Prophages of Staphylococcus aureus Newman and their contribution to virulence

Four prophages (φNM1–4) were identified in the genome of Staphylococcus aureus Newman, a human clinical isolate. φNM1, φNM2 and φNM4, members of the siphoviridae family, insert at different sites (poiA, downstream of isdB and geh) in the staphylococcal chromosome. φNM3, a β‐haemolysin (hlb) converting phage, encodes modulators of innate immune responses (sea, sak, chp and scn) in addition to other virulence genes. Replication of φNM1, φNM2 and φNM4 occurs in culture and during animal infection, whereas φNM3 prophage replication was not observed. Prophages were excised from the chromosome and S. aureus variants lacking φNM3 or φNM1, φNM2 and φNM4 displayed organ specific virulence defects in a murine model of abscess formation. S. aureus Newman lacking all four prophages was unable to cause disease, thereby revealing essential contributions of prophages to the pathogenesis of staphylococcal infections.

[1]  C. Wolz,et al.  Extensive phage dynamics in Staphylococcus aureus contributes to adaptation to the human host during infection , 2006, Molecular microbiology.

[2]  O. Schneewind,et al.  Cross-Linked Peptidoglycan Mediates Lysostaphin Binding to the Cell Wall Envelope of Staphylococcus aureus , 2006, Journal of bacteriology.

[3]  G. Sensabaugh,et al.  Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus , 2006, The Lancet.

[4]  L. Marraffini,et al.  Sortases and the Art of Anchoring Proteins to the Envelopes of Gram-Positive Bacteria , 2006, Microbiology and Molecular Biology Reviews.

[5]  W. V. van Wamel,et al.  The Innate Immune Modulators Staphylococcal Complement Inhibitor and Chemotaxis Inhibitory Protein of Staphylococcus aureus Are Located on β-Hemolysin-Converting Bacteriophages , 2006, Journal of bacteriology.

[6]  Fred C Tenover,et al.  Prevalence of Staphylococcus aureus nasal colonization in the United States, 2001-2002. , 2006, The Journal of infectious diseases.

[7]  C. Wolz,et al.  Ciprofloxacin and Trimethoprim Cause Phage Induction and Virulence Modulation in Staphylococcus aureus , 2006, Antimicrobial Agents and Chemotherapy.

[8]  O. Schneewind,et al.  Allelic replacement in Staphylococcus aureus with inducible counter-selection. , 2006, Plasmid.

[9]  M. Holden,et al.  Understanding the rise of the superbug: investigation of the evolution and genomic variation of Staphylococcus aureus , 2006, Functional & Integrative Genomics.

[10]  M. Schaller,et al.  Phage release from biofilm and planktonic Staphylococcus aureus cells. , 2005, FEMS microbiology letters.

[11]  M. Mock,et al.  Identification of the Bacillus anthracis γ Phage Receptor , 2005 .

[12]  Robert B Sim,et al.  Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases , 2005, Nature Immunology.

[13]  Samuel V. Angiuoli,et al.  Insights on Evolution of Virulence and Resistance from the Complete Genome Analysis of an Early Methicillin-Resistant Staphylococcus aureus Strain and a Biofilm-Producing Methicillin-Resistant Staphylococcus epidermidis Strain , 2005, Journal of bacteriology.

[14]  L. Bossi,et al.  Prophage Arsenal of Salmonella enterica Serovar Typhimurium , 2005 .

[15]  M. Mock,et al.  Identification of the Bacillus anthracis (gamma) phage receptor. , 2005, Journal of bacteriology.

[16]  Wolf-Dietrich Hardt,et al.  Phages and the Evolution of Bacterial Pathogens: from Genomic Rearrangements to Lysogenic Conversion , 2004, Microbiology and Molecular Biology Reviews.

[17]  E. Glass,et al.  Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Andreas Peschel,et al.  Chemotaxis Inhibitory Protein of Staphylococcus aureus, a Bacterial Antiinflammatory Agent , 2004, The Journal of experimental medicine.

[19]  B. Neumeister,et al.  Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections , 2004, Nature Medicine.

[20]  M. Waldor,et al.  Transcription of the Toxin Genes Present within the Staphylococcal Phage φSa3ms Is Intimately Linked with the Phage's Life Cycle , 2003, Journal of bacteriology.

[21]  G. Reed,et al.  Coevolutionary patterns in plasminogen activation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  R. Novick Autoinduction and signal transduction in the regulation of staphylococcal virulence , 2003, Molecular microbiology.

[23]  R. Novick Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. , 2003, Plasmid.

[24]  Eric P. Skaar,et al.  Passage of Heme-Iron Across the Envelope of Staphylococcus aureus , 2003, Science.

[25]  D. Karamata,et al.  tagO is involved in the synthesis of all anionic cell-wall polymers in Bacillus subtilis 168. , 2002, Microbiology.

[26]  James M. Musser,et al.  Evolutionary genomics of Staphylococcus aureus: Insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[27]  R. Novick,et al.  Molecular genetics of SaPI1 – a mobile pathogenicity island in Staphylococcus aureus , 2001, Molecular microbiology.

[28]  P. Schlievert,et al.  Pathogenicity and resistance islands of staphylococci. , 2001, Microbes and infection.

[29]  J. Kaneko,et al.  Phage conversion of Panton-Valentine leukocidin in Staphylococcus aureus: molecular analysis of a PVL-converting phage, phiSLT. , 2001, Gene.

[30]  M. Kanehisa,et al.  Whole genome sequencing of meticillin-resistant Staphylococcus aureus , 2001, The Lancet.

[31]  M. Ohnishi,et al.  Phage conversion of exfoliative toxin A production in Staphylococcus aureus , 2000, Molecular microbiology.

[32]  S. Mazmanian,et al.  Staphylococcus aureus sortase mutants defective in the display of surface proteins and in the pathogenesis of animal infections. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Kaneko,et al.  Prophage, φPV83-pro, Carrying Panton-Valentine Leukocidin Genes, on the Staphylococcus aureus P83 Chromosome: Comparative Analysis of the Genome Structures of φPV83-pro, φPVL, φ11, and Other Phages , 2000 .

[34]  J. Kaneko,et al.  Prophage, phiPV83-pro, carrying panton-valentine leukocidin genes, on the Staphylococcus aureus P83 chromosome: comparative analysis of the genome structures of phiPV83-pro, phiPVL, phi11, and other phages. , 2000, Bioscience, biotechnology, and biochemistry.

[35]  Paul M. Orwin,et al.  Exotoxins of Staphylococcus aureus. , 2000, Clinical microbiology reviews.

[36]  A. Conde Staphylococcus aureus infections. , 1998, The New England journal of medicine.

[37]  R. Huber,et al.  The ternary microplasmin–staphylokinase–microplasmin complex is a proteinase–cofactor–substrate complex in action , 1998, Nature Structural Biology.

[38]  T. Kimura,et al.  Complete nucleotide sequence and molecular characterization of the temperate staphylococcal bacteriophage phiPVL carrying Panton-Valentine leukocidin genes. , 1998, Gene.

[39]  G. Archer Staphylococcus aureus: a well-armed pathogen. , 1998, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[40]  J. Strominger,et al.  Isolation of HLA-DR1.(staphylococcal enterotoxin A)2 trimers in solution. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[41]  D. Ohlendorf,et al.  Crystal structure of the superantigen staphylococcal enterotoxin type A. , 1995, The EMBO journal.

[42]  D. Cavanagh,et al.  Novel organization of the site‐specific integration and excision recombination functions of the Staphylococcus aureus serotype F virulence‐converting phages φ13 and φ42 , 1995, Molecular microbiology.

[43]  A L Cheung,et al.  Diminished virulence of a sar-/agr- mutant of Staphylococcus aureus in the rabbit model of endocarditis. , 1994, The Journal of clinical investigation.

[44]  M. Björklund,et al.  Immunopharmacology of the superantigen staphylococcal enterotoxin A in T-cell receptor V beta 3 transgenic mice. , 1993, Immunology.

[45]  D. Coleman,et al.  Serotype F double- and triple-converting phage insertionally inactivate the Staphylococcus aureus beta-toxin determinant by a common molecular mechanism. , 1993, FEMS microbiology letters.

[46]  I. Charles,et al.  Insertional inactivation of the Staphylococcus aureusβ‐toxin by bacteriophage φ13 occurs by site‐and orientation‐specific integration of the φ 13 genome , 1991, Molecular microbiology.

[47]  R. Arbeit,et al.  Virulence of Staphylococcus aureus mutants altered in type 5 capsule production , 1991, Infection and immunity.

[48]  R. Novick Genetic systems in staphylococci. , 1991, Methods in enzymology.

[49]  I. Charles,et al.  Insertional inactivation of the Staphylococcus aureus beta-toxin by bacteriophage phi 13 occurs by site- and orientation-specific integration of the phi 13 genome. , 1991, Molecular microbiology.

[50]  J. Iandolo,et al.  Structural analysis of staphylococcal bacteriophage phi 11 attachment sites , 1988, Journal of bacteriology.

[51]  D. Coleman,et al.  Cloning and expression in Escherichia coli and Staphylococcus aureus of the beta-lysin determinant from Staphylococcus aureus: evidence that bacteriophage conversion of beta-lysin activity is caused by insertional inactivation of the beta-lysin determinant. , 1986, Microbial pathogenesis.

[52]  J. Iandolo,et al.  Integration of staphylococcal phage L54a occurs by site-specific recombination: structural analysis of the attachment sites. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[53]  M. O'Reilly,et al.  The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage , 1983, Nature.

[54]  N. Thompson,et al.  Genetic transformation in Staphylococcus aureus: demonstration of a competence-conferring factor of bacteriophage origin in bacteriophage 80 alpha lysates , 1981, Journal of bacteriology.

[55]  K. Amako,et al.  Localization of bacteriophage receptor, clumping factor, and protein A on the cell surface of Staphylococcus aureus , 1980, Journal of bacteriology.

[56]  L. Philipson,et al.  Factors Affecting Competence for Transformation in Staphylococcus aureus , 1974, Journal of bacteriology.

[57]  E Borek,et al.  Lysogenic induction. , 1973, Progress in Nucleic Acid Research and Molecular Biology.

[58]  J. Ghuysen,et al.  Structure of the cell wall of Staphylococcus aureus, strain Copenhagen. IX. Teichoic acid and phage adsorption. , 1968, Biochemistry.

[59]  R. Novick Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus. , 1967, Virology.

[60]  E. Duthie,et al.  Staphylococcal coagulase; mode of action and antigenicity. , 1952, Journal of general microbiology.