Molecular signatures identify a candidate target of balancing selection in an arcD-like gene of Staphylococcus epidermidis

Journal of Molecular Evolution

Volumn 75, Issue 1-2, 2012, Pages 43-54

  Zhang, Liangfen ^a   Thomas, Jonathan C ^a   Didelot, Xavier ^b   Robinson, D Ashley ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Approximate bayesian computation; Balancing selection; Genetic hitchhiking; Population genetics; Staphylococcus aureus; Staphylococcus epidermidis

Indexed keywords

AMINO ACID TRANSPORTER; ANTIPORTER; ARCD PROTEIN, BACTERIA; BACTERIAL PROTEIN;

BACTERIAL GENE; BIOLOGICAL MODEL; GENETIC RECOMBINATION; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTILOCUS SEQUENCE TYPING; NUCLEOTIDE SEQUENCE; PHYLOGENY; REVIEW; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS INFECTION; STATISTICAL MODEL;

AMINO ACID TRANSPORT SYSTEMS; ANTIPORTERS; BACTERIAL PROTEINS; BASE SEQUENCE; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENES, BACTERIAL; GENETIC VARIATION; HUMANS; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; MOLECULAR SEQUENCE ANNOTATION; MOLECULAR SEQUENCE DATA; MULTILOCUS SEQUENCE TYPING; PHYLOGENY; RECOMBINATION, GENETIC; SELECTION, GENETIC; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 84868573047     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-012-9520-5     Document Type: Review

References (84)

1. Andrés AM, Hubisz MJ, Indap A, Torgerson DG, Degenhardt JD, Boyko AR, Gutenkunst RN, White TJ, Green ED, Bustamante CD, Clark AG, Nielsen R (2009) Targets of balancing selection in the human genome. Mol Biol Evol 26:2755-2764
2. Beaumont MA, Zhang W, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025-2035
3. Boucher H, Miller LG, Razonable RR (2010) Serious infections caused by methicillin-resistant Staphylococcus aureus. Clin Infect Dis 51:S183-S197
4. Brisson D, Dykhuizen DE (2004) ospC diversity in Borrelia burgdorferi. Genetics 168:713-722
5. Camus-Kulandaivelu L, Chevin LM, Tollon-Cordet C, Charcosset A, Manicacci D, Tenaillon MI (2008) Patterns of molecular evolution associated with two selective sweeps in the Tb1-Dwarf8 region in maize. Genetics 180:1107-1121
6. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540-552
7. Castric V, Bechsgaard J, Schierup MH, Vekemans X (2008) Repeated adaptive introgression at a gene under multiallelic balancing selection. PLoS Genet 4:e1000168
8. Charlesworth D (2006) Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2:e64
9. Chen JS, Reddy V, Chen JH, Shlykov MA, Zheng WH, Cho J, Yen MR, Saier MH Jr (2011) Phylogenetic characterization of transport protein superfamilies: superiority of SuperfamilyTree programs over those based on multiple alignments. J Mol Microbiol Biotechnol 21:83-96
10. Chevin LM, Billiard S, Hospital F (2008) Hitchhiking both ways: effect of two interfering selective sweeps on linked neutral variation. Genetics 180:301-316
11. Darling AE, Mau B, Perna NT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147
12. Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465-W469
13. Didelot X, Falush D (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175:1251-1266
14. Didelot X, Maiden MC (2010) Impact of recombination on bacterial evolution. Trends Microbiol 18:315-322
15. Diep BA, Gill SR, Chang RF, Phan TH, Chen JH, Davidson MG, Lin F, Lin J, Carleton HA, Mongodin EF, Sensabaugh GF, Perdreau-Remington F (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367:731-739
16. Diep BA, Stone GG, Basuino L, Graber CJ, Miller A, des Etages SA, Jones A, Palazzolo-Ballance AM, Perdreau-Remington F, Sensabaugh GF, De Leo FR, Chambers HF (2008) The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 197:1523-1530
17. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792-1797
18. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG (2000) Multilocus sequence typing for characterization of methicillinresistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38:1008-1015
19. Evans PD, Mekel-Bobrov N, Vallender EJ, Hudson RR, Lahn BT (2006) Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homo lineage. Proc Natl Acad Sci USA 103:18178-18183
20. Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405-1413
21. Feil EJ, Cooper JE, Grundmann H, Robinson DA, Enright MC, Berendt T, Peacock SJ, Smith JM, Murphy M, Spratt BG, Moore CE, Day NPJ (2003) How clonal is Staphylococcus aureus? J Bacteriol 185:3307-3316
22. Foster TJ (2005) Immune evasion by staphylococci. Nat Rev Microbiol 3:948-958
23. Fumagalli M, Cagliani R, Riva S, Pozzoli U, Biasin M, Piacentini L, Comi GP, Bresolin N, Clerici M, Sironi M (2010) Population genetics of IFIH1: ancient population structure, local selection, and implications for susceptibility to type 1 diabetes. Mol Biol Evol 27:2555-2566
24. Gill SR, Fouts DE, Archer GL et al (2005) 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. J Bacteriol 187:2426-2438
25. Gordo I, Gomes MG, Reis DG, Campos PR (2009) Genetic diversity in the SIR model of pathogen evolution. PLoS One 4:e4876
26. Grundmann H, Hori S, Tanner G (2001) Determining confidence intervals when measuring genetic diversity and the discriminatory abilities of typing methods for microorganisms. J Clin Microbiol 39:4190-4192
27. Hiwatashi T, Okabe Y, Tsutsui T, Melin AD, Oota H, Schaffner CM, Aureli F, Fedigan LM, Innan H, Kawamura S (2010) An explicit signature of balancing selection for color-vision variation in new world monkeys. Mol Biol Evol 27:453-464
28. Hudson RR (2002) Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinfomatics 18:337-338
29. Hudson RR, Kreitman M, Aguadé M (1987) A testof neutral molecular evolution based on nucleotide data. Genetics 116:153-159
30. Ingvarsson PK (2004) Population subdivision and the Hudson-Kreitman- Aguade test: testing for deviations from the neutral model in organelle genomes. Genet Res 83:31-39
31. Innan H (2006) Modified Hudson-Kreitman-Aguadé test and two-dimensional evaluation of neutrality tests. Genetics 173:1725-1733
32. Joshi GS, Spontak JS, Klapper DG, Richardson AR (2011) Arginine catabolic mobile element encoded speG abrogates the unique hypersensitivity of Staphylococcus aureus to exogenous polyamines. Mol Microbiol 82:19-20
33. Kozitskaya S, Olson ME, Fey PD, Witte W, Ohlsen K, Ziebuhr W (2005) Clonal analysis of Staphylococcus epidermidis isolates carrying or lacking biofilm-mediating genes by multilocus sequence typing. J Clin Microbiol 43:4751-4757
34. Kreitman M (2000) Methods to detect selection in populations with application to the human. Annu Rev Genomics Hum Genet 1:539-559
35. Kreitman M, Di Rienzo A (2004) Balancing claims for balancing selection. Trends Genet 20:300-304
36. Kuroda M, Ohta T, Uchiyama I et al (2001) Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet 357:1225-1240
37. Kuroda M, Yamashita A, Hirakawa H, Kumano M, Morikawa K, Higashide M, Maruyama A, Inose Y, Matoba K, Toh H, Kuhara S, Hattori M, Ohta T (2005) Whole genome sequence of Staphylococcus saprophyticus reveals the pathogenesis of uncomplicated urinary tract infection. Proc Natl Acad Sci USA 102:13272-13277
38. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451-1452
39. Liu Y, Dong Y, Chen YY, Burne RA (2008) Environmental and growth phase regulation of the Streptococcus gordonii arginine deiminase genes. Appl Environ Microbiol 74:5023-5030
40. Loader CR (1996) Local likelihood density estimation. Ann Stat 24:1602-1618
41. Lolkema JS, Slotboom DJ (2003) Classification of 29 families of secondary transport proteins into a single structural class using hydropathy profile analysis. J Mol Biol 327:901-909
42. Makhlin J, Kofman T, Borovok I, Kohler C, Engelmann S, Cohen G, Aharonowitz Y (2007) Staphylococcus aureus ArcR controls expression of the arginine deiminase operon. J Bacteriol 189:5976-5986
43. Martin D, Rybicki E (2000) RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562-563
44. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462-2463
45. Mathema B, Mediavilla JR, Chen L, Kreiswirth B (2009) Evolution and taxonomy of staphylococci. In: Crossley KB, Jefferson KK, Archer GL, Fowler VG (eds) Staphylococci in human disease, 2nd edn. Wiley-Blackwell, Oxford
46. Maynard Smith J (1992) Analyzing the mosaic structure of genes. J Mol Evol 34:126-129
47. Miragaia M, Thomas JC, Couto I, Enright MC, de Lencastre H (2007) Inferringapopulationstructure forStaphylococcusepidermidisfrom multilocus sequence typing data. J Bacteriol 189:2540-2552
48. Miragaia M, de Lencastre H, Perdreau-Remington F, Chambers HF, Higashi J, Sullam PM, Lin J, Wong KI, King KA, Otto M, Sensabaugh GF, Diep BA (2009) Genetic diversity of arginine catabolic mobile element in Staphylococcus epidermidis. PLoS One 4:e7722
49. Montgomery CP, Boyle-Vavra S, Daum RS (2009) The arginine catabolic mobile element is not associated with enhanced virulence in experimental invasive disease caused by the community-associated methicillin-resistant Staphylococcus aureus USA300 genetic background. Infect Immun 77:2650-2656
50. Ochola LI, Tetteh KK, Stewart LB, Riitho V, Marsh K, Conway DJ (2010) Allele frequency-based and polymorphism-versus-divergence indices of balancing selection in a new filtered set of polymorphic genes in Plasmodium falciparum. Mol Biol Evol 27:2344-2351
51. Otto M (2009) Staphylococcus epidermidis-the 'accidental' pathogen. Nat Rev Microbiol 7:555-567
52. Padhukasahasram B, Marjoram P, Nordborg M (2004) Estimating the rate of gene conversion on human chromosome 21. Am J Hum Genet 75:386-397
53. Pérez-Losada M, Browne EB, Madsen A, Wirth T, Viscidi RP, Crandall KA (2006) Population genetics of microbial pathogens estimated from multilocus sequence typing (MLST) data. Infect Genet Evol 6:97-112
54. Plagnol V, Wall JD (2006) Possible ancestral structure in human populations. PLoS Genet 2:e105
55. Posada D, Crandall KA (2001) Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 98:13757-13762
56. Prakash S, Cooper G, Singhi S, Saier MH Jr (2003) The ion transporter superfamily. Biochim Biophys Acta 1618:79-92
57. Przeworski M, Coop G, Wall JD (2005) The signature of positive selection on standing genetic variation. Evolution 59:2312-2323
58. Rambaut A, Grassly NC (1997) Seq-Gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees. Comput Appl Biosci 13:235-238
59. Richman A (2000) Evolution of balanced genetic polymorphism. Mol Ecol 9:1953-1963
60. Ruimy R, Maiga A, Armand-Lefevre L, Maiga I, Diallo A, Koumaré AK, Ouattara K, Soumaré S, Gaillard K, Lucet JC, Andremont A, Feil EJ (2008) The carriage population of Staphylococcus aureus from Mali is composed of a combination of pandemic clones and the divergent Panton-Valentine leukocidin-positive genotype ST152. J Bacteriol 190:3962-3968
61. Saier MH Jr, Tran CV, Barabote RD (2006) TCDB: the Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Res 34:D181-D186
62. Sawyer SA (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526-538
63. Smyth DS, Robinson DA (2010) Population genetics of Staphylococcus. In: Robinson DA, Falush D, Feil EJ (eds) Bacterial population genetics in infectious disease, 1st edn. Wiley-Blackwell, New Jersey
64. Smyth DS, Wong A, Robinson DA (2011) Cross-species spread of SCCmec IV subtypes in staphylococci. Infect Genet Evol 11:446-451
65. Storz JF, Wheat CW (2010) Integrating evolutionary and functional approaches to infer adaptation at specific loci. Evolution 64:2489-2509
66. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595
67. Takeuchi F, Watanabe S, Baba T, Yuzawa H, Ito T, Morimoto Y, Kuroda M, Cui L, Takahashi M, Ankai A, Baba S, Fukui S, Lee JC, Hiramatsu K (2005) Whole-genome sequencing of Staphylococcus haemolyticus uncovers the extreme plasticity of its genome and the evolution of human-colonizing staphylococcal species. J Bacteriol 187:7292-7308
68. Thomas JC, Vargas MR, Miragaia M, Peacock SJ, Archer GL, Enright MC (2007) An improved multilocus sequence typing scheme for Staphylococcus epidermidis. J Clin Microbiol 45:616-619
69. Thomas JC, Godfrey PA, Feldgarden M, Robinson DA (2012) Candidate targets of balancing selection in the genome of Staphylococcus aureus. Mol Biol Evol 29:1175-1186
70. Thornton K, Andolfatto P (2006) Approximate Bayesian inference reveals evidence for a recent, severe bottleneck in a Netherlands population of Drosophila melanogaster. Genetics 172:1607-1619
71. van Belkum A, Melles DC, Nouwen J, van Leeuwen WB, van Wamel W, Vos MC, Wertheim HFL, Verbrugh HA (2009) Co-evolutionary aspects of human colonisation and infection by Staphylococcus aureus. Infect Genet Evol 9:32-47
72. Verhoogt HJ, Smit H, Abee T, Gamper M, Driessen AJ, Haas D, Konings WN (1992) arcD, the first gene of the arc operon for anaerobic arginine catabolism in Pseudomonas aeruginosa, encodes an arginine-ornithine exchanger. J Bacteriol 174:1568-1573
73. Vilella AJ, Blanco-Garcia A, Hutter S, Rozas J (2005) VariScan: analysis of evolutionary patterns from large-scale DNA sequence polymorphism data. Bioinformatics 21:2791-2793
74. von Eiff C, Peters G, Heilmann C (2002) Pathogenesis of infections due to coagulase-negative staphylococci. Lancet Infect Dis 2:677-685
75. Vos M, Didelot X (2009) A comparison of homologous recombination rates in bacteria and archaea. ISME J 3:199-208
76. Watterson GA (1975) Number of segregating sites in genetics models without recombination. Theor Popul Biol 7:256-276
77. Weedall GD, Conway DJ (2010) Detecting signatures of balancing selection to identify targets of anti-parasite immunity. Trends Parasitol 26:363-369
78. Wildschutte H, Lawrence JG (2007) Differential Salmonella survival against communities of intestinal amoebae. Microbiology 41:10095-10104
79. Wiuf C, Zhao K, Innan H, Nordborg M (2004) The probability and chromosomal extent of trans-specific polymorphism. Genetics 168:2363-2372
80. Wong A, Reddy SP, Smyth DS, Aguero-Rosenfeld ME, Sakoulas G, Robinson DA (2010) Polyphyletic emergence of linezolidresistant staphylococci in the United States. Antimicrob Agents Chemother 54:742-748
81. Zhang YQ, Ren SX, Li HL, Wang YX, Fu G, Yang J, Qin ZQ, Miao YG, Wang WY, Chen RS, Shen Y, Chen Z, Yuan ZH, Zhao GP, Qu D, Danchin A, Wen YM (2003) Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol Microbiol 49:1577-1593
82. Zhu Y, Weiss EC, Otto M, Fey PD, Smeltzer MS, Somerville GA (2007) Staphylococcus aureus biofilm metabolism and the influence of arginine on polysaccharide intercellular adhesin synthesis, biofilm formation, and pathogenesis. Infect Immun 75:4219-4226
83. Zúñiga M, Champomier-Verges M, Zagorec M, Pérez-Martínez G (1998) Structural and functional analysis of the gene cluster encoding the enzymes of the arginine deiminase pathway of Lactobacillus sake. J Bacteriol 180:4154-4159
84. Zúñiga M, Pérez G, González-Candelas F (2002) Evolution of arginine deiminase (ADI) pathway genes. Mol Phylogenet Evol 25:429-444