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Neutral Genomic Microevolution of a Recently Emerged Pathogen, Serovar Agona


Salmonella enterica serovar Agona has caused multiple food-borne outbreaks of gastroenteritis since it was first isolated in 1952. We analyzed the genomes of 73 isolates from global sources, comparing five distinct outbreaks with sporadic infections as well as food contamination and the environment. Agona consists of three lineages with minimal mutational diversity: only 846 single nucleotide polymorphisms (SNPs) have accumulated in the non-repetitive, core genome since Agona evolved in 1932 and subsequently underwent a major population expansion in the 1960s. Homologous recombination with other serovars of S. enterica imported 42 recombinational tracts (360 kb) in 5/143 nodes within the genealogy, which resulted in 3,164 additional SNPs. In contrast to this paucity of genetic diversity, Agona is highly diverse according to pulsed-field gel electrophoresis (PFGE), which is used to assign isolates to outbreaks. PFGE diversity reflects a highly dynamic accessory genome associated with the gain or loss (indels) of 51 bacteriophages, 10 plasmids, and 6 integrative conjugational elements (ICE/IMEs), but did not correlate uniquely with outbreaks. Unlike the core genome, indels occurred repeatedly in independent nodes (homoplasies), resulting in inaccurate PFGE genealogies. The accessory genome contained only few cargo genes relevant to infection, other than antibiotic resistance. Thus, most of the genetic diversity within this recently emerged pathogen reflects changes in the accessory genome, or is due to recombination, but these changes seemed to reflect neutral processes rather than Darwinian selection. Each outbreak was caused by an independent clade, without universal, outbreak-associated genomic features, and none of the variable genes in the pan-genome seemed to be associated with an ability to cause outbreaks.


Vyšlo v časopise: Neutral Genomic Microevolution of a Recently Emerged Pathogen, Serovar Agona. PLoS Genet 9(4): e32767. doi:10.1371/journal.pgen.1003471
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003471

Souhrn

Salmonella enterica serovar Agona has caused multiple food-borne outbreaks of gastroenteritis since it was first isolated in 1952. We analyzed the genomes of 73 isolates from global sources, comparing five distinct outbreaks with sporadic infections as well as food contamination and the environment. Agona consists of three lineages with minimal mutational diversity: only 846 single nucleotide polymorphisms (SNPs) have accumulated in the non-repetitive, core genome since Agona evolved in 1932 and subsequently underwent a major population expansion in the 1960s. Homologous recombination with other serovars of S. enterica imported 42 recombinational tracts (360 kb) in 5/143 nodes within the genealogy, which resulted in 3,164 additional SNPs. In contrast to this paucity of genetic diversity, Agona is highly diverse according to pulsed-field gel electrophoresis (PFGE), which is used to assign isolates to outbreaks. PFGE diversity reflects a highly dynamic accessory genome associated with the gain or loss (indels) of 51 bacteriophages, 10 plasmids, and 6 integrative conjugational elements (ICE/IMEs), but did not correlate uniquely with outbreaks. Unlike the core genome, indels occurred repeatedly in independent nodes (homoplasies), resulting in inaccurate PFGE genealogies. The accessory genome contained only few cargo genes relevant to infection, other than antibiotic resistance. Thus, most of the genetic diversity within this recently emerged pathogen reflects changes in the accessory genome, or is due to recombination, but these changes seemed to reflect neutral processes rather than Darwinian selection. Each outbreak was caused by an independent clade, without universal, outbreak-associated genomic features, and none of the variable genes in the pan-genome seemed to be associated with an ability to cause outbreaks.


Zdroje

1. NicolayN, ThorntonL, CotterS, GarveyP, BannonO, et al. (2011) Salmonella enterica serovar Agona European outbreak associated with a food company. Epidemiol Infect 139: 1272–1280.

2. TaylorJP, BarnettBJ, delRL, WilliamsK, BarthSS (1998) Prospective investigation of cryptic outbreaks of Salmonella agona salmonellosis. J Clin Microbiol 36: 2861–2864.

3. ThrelfallEJ, HamptonMD, WardLR, RoweB (1996) Application of pulsed-field gel electrophoresis to an international outbreak of Salmonella agona. Emerg Infect Dis 2: 130–132.

4. TenoverFC, ArbeitRD, GoeringRV, MickelsenPA, MurrayBE, et al. (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33: 2233–2239.

5. BarrettTJ, Gerner-SmidtP, SwaminathanB (2006) Interpretation of pulsed-field gel electrophoresis patterns in foodborne disease investigations and surveillance. Foodborne Pathog Dis 3: 20–31.

6. AllardMW, LuoY, StrainE, LiC, KeysCE, et al. (2012) High resolution clustering of Salmonella enterica serovar Montevideo strains using a Next-generation Sequencing approach. BMC Genomics 13: 32.

7. DiepBA, GillSR, ChangRF, PhanTH, ChenJH, et al. (2006) Complete genome sequence of USA300, an epidemic clone of community-acquired meticillin-resistant Staphylococcus aureus. Lancet 367: 731–739.

8. DiepBA, CarletonHA, ChangRF, SensabaughGF, Perdreau-RemingtonF (2006) Roles of 34 virulence genes in the evolution of hospital- and community-associated strains of methicillin-resistant Staphylococcus aureus. J Infect Dis 193: 1495–1503.

9. den BakkerHC, FortesED, WiedmannM (2010) Multilocus sequence typing of outbreak-associated Listeria monocytogenes isolates to identify epidemic clones. Foodborne Pathog Dis 7: 257–265.

10. HeM, MiyajimaF, RobertsP, EllisonL, PickardDJ, et al. (2012) Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nature Genet 45: 109–113.

11. AchtmanM, WainJ, WeillF-X, NairS, ZhouZ, et al. (2012) Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog 8: e1002776 doi:10.1371/journal.ppat.1002776.

12. RoumagnacP, WeillF-X, DolecekC, BakerS, BrisseS, et al. (2006) Evolutionary history of Salmonella Typhi. Science 314: 1301–1304.

13. HoltKE, ParkhillJ, MazzoniCJ, RoumagnacP, WeillF-X, et al. (2008) High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nature Genet 40: 987–993.

14. SangalV, HarbottleH, MazzoniCJ, HelmuthR, GuerraB, et al. (2010) Evolution and population structure of Salmonella enterica serovar Newport. J Bacteriol 192: 6465–6476.

15. GuineePAM, KampelmacherEH, WillemsHMCC (1961) Six new Salmonella types, isolated in Ghana (S. volta, S. agona, S. wa, S. techimani, S. mampong and S. tafo). Ant v Leeuwenhoek J 27: 469–472.

16. BarkerR, OldDC, TycZ (1982) Differential typing of Salmonella agona: type divergence in a new serotype. J Hyg (Lond) 88: 413–423.

17. HendriksenRS, VieiraAR, KarlsmoseS, Lo Fo WongDM, JensenAB, et al. (2011) Global monitoring of Salmonella serovar distribution from the World Health Organization Global Foodborne Infections Network Country Data Bank: Results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis 8: 887–900.

18. ClarkGM, KaufmannAF, GangarosaEJ, ThompsonMA (1973) Epidemiology of an international outbreak of Salmonella agona. Lancet 2: 490–493.

19. LeeJA (1974) Recent trends in human salmonellosis in England and Wales: the epidemiology of prevalent serotypes other than Salmonella typhimurium. J Hyg (Lond) 72: 185–195.

20. DioneMM, GeertsS, AntonioM (2012) Characterisation of novel strains of multiply antibiotic-resistant Salmonella recovered from poultry in Southern Senegal. J Infect Dev Ctries 6: 436–442.

21. HaleyCA, DargatzDA, BushEJ, ErdmanMM, Fedorka-CrayPJ (2012) Salmonella prevalence and antimicrobial susceptibility from the National Animal Health Monitoring System Swine 2000 and 2006 studies. J Food Prot 75: 428–436.

22. Quiroz-SantiagoC, Rodas-SuarezOR, CarlosR, V, FernandezFJ, Quinones-RamirezEI, et al. (2009) Prevalence of Salmonella in vegetables from Mexico. J Food Prot 72: 1279–1282.

23. AndersonPN, HumeME, ByrdJA, HernandezC, StevensSM, et al. (2010) Molecular analysis of Salmonella serotypes at different stages of commercial turkey processing. Poult Sci 89: 2030–2037.

24. CDC (1998) Multistate outbreak of Salmonella serotype Agona infections linked to toasted oats cereal–United States, April-May, 1998. MMWR 47: 462–464.

25. BrouardC, EspieE, WeillFX, KerouantonA, BrisaboisA, et al. (2007) Two consecutive large outbreaks of Salmonella enterica serotype Agona infections in infants linked to the consumption of powdered infant formula. Pediatr Infect Dis J 26: 148–152.

26. Anon. (2012) Investigation of outbreak of Infections caused by Salmonella Agona. Available: http://www.cdc.gov/salmonella/agona/.

27. LindqvistN, SiitonenA, PelkonenS (2002) Molecular follow-up of Salmonella enterica subsp. enterica serovar Agona infection in cattle and humans. J Clin Microbiol 40: 3648–3653.

28. RabschW, PragerR, KochJ, StarkK, RoggentinP, et al. (2005) Molecular epidemiology of Salmonella enterica serovar Agona: characterization of a diffuse outbreak caused by aniseed-fennel-caraway infusion. Epidemiol Infect 133: 837–844.

29. MutrejaA, KimDW, ThomsonNR, ConnorTR, LeeJH, et al. (2011) Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477: 462–465.

30. HarrisSR, FeilEJ, HoldenMT, QuailMA, NickersonEK, et al. (2010) Evolution of MRSA during hospital transmission and intercontinental spread. Science 327: 469–474.

31. KoserCU, HoldenMT, EllingtonMJ, CartwrightEJ, BrownNM, et al. (2012) Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. New England J Med 366: 2267–2275.

32. LeopoldSR, MagriniV, HoltNJ, ShaikhN, MardisER, et al. (2009) A precise reconstruction of the emergence and constrained radiations of Escherichia coli O157 portrayed by backbone concatenomic analysis. Proc Natl Acad Sci USA 106: 8713–8718.

33. HarrisSR, ClarkeIN, Seth-SmithHM, SolomonAW, CutcliffeLT, et al. (2012) Whole-genome analysis of diverse Chlamydia trachomatis strains identifies phylogenetic relationships masked by current clinical typing. Nature Genet 44: 413–419.

34. DidelotX, FalushD (2007) Inference of bacterial microevolution using multilocus sequence data. Genetics 175: 1251–1266.

35. NeumanJA, IsakovO, ShomronN (2013) Analysis of insertion-deletion from deep-sequencing data: software evaluation for optimal detection. Brief Bioinform 14: 46–55.

36. DrummondAJ, SuchardMA, XieD, RambautA (2012) Bayesian Phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29: 1969–1973.

37. CohanFM, PerryEB (2007) A systematics for discovering the fundamental units of bacterial diversity. Curr Biol 17: R373–R386.

38. CohanFM, KoeppelAF (2008) The origins of ecological diversity in prokaryotes. Curr Biol 18: R1024–R1034.

39. GuibourdencheM, RoggentinP, MikoleitM, FieldsPI, BockemuhlJ, et al. (2010) Supplement 2003–2007 (No. 47) to the White-Kauffmann-Le Minor scheme. Res Microbiol 161: 26–29.

40. MorelliG, DidelotX, KusecekB, SchwarzS, FalushD, et al. (2010) Microevolution of Helicobacter pylori during prolonged infection of single hosts and within families. PLoS Genet 6: e1001036 doi:10.1371/journal.pgen.1001036.

41. van Oye E (1964) The world problem of Salmonellosis. The Hague: Dr. W. Junk Publishers. 606 p.

42. HoSY, ShapiroB, PhillipsMJ, CooperA, DrummondAJ (2007) Evidence for time dependency of molecular rate estimates. Syst Biol 56: 515–522.

43. RochaEP, SmithJM, HurstLD, HoldenMT, CooperJE, et al. (2006) Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol 239: 226–235.

44. den BakkerHC, Moreno SwittAI, CummingsCA, HoelzerK, DegoricijaL, et al. (2011) A whole genome SNP based approach to trace and identify outbreaks linked to a common Salmonella enterica subsp. enterica serovar Montevideo Pulsed Field Gel Electrophoresis type. Appl Environ Microbiol 77: 8648–8655.

45. PelludatC, MiroldS, HardtWD (2003) The SopEΦ phage integrates into the ssrA gene of Salmonella enterica serovar Typhimurium A36 and is closely related to the Fels-2 prophage. J Bacteriol 185: 5182–5191.

46. AsadulghaniM, OguraY, OokaT, ItohT, SawaguchiA, et al. (2009) The defective prophage pool of Escherichia coli O157: prophage-prophage interactions potentiate horizontal transfer of virulence determinants. PLoS Pathog 5: e1000408 doi:10.1371/journal.ppat.1000408.

47. den BakkerHC, Moreno SwittAI, GovoniG, CummingsCA, RanieriML, et al. (2011) Genome sequencing reveals diversification of virulence factor content and possible host adaptation in distinct subpopulations of Salmonella enterica. BMC Genomics 12: 425.

48. JacobsenA, HendriksenRS, AaresturpFM, UsseryDW, FriisC (2011) The Salmonella enterica Pan-genome. Microb Ecol 62: 487–504.

49. HeM, MiyajimaF, RobertsP, EllisonL, PickardDJ, et al. (2012) Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nature Genet

50. OguraY, OokaT, IguchiA, TohH, AsadulghaniM, et al. (2009) Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli. Proc Natl Acad Sci USA 106: 17939–17944.

51. WaldorMK, MekalanosJJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272: 1910–1914.

52. SitkiewiczI, NagiecMJ, SumbyP, ButlerSD, Cywes-BentleyC, et al. (2006) Emergence of a bacterial clone with enhanced virulence by acquisition of a phage encoding a secreted phospholipase A2. Proc Natl Acad Sci USA 103: 16009–16014.

53. CroucherNJ, HarrisSR, FraserC, QuailMA, BurtonJ, et al. (2011) Rapid pneumococcal evolution in response to clinical interventions. Science 331: 430–434.

54. FabreL, ZhangJ, GuigonG, Le HelloS, GuibertV, et al. (2012) CRISPR typing and subtyping for improved laboratory surveillance of Salmonella infections. PLoS ONE 7: e36995 doi:10.1371/journal.pone.0036995.

55. WeinbergerAD, SunCL, PlucinskiMM, DenefVJ, ThomasBC, et al. (2012) Persisting viral sequences shape microbial CRISPR-based immunity. PLoS Comput Biol 8: e1002475 doi:10.1371/journal.pcbi.1002475.

56. Castillo-RamirezS, HarrisSR, HoldenMT, HeM, ParkhillJ, et al. (2011) The Impact of recombination on dN/dS within recently emerged bacterial clones. PLoS Pathog 7: e1002129 doi:10.1371/journal.ppat.1002129.

57. MorelliG, SongY, MazzoniCJ, EppingerM, RoumagnacP, et al. (2010) Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nature Genet 42: 1140–1143.

58. CuiY, YuC, YanY, LiD, LiY, et al. (2013) Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proc Natl Acad Sci USA 110: 577–582.

59. LiR, ZhuH, RuanJ, QianW, FangX, et al. (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20: 265–272.

60. HuQ, CoburnB, DengW, LiY, ShiX, et al. (2008) Salmonella enterica serovar Senftenberg human clinical isolates lacking SPI-1. J Clin Microbiol 46: 1330–1336.

61. Brown EW (2012) Use of Next-Generation Sequencing to augment characterization of Salmonella enterica strains associated with contamination of the food supply. In: 16th Annual PulseNet Meeting; 29 August 2012; Atlanta, GA, USA. Available: http://www.aphl.org/conferences/proceedings/Documents/2012/2012-PulseNet-OutbreakNet/013-Brown_E.pdf.

62. FrickeWF, MammelMK, McDermottPF, TarteraC, WhiteDG, et al. (2011) Comparative genomics of 28 Salmonella enterica isolates: Evidence for CRISPR-mediated adaptive sublineage evolution. J Bacteriol 193: 3556–3568.

63. LiR, LiY, KristiansenK, WangJ (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24: 713–714.

64. KurtzS, PhillippyA, DelcherAL, SmootM, ShumwayM, et al. (2004) Versatile and open software for comparing large genomes. Genome Biol 5: R12.

65. BensonG (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27: 573–580.

66. TamuraK, DudleyJ, NeiM, KumarS (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.

67. GuindonS, GascuelO (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696–704.

68. KeaneTM, NaughtonTJ, McInerneyJO (2007) MultiPhyl: a high-throughput phylogenomics webserver using distributed computing. Nucleic Acids Res 35: W33–W37.

69. KassRE, RafteryAE (1995) Bayes Factors. J Amer Statist Assoc 90: 773–795.

70. SalzbergSL, DelcherAL, KasifS, WhiteO (1998) Microbial gene identification using interpolated Markov models. Nucleic Acids Res 26: 544–548.

71. SuzekBE, HuangH, McGarveyP, MazumderR, WuCH (2007) UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics 23: 1282–1288.

72. MullerJ, SzklarczykD, JulienP, LetunicI, RothA, et al. (2010) eggNOG v2.0: extending the evolutionary genealogy of genes with enhanced non-supervised orthologous groups, species and functional annotations. Nucleic Acids Res 38: D190–D195.

73. SiguierP, PerochonJ, LestradeL, MahillonJ, ChandlerM (2006) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34: D32–D36.

74. NingZ, CoxAJ, MullikinJC (2001) SSAHA: a fast search method for large DNA databases. Genome Res 11: 1725–1729.

75. AlbersCA, LunterG, MacArthurDG, McVeanG, OuwehandWH, et al. (2011) Dindel: accurate indel calls from short-read data. Genome Res 21: 961–973.

76. ChenL, XiongZ, SunL, YangJ, JinQ (2012) VFDB 2012 update: toward the genetic diversity and molecular evolution of bacterial virulence factors. Nucleic Acids Res 40: D641–D645.

77. TobeT, BeatsonSA, TaniguchiH, AbeH, BaileyCM, 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: 14941–14946.

78. MarinusMG, MorrisNR (1973) Isolation of deoxyribonucleic acid methylase mutants of Escherichia coli K-12. J Bacteriol 114: 1143–1150.

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