Evolutionary genomics of Staphylococcus aureus reveals insights into the origin and molecular basis of ruminant host adaptation

Genome Biology and Evolution

Volumn 2, Issue 1, 2010, Pages 454-466

  Guinane, Caitriona M ^a   Zakour, Nouri L Ben ^a   Tormo Mas, Maria A ^b   Weinert, Lucy A ^c   Lowder, Bethan V ^a   Cartwright, Robyn A ^a   Smyth, Davida S ^d   Smyth, Cyril J ^e   Lindsay, Jodi A ^f   Gould, Katherine A ^f   Witney, Adam ^f   Hinds, Jason ^f   Bollback, Jonathan P ^c   Rambaut, Andrew ^c   Penadés, José R ^b   Fitzgerald, J Ross ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b INSTITUTO VALENCIANO DE INVESTIGACIONES AGRARIAS IVIA   (Spain)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSITY OF MISSISSIPPI   (United States)

^e TRINITY COLLEGE DUBLIN   (Ireland)

^f ST GEORGE S HOSPITAL   (United Kingdom)

Author keywords

Bacteria; Genome diversification; Mobile genetic elements; Niche adaptation; Population genetics

Indexed keywords

BACTERIAL DNA;

ADAPTATION; ANIMAL; ARTICLE; BACTERIAL GENOME; BOVIDS; CATTLE; CLASSIFICATION; COMPARATIVE GENOMIC HYBRIDIZATION; COMPARATIVE STUDY; ECOSYSTEM; GENETICS; GOAT; HOST PATHOGEN INTERACTION; HUMAN; INTERSPERSED REPEAT; MICROBIOLOGY; MOLECULAR EVOLUTION; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; SHEEP; SPECIES DIFFERENCE; STAPHYLOCOCCUS AUREUS;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BASE SEQUENCE; CATTLE; COMPARATIVE GENOMIC HYBRIDIZATION; DNA, BACTERIAL; ECOSYSTEM; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; GOATS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERSPERSED REPETITIVE SEQUENCES; PHYLOGENY; RUMINANTS; SHEEP; SPECIES SPECIFICITY; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); BOVIDAE; BOVINAE; OVIS ARIES; STAPHYLOCOCCUS AUREUS; UNGULATA;

EID: 77956622219     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evq031     Document Type: Article

References (83)

1. Aires-de-Sousa M, et al. 2007. Characterization of Staphylococcus aureus isolates from buffalo, bovine, ovine, and caprine milk samples collected in Rio de Janeiro State, Brazil. Appl Environ Microbiol. 73:3845-3849.
2. Anisimova M, Nielsen R, Yang Z. 2003. Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics. 164:1229-1236.
3. Aziz R, et al. 2008. The RAST Server: rapid annotations using subsystems technology. BMC Genomics. 9:75.
4. Baba T, et al. 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet. 359:1819-1827.
5. Bae T, Baba T, Hiramatsu K, Schneewind O. 2006. Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol Microbiol. 62:1035-1047.
6. Barrio MB, Rainard P, Prevost G. 2006. LukM/LukF'-PV is the most active Staphylococcus aureus leukotoxin on bovine neutrophils. Microbes Infect. 8:2068-2074.
7. Battisti A, et al. 2010. Heterogeneity among methicillin-resistant Staphylococcus aureus from Italian pig finishing holdings. Vet Microbiol. 142:361-366.
8. Ben Zakour NL, et al. 2008. Genome-wide analysis of ruminant Staphylococcus aureus reveals diversification of the core genome. J Bacteriol. 190:6302-6317.
9. Bjerketorp J, et al. 2002. A novel von Willebrand factor binding protein expressed by Staphylococcus aureus. Microbiology. 148:2037-2044.
10. Bjerketorp J, Rosander A, Nilsson M, Jacobsson K, Frykberg L. 2004. Sorting a Staphylococcus aureus phage display library against ex vivo biomaterial. J Med Microbiol. 53:945-951.
11. Brody T, et al. 2008. Horizontal gene transfers link a human MRSA pathogen to contagious bovine mastitis bacteria. PLoS One. 3: e3074.
12. Bruckner R. 1997. Gene replacement in Staphylococcus carnosus and Staphylococcus xylosus. FEMS Microbiol Lett. 151:1-8. (Pubitemid 27286260)
13. Bubeck Wardenburg J, Williams WA, Missiakas D. 2006. Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins. Proc Natl Acad Sci U S A. 103:13831-13836.
14. Carver TJ, et al. 2008. Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics. 24:2672-2676.
15. Carver TJ, et al. 2005. ACT: the Artemis Comparison Tool. Bioinformatics. 21:3422-3423.
16. Cheng AG, et al. 2009. Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J. 23:3393-3404.
17. Clarke SR, Foster SJ. 2006. Surface adhesins of Staphylococcus aureus. Adv Microb Physiol. 51:187-224.
18. Cooper JE, Feil EJ. 2006. The phylogeny of Staphylococcus aureus-which genes make the best intra-species markers? Microbiology. 152:1297-1305.
19. Corrigan RM, Miajlovic H, Foster TJ. 2009. Surface proteins that promote adherence of Staphylococcus aureus to human desquamated nasal epithelial cells. BMC Microbiol. 9:22.
20. Deringer JR, Ely RJ, Monday SR, Stauffacher CV, Bohach GA. 1997. Vbeta-dependent stimulation of bovine and human T cells by hostspecific staphylococcal enterotoxins. Infect Immun. 65:4048-4054.
21. Devriese LA. 1984. A simplified system for biotyping Staphylococcus aureus strains isolated from animal species. J Appl Bacteriol. 56:215-220.
22. Drummond AJ, Ho SY, Phillips MJ, Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4: e88.
23. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 7:214.
24. Eppinger M, et al. 2006. Who ate whom? Adaptive Helicobacter genomic changes that accompanied a host jump from early humans to large felines. PLoS Genet. 2: e120.
25. Ewing B, Hillier L, Wendl MC, Green P. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8:175-185. (Pubitemid 28177229)
26. Feil EJ, et al. 2003. How clonal is Staphylococcus aureus? J Bacteriol. 185:3307-3316.
27. Fitzgerald JR, Meaney WJ, Hartigan PJ, Smyth CJ, Kapur V. 1997. Fine-structure molecular epidemiological analysis of Staphylococcus aureus recovered from cows. Epidemiol Infect. 119:261-269.
28. Fitzgerald JR, et al. 2001. Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol. 183:63-70.
29. Gordon D. 2003. Viewing and editing assembled sequences using Consed. Curr Protoc Bioinformatics. Chapter 11: Unit11.2
30. Guinane CM, et al. 2008. Pathogenomic analysis of the common bovine Staphylococcus aureus clone (ET3): emergence of a virulent subtype with potential risk to public health. J Infect Dis. 197:205-213.
31. Harris SR, et al. 2010. Evolution of MRSA during hospital transmission and intercontinental spread. Science. 327:469-474.
32. Hasegawa M, Kishino H, Yano T. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 22:160-174.
33. Herron-Olson L, Fitzgerald JR, Musser JM, Kapur V. 2007. Molecular correlates of host specialization in Staphylococcus aureus. PLoS One. 2: e1120.
34. Herron LL, et al. 2002. Genome sequence survey identifies unique sequences and key virulence genes with unusual rates of amino acid substitution in bovine Staphylococcus aureus. Infect Immun. 70:3978-3981.
35. Iandolo JJ, et al. 2002. Comparative analysis of the genomes of the temperate bacteriophages phi 11, phi 12 and phi 13 of Staphylococcus aureus 8325. Gene. 289:109-118.
36. Ito T, et al. 2001. Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 45:1323-1336.
37. Jorgensen HJ, Mork T, Hogasen H, Rorvik LM. 2005. Enterotoxigenic Staphylococcus aureus in bulk milk in Norway. J Appl Microbiol. 99:158-166.
38. Kapur V, Sischo WM, Greer RS, Whittam TS, Musser JM. 1995. Molecular population genetic analysis of Staphylococcus aureus recovered from cows. J Clin Microbiol. 33:376-380.
39. Kishino H, Hasegawa M. 1989. Evaluation of the maximum likelihood estimates of the evolutionary tree topologies from sequence data, and the branching order in Hominoidea. J Mol Evol. 29:170-179.
40. Kosakovsky Pond SL, Frost SD, Muse SV. 2005. HyPhy: hypothesis testing using phylogenies. Bioinformatics. 21:676-679.
41. Lee PK, et al. 1992. Nucleotide sequences and biologic properties of toxic shock syndrome toxin 1 from ovine-and bovine-associated Staphylococcus aureus. J Infect Dis. 165:1056-1063.
42. Lefebure T, Stanhope MJ. 2007. Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition. Genome Biol. 8: R71.
43. Lindsay JA, et al. 2006. Microarrays reveal that each of the ten dominant lineages of Staphylococcus aureus has a unique combination of surface-associated and regulatory genes. J Bacteriol. 188:669-676.
44. Lowder BV, et al. 2009. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad Sci U S A. 106:19545-19550.
45. Ma XX, Ito T, Chongtrakool P, Hiramatsu K. 2006. Predominance of clones carrying Panton-Valentine leukocidin genes among methicillinresistant Staphylococcus aureus strains isolated in Japanese hospitals from 1979 to 1985. J Clin Microbiol. 44:4515-4527.
46. Madison RR. 1935. Fibrinolytic staphylococci. Proc Sac Exp Biol. 33:309.
47. Minnett FC. 1936. Staphylococci from animals with particular reference to toxin production. J Pathol Bacteriol. 42:247-259.
48. Moreillon P, et al. 1995. Role of Staphylococcus aureus coagulase and clumping factor in pathogenesis of experimental endocarditis. Infect Immun. 63:4738-4743.
49. Mwangi MM, et al. 2007. Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc Natl Acad Sci U S A. 104:9451-9456.
50. Ochman H. 2003. Neutral mutations and neutral substitutions in bacterial genomes. Mol Biol Evol. 20:2091-2096.
51. O'Neill AJ, Larsen AR, Skov R, Henriksen AS, Chopra I. 2007. Characterization of the epidemic European fusidic acid-resistant impetigo clone of Staphylococcus aureus. J Clin Microbiol. 45:1505-1510.
52. Overbeek R, et al. 2005. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 33:5691-5702.
53. Petersen L, Bollback JP, Dimmic M, Hubisz M, Nielsen R. 2007. Genes under positive selection in Escherichia coli. Genome Res. 17:1336-1343.
54. Raulf M, Alouf JE, Konig W. 1990. Effect of staphylococcal delta-toxin and bee venom peptide melittin on leukotriene induction and metabolism of human polymorphonuclear granulocytes. Infect Immun. 58:2678-2682.
55. Robinson DA, Monk AB, Cooper JE, Feil EJ, Enright MC. 2005. Evolutionary genetics of the accessory gene regulator (agr) locus in Staphylococcus aureus. J Bacteriol. 187:8312-8321.
56. Rodgers JD, McCullagh JJ, McNamee PT, Smyth JA, Ball HJ. 1999. Comparison of Staphylococcus aureus recovered from personnel in a poultry hatchery and in broiler parent farms with those isolated from skeletal disease in broilers. Vet Microbiol. 69:189-198.
57. Rooijakkers SH, et al. 2007. Staphylococcal complement inhibitor: structure and active sites. J Immunol. 179:2989-2998.
58. Rooijakkers SH, et al. 2006. Early expression of SCIN and CHIPS drives instant immune evasion by Staphylococcus aureus. Cell Microbiol. 8:1282-1293.
59. Rooijakkers SH, van Strijp JA. 2007. Bacterial complement evasion. Mol Immunol. 44:23-32.
60. Rutherford K, et al. 2000. Artemis: sequence visualization and annotation. Bioinformatics. 16:944-945.
61. Schmitz FJ, Veldkamp KE, Van Kessel KP, Verhoef J, Van Strijp JA. 1997. Delta-toxin from Staphylococcus aureus as a costimulator of human neutrophil oxidative burst. J Infect Dis. 176:1531-1537. (Pubitemid 27518154)
62. Schoen C, Joseph B, Claus H, Vogel U, Frosch M. 2007. Living in a changing environment: insights into host adaptation in Neisseria meningitidis from comparative genomics. Int J Med Microbiol. 297:601-613.
63. Shriner D, Nickle DC, Jensen MA, Mullins JI. 2003. Potential impact of recombination on sitewise approaches for detecting positive natural selection. Genet Res. 81:115-121.
64. Sloane R, et al. 1991. A toxic shock syndrome toxin mutant of Staphylococcus aureus isolated by allelic replacement lacks virulence in a rabbit uterine model. FEMS Microbiol Lett. 62:239-244.
65. Smith EM, et al. 2005. Multilocus sequence typing of intercontinental bovine Staphylococcus aureus isolates. J Clin Microbiol. 43:4737-4743.
66. Smyth DS, et al. 2009. Molecular genetic typing reveals further insights into the diversity of animal-associated Staphylococcus aureus. J Med Microbiol. 58:1343-1353.
67. Smyth DS, et al. 2010. Population structure of a hybrid clonal group of methicillin-resistant Staphylococcus aureus, ST239-MRSA-III. PLoS One. 5: e8582.
68. Stinear TP, et al. 2007. Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer. Genome Res. 17:192-200.
69. Strimmer K. 2008. fdrtool: a versatile R package for estimating local and tail area-based false discovery rates. Bioinformatics. 24:1461-1462.
70. Sung JM, Lloyd DH, Lindsay JA. 2008. Staphylococcus aureus host specificity: comparative genomics of human versus animal isolates by multi-strain microarray. Microbiology. 154:1949-1959.
71. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 24:1596-1599.
72. Tcherepanov V, Ehlers A, Upton C. 2006. Genome Annotation Transfer Utility (GATU): rapid annotation of viral genomes using a closely related reference genome. BMC Genomics 7:150.
73. Thompson JD, Higgins DG, Gibson TJ. 1994. 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.
74. Ubeda C, et al. 2005. Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol Microbiol. 56:836-844.
75. van Hijum SA, Zomer AL, Kuipers OP, Kok J. 2005. Projector 2: contig mapping for efficient gap-closure of prokaryotic genome sequence assemblies. Nucleic Acids Res. 33: W560-W566.
76. van Leeuwen WB, et al. 2003. Multilocus sequence typing of Staphylococcus aureus with DNA array technology. J Clin Microbiol. 41:3323-3326.
77. Waldron DE, Lindsay JA. 2006. Sau1: a novel lineage-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between S. aureus isolates of different lineages. J Bacteriol. 188:5578-5585.
78. *. Curr Protoc Bioinformatics. Chapter 6:Unit 6.4
79. Wren BW. 2000. Microbial genome analysis: insights into virulence, host adaptation and evolution. Nat Rev Genet. 1:30-39.
80. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556.
81. Yang Z, Nielsen R. 2000. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol. 17:32-43.
82. Yang Z, Wong WS, Nielsen R. 2005. Bayes empirical bayes inference of amino acid sites under positive selection. Mol Biol Evol. 22:1107-1118.
83. Zou D, Kaneko J, Narita S, Kamio Y. 2000. 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. Biosci Biotechnol Biochem. 64:2631-2643.