Prophages and satellite prophages are widespread in Streptococcus and may play a role in pneumococcal pathogenesis


  • 1.

    Krzyściak, W., Pluskwa, K., Jurczak, A. & Kościelniak, D. The pathogenicity of the Streptococcus genus. Eur. J. Clin. Microbiol. Infect. Dis. 32, 1361–1376 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 2.

    O’Brien, K.Hib and Pneumococcal Global Burden of Disease Study Team et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374, 893–902 (2009).

    Article 

    Google Scholar
     

  • 3.

    Carapetis, J., Steer, A., Mulholland, E. & Weber, M. The global burden of group A streptococcal diseases. Lancet Infect. Dis. 5, 685–694 (2005).

    PubMed 
    Article 

    Google Scholar
     

  • 4.

    Vornhagen, J., Adams Waldorf, K. & Rajagopal, L. Perinatal group B Streptococcal infections: virulence factors, immunity, and prevention strategies. Trends Microbiol. 25, 919–931 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 5.

    Boyd, E. & Brüssow, H. Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol. 10, 521–529 (2002).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 6.

    Casjens, S. Prophages and bacterial genomics: what have we learned so far? Mol. Microbiol. 49, 277–300 (2003).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 7.

    Bensing, B., Siboo, I. & Sullam, P. Proteins PblA and PblB of Streptococcus mitis, which promote binding to human platelets, are encoded within a lysogenic bacteriophage. Infect. Immun. 69, 6186–6192 (2001).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 8.

    Vaca Pacheco, S., Garcıća González, O. & Paniagua Contreras, G. The lom gene of bacteriophage λ is involved in Escherichia coli K12 adhesion to human buccal epithelial cells. FEMS Microbiol. Lett. 156, 129–132 (2006).

    Article 

    Google Scholar
     

  • 9.

    Mirold, S. et al. Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc. Natl. Acad. Sci. USA 96, 9845–9850 (1999).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 10.

    Bulgin, R. et al. Bacterial guanine nucleotide exchange factors SopE-like and WxxxE effectors. Infect. Immun. 78, 1417–1425 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 11.

    Figueroa-Bossi, N., Uzzau, S., Maloriol, D. & Bossi, L. Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. Mol. Microbiol. 39, 260–272 (2001).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 12.

    Menouni, R., Hutinet, G., Petit, M. & Ansaldi, M. Bacterial genome remodeling through bacteriophage recombination. FEMS Microbiol. Lett. 362, 1–10 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 13.

    Feiner, R. et al. A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat. Rev. Microbiol. 13, 641–650 (2015).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 14.

    Koskella, B. & Brockhurst, M. Bacteria–phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev. 38, 916–931 (2014).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 15.

    Varon, M. & Levisohn, R. Three-membered parasitic system: a bacteriophage, Bdellovibrio bacteriovorus, and Escherichia coli. J. Virol. 9, 519–525 (1972).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 16.

    Belfort, M. Bacteriophage introns: parasites within parasites? Trends Genet. 5, 209–213 (1989).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  • 17.

    Novick, R. Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid 49, 93–105 (2003).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  • 18.

    Novick, R., Christie, G. & Penadés, J. The phage-related chromosomal islands of Gram-positive bacteria. Nat. Rev. Microbiol. 8, 541–551 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 19.

    Penadés, J. & Christie, G. The phage-inducible chromosomal islands: a family of highly evolved molecular parasites. Ann. Rev. Virol. 2, 181–201 (2015).

    Article 
    CAS 

    Google Scholar
     

  • 20.

    Frígols, B. et al. Virus satellites drive viral evolution and ecology. PLOS Genet. 11, e1005609 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 21.

    O’Neill, A., Larsen, A., Skov, R., Henriksen, A. & Chopra, I. Characterization of the epidemic European fusidic acid-resistant impetigo clone of Staphylococcus aureus. J. Clin. Microbiol. 45, 1505–1510 (2007).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 22.

    Scott J., Nguyen S., King C., Hendrickson C., McShan W. Phage-Like Streptococcus pyogenes chromosomal islands (SpyCI) and mutator phenotypes: control by growth state and rescue by a SpyCI-encoded promoter. Front. Microbiol. 3, 317 (2012).

  • 23.

    Seed, K., Lazinski, D., Calderwood, S. & Camilli, A. A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494, 489–491 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 24.

    Lindsay, J., Ruzin, A., Ross, H., Kurepina, N. & Novick, R. The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol. Microbiol. 29, 527–543 (1998).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  • 25.

    Martínez-Rubio, R. et al. Phage-inducible islands in the Gram-positive cocci. ISME J. 11, 1029–1042 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 26.

    Brueggemann A., et al. Pneumococcal prophages are diverse, but not without structure or history. Sci. Rep. 7, 42946 (2017).

  • 27.

    Romero, P., García, E. & Mitchell, T. J. Development of a prophage typing system and analysis of prophage carriage in Streptococcus pneumoniae. Appl. Environ. Microbiol. 75, 1642–1649 (2009).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 28.

    Ramirez, M., Severina, E. & Tomasz, A. A high incidence of prophage carriage among natural isolates of Streptococcus pneumoniae. J. Bacteriol. 181, 3618–3625 (1999).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 29.

    Beres, S. et al. Genome sequence of a serotype M3 strain of group A Streptococcus: phage-encoded toxins, the high-virulence phenotype, and clone emergence. Proc. Nat. Acad. Sci. USA 99, 10078–10083 (2002).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  • 30.

    McShan W. M., Nguyen S. V. The bacteriophages of Streptococcus pyogenes. In: Ferretti J. J., Stevens D. L., Fischetti V. A., editors. Streptococcus pyogenes: Basic Biology to Clinical Manifestations. University of Oklahoma Health Sciences Center (2016). Available from: https://www.ncbi.nlm.nih.gov/books/NBK333409/.

  • 31.

    van der Mee-Marquet, N. et al. Analysis of the prophages carried by human infecting isolates provides new insight into the evolution of group B Streptococcus species. Clin. Microbiol. Infect. 24, 514–521 (2018).

    PubMed 
    Article 
    CAS 

    Google Scholar
     

  • 32.

    Canchaya, C. et al. Genome analysis of an inducible prophage and prophage remnants integrated in the Streptococcus pyogenes strain SF370. Virology 302, 245–258 (2002).

    CAS 
    Article 

    Google Scholar
     

  • 33.

    Davies, E., Winstanley, C., Fothergill, J. & James, C. The role of temperate bacteriophages in bacterial infection. FEMS Microbiol. Lett. 363, fnw015 (2016).

    PubMed 
    Article 
    CAS 

    Google Scholar
     

  • 34.

    Bobay, L., Touchon, M. & Rocha, E. Pervasive domestication of defective prophages by bacteria. Proc. Nat. Acad. Sci. USA 111, 12127–12132 (2014).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 35.

    Spratt, B. G. & Maiden, M. C. Bacterial population genetics, evolution and epidemiology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354, 701–710 (1999).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 36.

    Feil, E. J., Smith, J. M., Enright, M. C. & Spratt, B. G. Estimating recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. Genetics 154, 1439–1450 (2000).

    CAS 
    PubMed 

    Google Scholar
     

  • 37.

    Ackermann, H. et al. Guidelines for bacteriophage characterization. Adv. Virus Res. 23, 1–24 (1978).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 38.

    Ji, X. et al. A novel virulence-associated protein, VapE, in Streptococcus suis serotype 2. Mol. Med. Rep. 13, 2871–2877 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 39.

    Blanchette, K. A. et al. Neuraminidase A-exposed galactose promotes Streptococcus pneumoniae biofilm formation during colonization. Infect. Immun. 84, 2922–2932 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 40.

    Ross, A., Ward, S. & Hyman, P. More is better: selecting for broad host range bacteriophages. Front. Microbiol. 7, 352 (2016).

    Article 

    Google Scholar
     

  • 41.

    Gilley, R. P. & Orihuela, C. J. Pneumococci in biofilms are non-invasive: implications on nasopharyngeal colonization. Front. Cell Infect. Microbiol. 4, 163 (2014).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 42.

    Lima-Mendez, G., Van Helden, J., Toussaint, A. & Leplae, R. Prophinder: a computational tool for prophage prediction in prokaryotic genomes. Bioinformatics 24, 863–865 (2008).

    CAS 
    Article 

    Google Scholar
     

  • 43.

    Zhou, Y., Liang, Y., Lynch, K., Dennis, J. & Wishart, D. PHAST: a fast phage search tool. Nucl. Acids Res. 39, W347–W352 (2011).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 44.

    Crispim J., et al Screening and characterization of prophages in Desulfovibrio genomes. Sci. Rep. 8. 9273 (2018).

  • 45.

    Langille, M., Hsiao, W. & Brinkman, F. Detecting genomic islands using bioinformatics approaches. Nat. Rev. Microbiol. 8, 373–382 (2010).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 46.

    Kurioka, A. et al. Diverse Streptococcus pneumoniae strains drive a MAIT cell response through MR1-dependent and cytokine-driven pathways. J. Infect. Dis. 217, 988–999 (2018).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 47.

    Jolley, K. A. et al. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 158, 1005–1015 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 48.

    Francisco, A. P. et al. PHYLOViZ: phylogenetic inference and data visualization for sequence based typing methods. BMC Bioinformatics 13, 87 (2012).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 49.

    Jolley, K. A. & Maiden, M. C. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11, 595 (2010).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 50.

    Thompson, J. D., Higgins, D. G. & GibsonTJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 51.

    Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2–approximately maximum-likelihood trees for large alignments. PLOS ONE 5, e9490 (2010).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 52.

    Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659 (2006).

    CAS 
    Article 

    Google Scholar
     

  • 53.

    Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 54.

    Page, A. J. et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31, 3691–3693 (2015).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • 55.

    Huerta-Cepas, J. et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol. Biol. Evol. 34, 2115–2122 (2017).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 56.

    Huerta-Cepas, J. et al. eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res. 44, D286–D293 (2016).

    CAS 
    PubMed 
    Article 

    Google Scholar
     

  • 57.

    Didelot, X. & Wilson, D. J. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLOS Comput Biol. 11, e1004041 (2015).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 58.

    Letunic, I. & Bork, P. Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 39, W475–W478 (2011).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 59.

    Kjos, M. et al. Bright fluorescent Streptococcus pneumoniae for live-cell imaging of host-pathogen interactions. J. Bacteriol. 197, 807–818 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 60.

    Khandavilli, S. et al. Maturation of Streptococcus pneumoniae lipoproteins by a type II signal peptidase is required for ABC transporter function and full virulence. Mol. Microbiol. 67, 541–557 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  • 61.

    Basavanna, S. et al. The effects of methionine acquisition and synthesis on Streptococcus pneumoniae growth and virulence. PLOS ONE 8, e49638 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 62.

    Heckman, K. L. & Pease, L. R. Gene splicing and mutagenesis by PCR-driven overlap extension. Nat. Protoc. 2, 924–932 (2007).

    CAS 
    Article 

    Google Scholar
     

  • 63.

    Håvarstein, L. S., Coomaraswamy, G. & Morrison, D. A. An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc. Natl. Acad. Sci. USA 92, 11140–11144 (1995).

    ADS 
    Article 

    Google Scholar
     

  • 64.

    Lau, G. W. et al. A functional genomic analysis of type 3 Streptococcus pneumoniae virulence. Mol. Microbiol. 40, 555–571 (2001).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  • 65.

    Ramos-Sevillano, E. et al. Pleiotropic effects of cell wall amidase LytA on Streptococcus pneumoniae sensitivity to the host immune response. Infect. Immun. 83, 591–603 (2015).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar
     

  • 66.

    Yuste, J., Botto, M., Paton, J. C., Holden, D. W. & Brown, J. S. Additive inhibition of complement deposition by pneumolysin and PspA facilitates Streptococcus pneumoniae septicemia. J. Immunol. 175, 1813–1819 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  • 67.

    Beuzón, C. R. & Holden, D. W. Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect. 3, 1345–1352 (2001).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar
     

  • 68.

    Ramos-Sevillano, E., Moscoso, M., García, P., García, E. & Yuste, J. Nasopharyngeal colonization and invasive disease are enhanced by the cell wall hydrolases LytB and LytC of Streptococcus pneumoniae. PLoS ONE 6, e23626 (2011).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 69.

    Langmead, B. & Salzberg, S. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     

  • 70.

    Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar
     



  • Source link

    Leave a Reply

    Your email address will not be published. Required fields are marked *