapy.

Almosuli M, Kirtava A, Chkhotua A, Tsveniashvili L, Chanishvili N, Irfan S Commun Biol. 2025; 8(1):175.

PMID: 39905205 PMC: 11794546. DOI: 10.1038/s42003-025-07598-8.

Shotgun metagenomic sequencing reveals the influence of artisanal dairy environments on the microbiomes, quality, and safety of Idiazabal, a raw ewe milk PDO cheese.

Santamarina-Garcia G, Yap M, Crispie F, Amores G, Lordan C, Virto M Microbiome. 2024; 12(1):262.

PMID: 39707557 PMC: 11662609. DOI: 10.1186/s40168-024-01980-0.

References

Juhala R, Ford M, Duda R, Youlton A, Hatfull G, Hendrix R . Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol. 2000; 299(1):27-51. DOI: 10.1006/jmbi.2000.3729. View

Rhoads D, Wolcott R, Kuskowski M, Wolcott B, Ward L, Sulakvelidze A . Bacteriophage therapy of venous leg ulcers in humans: results of a phase I safety trial. J Wound Care. 2009; 18(6):237-8, 240-3. DOI: 10.12968/jowc.2009.18.6.42801. View

Matamouros S, England P, Dupuy B . Clostridium difficile toxin expression is inhibited by the novel regulator TcdC. Mol Microbiol. 2007; 64(5):1274-88. DOI: 10.1111/j.1365-2958.2007.05739.x. View

Levin B, Bull J . Population and evolutionary dynamics of phage therapy. Nat Rev Microbiol. 2004; 2(2):166-73. DOI: 10.1038/nrmicro822. View

Kim K, Born Y, Lurz R, Eichenseher F, Zimmer M, Loessner M . Inducible Clostridium perfringens bacteriophages ΦS9 and ΦS63: Different genome structures and a fully functional sigK intervening element. Bacteriophage. 2012; 2(2):89-97. PMC: 3442830. DOI: 10.4161/bact.21363. View

Chen J, Novick R . Phage-mediated intergeneric transfer of toxin genes. Science. 2009; 323(5910):139-41. DOI: 10.1126/science.1164783. View

Qin Z, Ou Y, Yang L, Zhu Y, Tolker-Nielsen T, Molin S . Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology (Reading). 2007; 153(Pt 7):2083-2092. DOI: 10.1099/mic.0.2007/006031-0. View

Capparelli R, Parlato M, Borriello G, Salvatore P, Iannelli D . Experimental phage therapy against Staphylococcus aureus in mice. Antimicrob Agents Chemother. 2007; 51(8):2765-73. PMC: 1932491. DOI: 10.1128/AAC.01513-06. View

Cleary P, LaPenta D, Vessela R, Lam H, Cue D . A globally disseminated M1 subclone of group A streptococci differs from other subclones by 70 kilobases of prophage DNA and capacity for high-frequency intracellular invasion. Infect Immun. 1998; 66(11):5592-7. PMC: 108706. DOI: 10.1128/IAI.66.11.5592-5597.1998. View

10.

Hodak H, Galan J . A Salmonella Typhi homologue of bacteriophage muramidases controls typhoid toxin secretion. EMBO Rep. 2012; 14(1):95-102. PMC: 3537140. DOI: 10.1038/embor.2012.186. View

11.

Moineau S, Pandian S, Klaenhammer T . Evolution of a Lytic Bacteriophage via DNA Acquisition from the Lactococcus lactis Chromosome. Appl Environ Microbiol. 1994; 60(6):1832-41. PMC: 201570. DOI: 10.1128/aem.60.6.1832-1841.1994. View

12.

Debarbieux L, Leduc D, Maura D, Morello E, Criscuolo A, Grossi O . Bacteriophages can treat and prevent Pseudomonas aeruginosa lung infections. J Infect Dis. 2010; 201(7):1096-104. DOI: 10.1086/651135. View

13.

Muller A, Kaiser P, Dittmar K, Weber T, Haueter S, Endt K . Salmonella gut invasion involves TTSS-2-dependent epithelial traversal, basolateral exit, and uptake by epithelium-sampling lamina propria phagocytes. Cell Host Microbe. 2012; 11(1):19-32. DOI: 10.1016/j.chom.2011.11.013. View

14.

Ingrey K, Ren J, Prescott J . A fluoroquinolone induces a novel mitogen-encoding bacteriophage in Streptococcus canis. Infect Immun. 2003; 71(6):3028-33. PMC: 155711. DOI: 10.1128/IAI.71.6.3028-3033.2003. View

15.

Kaneko J, Kimura T, Narita S, Tomita T, Kamio Y . Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage phiPVL carrying Panton-Valentine leukocidin genes. Gene. 1998; 215(1):57-67. DOI: 10.1016/s0378-1119(98)00278-9. View

16.

Seper A, Fengler V, Roier S, Wolinski H, Kohlwein S, Bishop A . Extracellular nucleases and extracellular DNA play important roles in Vibrio cholerae biofilm formation. Mol Microbiol. 2011; 82(4):1015-37. PMC: 3212620. DOI: 10.1111/j.1365-2958.2011.07867.x. View

17.

Postollec F, Mathot A, Bernard M, Divanach M, Pavan S, Sohier D . Tracking spore-forming bacteria in food: from natural biodiversity to selection by processes. Int J Food Microbiol. 2012; 158(1):1-8. DOI: 10.1016/j.ijfoodmicro.2012.03.004. View

18.

Neely M, Friedman D . Functional and genetic analysis of regulatory regions of coliphage H-19B: location of shiga-like toxin and lysis genes suggest a role for phage functions in toxin release. Mol Microbiol. 1998; 28(6):1255-67. DOI: 10.1046/j.1365-2958.1998.00890.x. View

19.

Eklund M, Poysky F, Reed S, Smith C . Bacteriophage and the toxigenicity of Clostridium botulinum type C. Science. 1971; 172(3982):480-2. DOI: 10.1126/science.172.3982.480. View

20.

Lee C, Iandolo J . Lysogenic conversion of staphylococcal lipase is caused by insertion of the bacteriophage L54a genome into the lipase structural gene. J Bacteriol. 1986; 166(2):385-91. PMC: 214616. DOI: 10.1128/jb.166.2.385-391.1986. View