Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-09T09:31:18.974Z Has data issue: false hasContentIssue false

3 - Phage-bacterium Co-evolution and Its Implication for Bacterial Pathogenesis

from PART II - Mobile Genetic Elements in Bacterial Evolution

Published online by Cambridge University Press:  16 September 2009

By
Harald Brüssow
Edited by
Michael Hensel  and
Herbert Schmidt
Michael Hensel
Affiliation:
Friedrich-Alexander-Universität Erlangen-Nürnberg, Germany
Herbert Schmidt
Affiliation:
Universität Hohenheim, Stuttgart
Get access

Summary

INTRODUCTION

Virulent phages such as Escherichia coli phage T4 are professional predators of bacteria. It is believed that this predator-prey relationship resulted in an evolutionary arms race in which bacteria developed anti-predation strategies against phages such as loss of receptor structures, restriction-modification systems, and abortive infection mechanisms. Temperate phages can lyse the bacterial host or alternatively integrate their DNA into the bacterial chromosome. As judged from the analysis of bacterial genomes, about a third of the bacteria might contain a prophage sequence. Temperate phages had thus a great impact on bacterial chromosome structure in general and the evolution of bacterial pathogenicity in special.

THEORETICAL FRAMEWORK FOR PHAGE-BACTERIUM INTERACTION

The peculiar life style of temperate phages makes them model systems to address a number of fundamental questions in evolutionary biology. The viral DNA undergoes different selective pressures when replicated during lytic infection cycles as compared to prophage DNA maintained in the bacterial genome during lysogeny. Darwinian considerations along with the selfish gene concept lead to interesting conjectures (Boyd and Brüssow, 2002; Brüssow and Hendrix, 2002; Brüssow et al., 2004; Canchaya et al., 2003, 2004; Lawrence et al., 2001). One could anticipate that the prophage decreases the fitness of its lysogenic host by at least two processes: first by the metabolic burden to replicate extra DNA and second by the lysis of the host after prophage induction. To compensate for these disadvantages one has to invoke the explanation that temperate phages encode functions that increase the fitness of the lysogen.

Type
Chapter
Information
Horizontal Gene Transfer in the Evolution of Pathogenesis , pp. 49 - 78
Publisher: Cambridge University Press
Print publication year: 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allison, G. E., Angeles, D., Tran-Dinh, N., and Verma, N. K. (2002). Complete genomic sequence of SfV, a serotype-converting temperate bacteriophage of Shigella flexneri. J Bacteriol, 184, 1974–87.CrossRefGoogle ScholarPubMed
Baba, T., Takeuchi, F., Kuroda, M., et al. (2002). Genome and virulence determinants of high virulence community-acquired MRSA. Lancet, 359, 1819–27.CrossRefGoogle ScholarPubMed
Barksdale, L., and Arden, S. B. (1974). Persisting bacteriophage infections, lysogeny, and phage conversions. Annu Rev Microbiol, 28, 265–99.CrossRefGoogle ScholarPubMed
Barondess, J. J., and Beckwith, J. (1990). A bacterial virulence determinant encoded by lysogenic coliphage lambda. Nature, 346, 871–4.CrossRefGoogle ScholarPubMed
Bensing, B. A., Siboo, I. R., and Sullam, P. M. (2001). Proteins PblA and PblB of Streptococcus mitis, which promote binding to human platelets, are encoded within a lysogenic bacteriophage. Infect Immun, 69, 6186–92.CrossRefGoogle ScholarPubMed
Beres, S. B., Sylva, G. L., Barbina, K. D., et al. (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 USA, 99, 10078–83.CrossRefGoogle ScholarPubMed
Bielaszewska, M., Fell, M., Greune, L., et al. (2004). Characterization of cytolethal distending toxin genes and expression in Shiga toxin-producing Escherichia coli strains of non-O157 serogroups. Infect Immun, 72, 1812–6.CrossRefGoogle ScholarPubMed
Bielaszewska, M., Sinha, B., Kuczius, T., and Karch, H. (2005). Cytolethal distending toxin from Shiga toxin-producing Escherichia coli O157 causes irreversible G2/M arrest, inhibition of proliferation, and death of human endothelial cells. Infect Immun, 73, 552–62.CrossRefGoogle ScholarPubMed
Bordenstein, S. R., Marshall, M. L., Fry, A. J., and Wernegreen, J. J. (2006). The tripartite associations between bacteriophage, Wolbachia, and arthropods. PLoS Biol, 2, e43.Google ScholarPubMed
Boyd, E. F., and Brüssow, H. (2002). Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol, 10, 521–9.CrossRefGoogle ScholarPubMed
Brinkmann, V., Reichard, U., Goosmann, C. B., et al. (2004). Neutrophil extracellular traps kill bacteria. Science, 303, 1532–5.CrossRefGoogle ScholarPubMed
Broudy, T. B., Pancholi, V., and Fischetti, V. A. (2001). Induction of lysogenic bacteriophage and phage-associated toxin from group a streptococci during coculture with human pharyngeal cells. Infect Immun, 69, 1440–3.CrossRefGoogle Scholar
Brüssow, H., and Hendrix, R. W. (2002). Phage genomics: small is beautiful. Cell, 108, 13–6.CrossRefGoogle ScholarPubMed
Brüssow, H., Canchaya, C., and Hardt, W.-D. (2004). Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev, 68, 560–602.CrossRefGoogle ScholarPubMed
Bushman, F. (2002). Lateral DNA transfer. New York: CSH Laboratory Press.Google Scholar
Campellone, K. G., Robbins, D., and Leong, J. M. (2004). EspFu is a translocated EHEC effector that interacts with Tir and N-WASP and promotes Nck-independent actin assembly. Dev Cell, 7, 217–28.CrossRefGoogle ScholarPubMed
Canchaya, C., Desiere, F., McShan, W. M., et al. (2002). Genome analysis of an inducible prophage and prophage remnants integrated in the Streptococcus pyogenes strain SF370. Virology, 302, 245–58.CrossRefGoogle ScholarPubMed
Canchaya, C., Proux, C., Fournous, G., Bruttin, A., and Brüssow, H. (2003). Prophage genomics. Microbiol Mol Biol Rev, 67, 238–76.CrossRefGoogle ScholarPubMed
Canchaya, C., Fournous, G., and Brüssow, H. (2004). The impact of prophages on bacterial chromosomes. Mol Microbiol, 53, 9–18.CrossRefGoogle ScholarPubMed
Casjens, S. (2003). Prophages and bacterial genomics: what have we learned so far?Mol Microbiol, 49, 277–300.CrossRefGoogle ScholarPubMed
Chen, Y., Golding, I., Sawai, S., Guo, L., and Cox, E. C. (2005). Population fitness and the regulation of Escherichia coli genes by bacterial viruses. PLoS Biol, 3, e229.CrossRefGoogle ScholarPubMed
Conway, J. F., Wikoff, W. R., Cheng, N., et al. (2001). Virus maturation involving large subunit rotations and local refolding. Science, 292, 744–8.CrossRefGoogle ScholarPubMed
Creuzburg, K., Recktenwald, J., Kuhle, V., et al. (2005). The Shiga toxin 1-converting bacteriophage BP-4795 encodes an NleA-like type III effector protein. J Bacteriol 187, 8494–8.CrossRefGoogle ScholarPubMed
Dahan, S., Wiles, S., Ragione, R. M., et al. (2005). EspJ is a prophage-carried type III effector protein of attaching and effacing pathogen that modulates infection dynamics. Infect Immun, 73, 679–86.CrossRefGoogle ScholarPubMed
Dozois, C. M., Daigle, F., and Curtiss III, R. (2003). Identification of pathogen-specific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc Natl Acad Sci USA, 100, 247–52.CrossRefGoogle ScholarPubMed
Edlin, G., Lin, L., and Kudnram, R. (1975). Lambda lysogens of E. coli reproduce more rapidly than non-lysogens. Nature, 255, 735–7.CrossRefGoogle ScholarPubMed
Ferretti, J. J., McShan, W. M., Ajdic, D., et al. (2001). Complete genome sequence of an M1 strain of Streptococcus pyogenes. Proc Natl Acad Sci USA, 98, 4658–63.CrossRefGoogle ScholarPubMed
Freeman, V. J. (1951). Studies on the virulence of bacteriophage infected strains of Corynebacterium diphtheriae. J Bacteriol, 61, 675–88.Google ScholarPubMed
Groth, A. C., Olivares, E. C., Thyagarajan, B., and Calos, M. P. (2000). A phage integrase directs efficient site-specific integration in human cells. Proc Natl Acad Sci USA, 97, 5995–6000.CrossRefGoogle ScholarPubMed
Gruenheid, S., Sekirov, I., Thomas, N. A., et al. (2004). Identification and characterization of NleA, a non-LEE-encoded type III translocated virulence factor of enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol, 51, 1233–49.CrossRefGoogle ScholarPubMed
Huber, K. E., and Waldor, M. K. (2002). Filamentous phage integration requires the host recombinases XerC and XerD. Nature, 417, 656–9.CrossRefGoogle ScholarPubMed
Hurst, M. R., Glare, T. R., and Jackson, T. A. (2004). Cloning Serratia entomophila antifeeding genes – a putative defective prophage active against the grass grub Costelytra zealandica. J Bacteriol, 186, 5116–28.CrossRefGoogle ScholarPubMed
Jiang, S. C., and Paul, J. H. (1998). Gene transfer by transduction in the marine environment. Appl Environ Microbiol, 64, 2780–7.Google ScholarPubMed
Jin, T., Bokarewa, M., Foster, T., et al. (2004). Staphylococcus aureus resists human defensins by production of staphylokinase, a novel bacterial evasion mechanism. J Immunol, 172, 1169–76.CrossRefGoogle ScholarPubMed
Kanamaru, S., Leiman, P. G., Kostyuchenko, V. A., et al. (2002). Structure of the cell-puncturing device of bacteriophage T4. Nature, 415, 553–7.CrossRefGoogle ScholarPubMed
Kuroda, M., Ohta, T., Uchiyama, I., et al. (2001). Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet, 357, 1225–40.CrossRefGoogle Scholar
Lang, A. S., and Beatty, J. T. (2000). Genetic analysis of a bacterial genetic exchange element: the gene transfer agent of Rhodobacter capsulatus. Proc Natl Acad Sci USA, 97, 859–64.CrossRefGoogle ScholarPubMed
Lara-Tejero, M., and Galan, J. E. (2000). A bacterial toxin that controls cell cycle progression as a deoxyribonuclease I-like protein. Science, 290, 354–7.CrossRefGoogle ScholarPubMed
Lara-Tejero, M., and Galan, J. E. (2002). Cytolethal distending toxin: limited damage as a strategy to modulate cellular functions. Trends Microbiol, 10, 147–52.CrossRefGoogle ScholarPubMed
Lawrence, J. G. (1997). Selfish operons and speciation by gene transfer. Trends Microbiol, 5, 355–9.CrossRefGoogle ScholarPubMed
Lawrence, J. G., and Ochman, H. (1997). Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol, 44, 383–97.CrossRefGoogle Scholar
Lawrence, J. G., and Ochman, H. (1998). Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA, 95, 9413–7.CrossRefGoogle ScholarPubMed
Lawrence, J. G., Hendrix, R. W., and Casjens, S. (2001). Where are the pseudogenes in bacterial genomes?Trends Microbiol, 9, 535–40.CrossRefGoogle ScholarPubMed
Makino, K., Yokoyama, K., Kubota, Y., et al. (1999). Complete nucleotide sequence of the prophage VT2-Sakai carrying the verotoxin 2 genes of the enterohemorrhagic Escherichia coli O157:H7 derived from the Sakai outbreak. Genes Genet Syst, 74, 227–39.CrossRefGoogle ScholarPubMed
Marches, O., Ledger, T. L., Boury, M., et al. (2003). Enteropathogenic and eneterohaemorrhagic Escherichia coli deliver a novel effector called Cif, which blocks cell cycle G2/M transition. Mol Microbiol, 50, 1553–67.CrossRefGoogle ScholarPubMed
Matson, E. G., Thompson, M. G., Humphrey, S. B., Zuerner, R. L., and Stanton, T. E. (2005). Identification of genes of VSH-1, a prophage-like gene transfer agent of Brachyspira hyodysenteriae. J Bacteriol, 187, 5885–92.CrossRefGoogle ScholarPubMed
Matz, C., and Kjelleberg, S. (2005). Off the hook – how bacteria survive protozoan grazing. Trends Microbiol, 13, 302–7.CrossRefGoogle ScholarPubMed
Matz, C., Deines, P., Boenigk, J., et al. (2004). Impact of violacein-producing bacteria on survival and feeding of bacteriovorous nano. Appl Environ Microbiol, 70, 1593–9.CrossRefGoogle Scholar
McLeod, S. M., Kimsey, H. H., Davies, B. M., and Waldor, M. K. (2005). CTXΦ and Vibrio cholerae: exploring a newly recognized type of phage-host cell relationship. Mol Microbiol, 57, 347–56.CrossRefGoogle ScholarPubMed
Mirold, S., Rabsch, W., Rohde, M., et al. (1999). Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc Natl Acad Sci USA, 96, 9845–50.CrossRefGoogle ScholarPubMed
Molineux, I. J. (2001). No syringes please, ejection of phage T7 DNA from the virion is enzyme driven. Mol Microbiol, 40, 1–8.CrossRefGoogle ScholarPubMed
Moran, N. A., Degnan, P. H., Santos, S. R., Dunbar, H. E., and Ochman, H. (2005). The players in a mutualistic symbiosis: insects, bacteria, viruses, and virulence genes. Proc Natl Acad Sci USA, 102, 16919–26.CrossRefGoogle Scholar
Nakagawa, I., Kurokawa, K., Yamashita, A., et al. (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, 1042–55.CrossRefGoogle ScholarPubMed
Nakayama, K., Kanaya, S., Ohnishi, M., Terawaki, Y., and Hayashi, T. (1999). The complete nucleotide sequence of ΦCTX, a cytotoxin-converting phage of Pseudomonas aeruginosa: implications for phage evolution and horizontal gene transfer via bacteriophages. Mol Microbiol, 31, 399–419.CrossRefGoogle Scholar
Nakayama, K., Takashima, K., Ishihara, H., et al. (2000). The R-type pyocin of Pseudomonas aeruginosa is related to P2 phage, and the F-type is related to lambda phage. Mol Microbiol, 38, 213–31.CrossRefGoogle ScholarPubMed
Ohnishi, M., Kurokawa, K., and Hayashi, T. (2001). Diversification of Escherichia coli genomes: are bacteriophages the major contributors? Trends Microbiol, 9, 481–5.CrossRefGoogle ScholarPubMed
Oliver, K. M., Russell, J. A., Moran, N. A., and Hunter, M. S. (2003). Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA, 100, 1803–7.CrossRefGoogle ScholarPubMed
Oliver, K. M., Moran, N. A., and Hunter, M. S. (2005). Variation in resistance to parasitism in aphids is due to symbionts not to host genotype. Proc Natl Acad Sci USA, 102, 12795–800.CrossRefGoogle ScholarPubMed
Perna, N. T., Plunkett, III, G., Burland, V., et al. (2001). Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature, 409, 529–33.CrossRef
Postma, B., Poppelier, M. J.Galen, J. C., et al. (2004). Chemotaxis inhibitory protein of Staphylococcus aureus binds specifically to the C5a and formylated peptide receptor. J Immunol, 172, 6994–7001.CrossRefGoogle ScholarPubMed
Rahimpour, R., Mitchell, G., Khandaker, M. H., et al. (1999). Bacterial superantigens induce down-modulation of CC chemokine responsiveness in human monocytes via an alternative chemokine ligand-independent mechanism. J Immunol, 162, 2299–307.Google ScholarPubMed
Robinson, C. M., Sinclair, J. F., Smith, M. J., and O'Brien, A. D. (2006). Shiga toxin of enterohemorrhagic Escherichia coli type O157:H7 promotes intestinal colonization. Proc Natl Acad Sci USA, 103, 9667–72.CrossRefGoogle ScholarPubMed
Rooijakkers, S. H., Ruyken, M., Roos, A., et al. (2005). Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat Immunol, 6, 920–7.CrossRefGoogle ScholarPubMed
Ruzin, A., Lindsay, J., and Novick, R. P. (2001). Molecular genetics of SaPI1-a mobile pathogenicity island in Staphylococcus aureus. Mol Microbiol, 41, 365–77.CrossRefGoogle ScholarPubMed
Sakaguchi, Y., Hayashi, T., Kurokawa, K., et al. (2005). The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny. Proc Natl Acad Sci USA 102: 17472–7.CrossRefGoogle ScholarPubMed
Saxena, S. K., O'Brien, A. D., and Ackerman, E. J. (1989). Shiga toxin, Shiga-like toxin II variant, and ricin are all single-site RNA N-glycosidases of 28 S RNA when microinjected into Xenopus oocytes. J Biol Chem, 264, 596–601.Google ScholarPubMed
Schlumberger, M. C., and Hardt, W.-D. (2006). Salmonella type III secretion effectors: pulling the host cell's strings. Curr Opin Microbiol, 9, 46–54.CrossRefGoogle ScholarPubMed
Sinkins, S. P., Walker, T., Lynd, A. R., et al. (2005). Wolbachia variability and host effects on crossing type in Culex mosquitoes. Nature, 436, 257–60.CrossRefGoogle ScholarPubMed
Smoot, L. M., Smoot, J. C., Graham, M. R., et al. (2001). Global differential gene expression in response to growth temperature alteration in group A Streptococcus. Proc Natl Acad Sci USA, 98, 10416–21.CrossRefGoogle ScholarPubMed
Smoot, J. C., Barbian, K. D., Gompel, J. J., et al. (2002). Genome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc Natl Acad Sci USA, 99, 4668–73.CrossRefGoogle ScholarPubMed
Strauch, E., Kaspar, H., Schaudinn, C., et al. (2001). Characterization of enterocoloticin, a phage tail-like bacteriocin, and its effect on pathogenic Yersinia enterocolitica strains. Appl Environ Microbiol, 67, 5634–42.CrossRefGoogle ScholarPubMed
Sumby, P., Barbian, K. D., Gardner, D. J., et al. (2005). Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc Natl Acad Sci USA, 102, 1679–84.CrossRefGoogle ScholarPubMed
Summer, E. J., Gonzales, C. F., Carlisle, T., et al. (2004). Burkholderia cenocepacia phage BcepMu and a family of Mu-like phages encoding potential pathogenesis factors. J Mol Biol, 340, 49–65.CrossRef
Tobe, T., Beatson, S. A., Taniguchi, H., et al. (2006). An extensive repertoire of type III secretion effectors in Escherichia coli O157 and the role of lambdoid phages in their dissemination. Proc Natl Acad Sci USA, 103, 14941–46.CrossRefGoogle ScholarPubMed
Sluys, M. A., Oliveira, M. C., Monteiro-Vitorello, C. B., et al. (2003). Comparative analyses of the complete genome sequences of Pierce's disease and citrus variegated chlorosis strains of Xylella fastidiosa. J Bacteriol, 185, 1018–26.CrossRefGoogle ScholarPubMed
Wamel, W. J., Rooijakkers, S. H., Ruyken, M., Kessel, K. P., and Strijp, J. A. (2006). The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J Bacteriol, 188, 1310–5.CrossRefGoogle ScholarPubMed
Wagner, P. L., Acheson, D. W., and Waldor, M. K. (2001a). Human neutrophils and their products induce Shiga toxin production by enterohemorrhagic Escherichia coli. Infect Immun, 69, 1934–7.CrossRefGoogle ScholarPubMed
Wagner, P. L., Neely, M. N., Zhang, X.et al. (2001b). Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J Bacteriol, 183, 2081–5.CrossRefGoogle ScholarPubMed
Waldor, M. K., and Friedman, D. I. (2005). Phage regulatory circuits and virulence gene expression. Curr Opin Microbiol, 8, 459–65.CrossRefGoogle ScholarPubMed
Waldor, M. K., and Mekalanos, J. J. (1996). Lysogenic conversion by a filamentous phage encoding cholera toxin. Science, 272, 1910–4.CrossRefGoogle ScholarPubMed
Wick, L. M., Qi, W., Lacher, D. W., and Whittam, T. S. (2005). Evolution of genomic content in the stepwise emergence of Escherichia coli O157:H7. J Bacteriol, 187, 1783–91.CrossRefGoogle ScholarPubMed
Wildschutte, H., Wolfe, D. M., Tamewitz, A., and Lawrence, J. G. (2004). Protozoan predation, diversifying selection, and the evolution of antigenic diversity in Salmonella. Proc Natl Acad Sci USA, 101, 10644–9.CrossRefGoogle ScholarPubMed
Williamson, S. J., Houchin, L. A., McDaniel, L., and Paul, J. H. (2002). Seasonal variation in lysogeny as depicted by prophage induction in Tampa Bay, Florida. Appl Environ Microbiol, 68, 4307–14.CrossRefGoogle ScholarPubMed
Wommack, K. E., and Colwell, R. R. (2000). Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev, 64, 69–114.CrossRefGoogle ScholarPubMed
Zhang, Z., Greene, B., Thuman-Commike, P. A., et al. (2000). Visualization of the maturation transition in bacteriophage P22 by electron cryomicroscopy. J Mol Biol, 297, 615–26.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×