Evolution of Salmonella enterica serotype Typhimurium driven by anthropogenic selection and niche adaptation

Autoři: Matt Bawn aff001;  Nabil-Fareed Alikhan aff001;  Gaëtan Thilliez aff001;  Mark Kirkwood aff001;  Nicole E. Wheeler aff003;  Liljana Petrovska aff004;  Timothy J. Dallman aff005;  Evelien M. Adriaenssens aff001;  Neil Hall aff002;  Robert A. Kingsley aff001
Působiště autorů: Quadram Institute Biosciences, Norwich Research Park, Norwich, United Kingdom aff001;  Earlham Institute, Norwich Research Park, Norwich, United Kingdom aff002;  Centre for Genomic Pathogen Surveillance, Wellcome Sanger Institute, Cambridge, United Kingdom aff003;  Animal and Plant Health Agency, Addlestone, United Kingdom aff004;  Gastrointestinal Bacteria Reference Unit, National Infection Service, Public Health England, London, United Kingdom aff005;  University of East Anglia, Norwich, United Kingdom aff006
Vyšlo v časopise: Evolution of Salmonella enterica serotype Typhimurium driven by anthropogenic selection and niche adaptation. PLoS Genet 16(6): e32767. doi:10.1371/journal.pgen.1008850
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008850


Salmonella enterica serotype Typhimurium (S. Typhimurium) is a leading cause of gastroenteritis and bacteraemia worldwide, and a model organism for the study of host-pathogen interactions. Two S. Typhimurium strains (SL1344 and ATCC14028) are widely used to study host-pathogen interactions, yet genotypic variation results in strains with diverse host range, pathogenicity and risk to food safety. The population structure of diverse strains of S. Typhimurium revealed a major phylogroup of predominantly sequence type 19 (ST19) and a minor phylogroup of ST36. The major phylogroup had a population structure with two high order clades (α and β) and multiple subclades on extended internal branches, that exhibited distinct signatures of host adaptation and anthropogenic selection. Clade α contained a number of subclades composed of strains from well characterized epidemics in domesticated animals, while clade β contained multiple subclades associated with wild avian species. The contrasting epidemiology of strains in clade α and β was reflected by the distinct distribution of antimicrobial resistance (AMR) genes, accumulation of hypothetically disrupted coding sequences (HDCS), and signatures of functional diversification. These observations were consistent with elevated anthropogenic selection of clade α lineages from adaptation to circulation in populations of domesticated livestock, and the predisposition of clade β lineages to undergo adaptation to an invasive lifestyle by a process of convergent evolution with of host adapted Salmonella serotypes. Gene flux was predominantly driven by acquisition and recombination of prophage and associated cargo genes, with only occasional loss of these elements. The acquisition of large chromosomally-encoded genetic islands was limited, but notably, a feature of two recent pandemic clones (DT104 and monophasic S. Typhimurium ST34) of clade α (SGI-1 and SGI-4).

Klíčová slova:

Antimicrobial resistance – Bacteriophages – Bird genomics – Livestock – Salmonella typhimurium – Sequence analysis – Sequence assembly tools – Sequence databases


1. Kingsley R, Bäumler J. Host adaptation and the emergence of infectious disease: the Salmonella paradigm. Mol Micro. 2000;36. doi: 10.1046/j.1365-2958.2000.01907.x 10844686

2. Kirk MD, Pires SM, Black RE, Caipo M, Crump JA, Devleesschauwer B, et al. World Health Organization Estimates of the Global and Regional Disease Burden of 22 Foodborne Bacterial, Protozoal, and Viral Diseases, 2010: A Data Synthesis. PLoS Med. 2015;12(12):e1001921. Epub 2015/12/04. doi: 10.1371/journal.pmed.1001921 26633831; PubMed Central PMCID: PMC4668831.

3. Rabsch W, Andrews HL, Kingsley RA, Prager R, Tschape H, Adams LG, et al. Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect Immun. 2002;70(5):2249–55. doi: 10.1128/iai.70.5.2249-2255.2002 11953356

4. Branchu P, Bawn M, Kingsley RA. Genome variation and molecular epidemiology of Salmonella Typhimurium pathovariants. Infect Immun. 2018;86(8):e00079–18. Epub 2018/05/23. doi: 10.1128/IAI.00079-18 29784861.

5. Anonymous. Salmonella in livestock production in Great Britain, 2017: gov.uk; 2018 [cited 2019 June 2019]. Available from: https://www.gov.uk/government/publications/salmonella-in-livestock-production-in-great-britain-2017.

6. Rabsch W. Salmonella Typhimurium Phage Typing for Pathogens. In: Schatten H, Eisenstark A, editors. Salmonella, Methods and Protocols. Methods in Molecular Biology. 394 ed. Totowa, New Jersey: Humana Press; 2007. p. 177–212.

7. Threlfall EJ, Ward LR, Rowe B. Spread of multiresistant strains of Salmonella typhimurium phage types 204 and 193 in Britain. Br Med J. 1978;2(6143):997.

8. Rabsch W, Tschape H, Baumler AJ. Non-typhoidal salmonellosis: emerging problems. Microbes Infect. 2001;3(3):237–47. doi: 10.1016/s1286-4579(01)01375-2 11358718.

9. Rabsch W, Truepschuch S, Windhorst D, Gerlach RG. Typing phages and prophages of Salmonella. Norfolk, UK: Caister Academic Press; 2011.

10. Tassinari E, Duffy G, Bawn M, Burgess CM, McCabe EM, Lawlor PG, et al. Microevolution of antimicrobial resistance and biofilm formation of Salmonella Typhimurium during persistence on pig farms. Sci Rep. 2019;9(1):8832. Epub 2019/06/22. doi: 10.1038/s41598-019-45216-w 31222015; PubMed Central PMCID: PMC6586642.

11. Ashton PM, Peters T, Ameh L, McAleer R, Petrie S, Nair S, et al. Whole Genome Sequencing for the Retrospective Investigation of an Outbreak of Salmonella Typhimurium DT 8. PLoS Curr. 2015;7. Epub 2015/02/26. doi: 10.1371/currents.outbreaks.2c05a47d292f376afc5a6fcdd8a7a3b6 25713745; PubMed Central PMCID: PMC4336196.

12. Mather AE, Lawson B, de Pinna E, Wigley P, Parkhill J, Thomson NR, et al. Genomic Analysis of Salmonella enterica Serovar Typhimurium from Wild Passerines in England and Wales. Appl Environ Microbiol. 2016;82(22):6728–35. Epub 2016/10/30. doi: 10.1128/AEM.01660-16 27613688; PubMed Central PMCID: PMC5086566.

13. Hughes LA, Shopland S, Wigley P, Bradon H, Leatherbarrow AH, Williams NJ, et al. Characterisation of Salmonella enterica serotype Typhimurium isolates from wild birds in northern England from 2005–2006. BMC Vet Res. 2008;4:4. Epub 2008/01/31. doi: 10.1186/1746-6148-4-4 18230128; PubMed Central PMCID: PMC2257933.

14. Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE, Gordon MA, et al. Epidemic multiple drug resistant Salmonella typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res. 2009;19. doi: 10.1101/gr.091017.109 19901036

15. Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA. Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet. 2012;379(9835):2489–99. Epub 2012/05/17. doi: 10.1016/S0140-6736(11)61752-2 22587967; PubMed Central PMCID: PMC3402672.

16. Cheng L, Connor TR, Siren J, Aanensen DM, Corander J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol. 2013;30(5):1224–8. Epub 2013/02/15. doi: 10.1093/molbev/mst028 23408797; PubMed Central PMCID: PMC3670731.

17. Hooton SP, Atterbury RJ, Connerton IF. Application of a bacteriophage cocktail to reduce Salmonella Typhimurium U288 contamination on pig skin. Int J Food Microbiol. 2011;151(2):157–63. Epub 2011/09/09. doi: 10.1016/j.ijfoodmicro.2011.08.015 21899907.

18. Petrovska L, Mather AE, AbuOun M, Branchu P, Harris SR, Connor T, et al. Microevolution of monophasic Salmonella Typhimurium during epidemic, United Kingdom, 2005–2010. Emerging infectious diseases. 2016;22(4):617. doi: 10.3201/eid2204.150531 26982594

19. Mather AE, Reid SWJ, Maskell DJ, Parkhill J, Fookes MC, Harris SR, et al. Distinguishable Epidemics of Multidrug-Resistant Salmonella Typhimurium DT104 in Different Hosts. Science. 2013;341(6153):1514–7. doi: 10.1126/science.1240578 WOS:000324894600051. 24030491

20. Leekitcharoenphon P, Hendriksen RS, Le Hello S, Weill FX, Baggesen DL, Jun SR, et al. Global Genomic Epidemiology of Salmonella enterica Serovar Typhimurium DT104. Appl Environ Microbiol. 2016;82(8):2516–26. Epub 2016/03/06. doi: 10.1128/AEM.03821-15 26944846; PubMed Central PMCID: PMC4959494.

21. Kingsley RA, Kay S, Connor T, Barquist L, Sait L, Holt KE, et al. Genome and Transcriptome Adaptation Accompanying Emergence of the Definitive Type 2 Host-Restricted Salmonella enterica Serovar Typhimurium Pathovar. mBio. 2013;4(5). doi: 10.1128/mBio.00565-13 23982073

22. Okoro CK, Kingsley RA, Connor TR, Harris SR, Parry CM, Al-Mashhadani MN, et al. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet. 2012;44(11):1215–21. doi: 10.1038/ng.2423 23023330; PubMed Central PMCID: PMC3491877.

23. Branchu P, Charity O, Bawn M, Thilliez G, Dallman TJ, Petrovska L, et al. SGI-4 in monophasic Salmonella Typhimurium ST34 is a novel ICE that enhances resistance to copper. Frontiers in microbiology. 2019;10:1118. doi: 10.3389/fmicb.2019.01118 31178839

24. Zhou Z, Alikhan NF, Mohamed K, Fan Y, Agama Study G, Achtman M. The EnteroBase user's guide, with case studies on Salmonella transmissions, Yersinia pestis phylogeny, and Escherichia core genomic diversity. Genome Res. 2020;30(1):138–52. Epub 2019/12/07. doi: 10.1101/gr.251678.119 31809257; PubMed Central PMCID: PMC6961584.

25. Turner AK, Nair S, Wain J. The acquisition of full fluoroquinolone resistance in Salmonella Typhi by accumulation of point mutations in the topoisomerase targets. Journal of Antimicrobial Chemotherapy. 2006;58(4):733–40. RefWorks:212. doi: 10.1093/jac/dkl333 16895934

26. Garcia V, Montero I, Bances M, Rodicio R, Rodicio MR. Incidence and Genetic Bases of Nitrofurantoin Resistance in Clinical Isolates of Two Successful Multidrug-Resistant Clones of Salmonella enterica Serovar Typhimurium: Pandemic "DT 104" and pUO-StVR2. Microb Drug Resist. 2017;23(4):405–12. Epub 2016/11/05. doi: 10.1089/mdr.2016.0227 27809653.

27. Oliva M, Monno R, D'Addabbo P, Pesole G, Dionisi AM, Scrascia M, et al. A novel group of IncQ1 plasmids conferring multidrug resistance. Plasmid. 2017;89:22–6. Epub 2016/12/06. doi: 10.1016/j.plasmid.2016.11.005 27916622.

28. Lobato-Marquez D, Molina-Garcia L, Moreno-Cordoba I, Garcia-Del Portillo F, Diaz-Orejas R. Stabilization of the Virulence Plasmid pSLT of Salmonella Typhimurium by Three Maintenance Systems and Its Evaluation by Using a New Stability Test. Frontiers in molecular biosciences. 2016;3:66. Epub 2016/11/02. doi: 10.3389/fmolb.2016.00066 27800482; PubMed Central PMCID: PMC5065971.

29. Hooton SP, Timms AR, Cummings NJ, Moreton J, Wilson R, Connerton IF. The complete plasmid sequences of Salmonella enterica serovar Typhimurium U288. Plasmid. 2014;76:32–9. Epub 2014/09/02. doi: 10.1016/j.plasmid.2014.08.002 25175817.

30. Ilyas B, Tsai CN, Coombes BK. Evolution of Salmonella-Host Cell Interactions through a Dynamic Bacterial Genome. Frontiers in cellular and infection microbiology. 2017;7:428. Epub 2017/10/17. doi: 10.3389/fcimb.2017.00428 29034217; PubMed Central PMCID: PMC5626846.

31. Gerlach RG, Jackel D, Stecher B, Wagner C, Lupas A, Hardt WD, et al. Salmonella Pathogenicity Island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol. 2007;9(7):1834–50. doi: 10.1111/j.1462-5822.2007.00919.x 17388786.

32. Sana TG, Flaugnatti N, Lugo KA, Lam LH, Jacobson A, Baylot V, et al. Salmonella Typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc Natl Acad Sci U S A. 2016;113(34):E5044–51. Epub 2016/08/10. doi: 10.1073/pnas.1608858113 27503894; PubMed Central PMCID: PMC5003274.

33. Wheeler NE, Barquist L, Kingsley RA, Gardner PP. A profile-based method for identifying functional divergence of orthologous genes in bacterial genomes. Bioinformatics. 2016;32(23):3566–74. Epub 2016/08/10. doi: 10.1093/bioinformatics/btw518 27503221; PubMed Central PMCID: PMC5181535.

34. Wheeler NE, Gardner PP, Barquist L. Machine learning identifies signatures of host adaptation in the bacterial pathogen Salmonella enterica. PLoS genetics. 2018;14(5):e1007333–e. doi: 10.1371/journal.pgen.1007333 29738521.

35. Van Puyvelde S, Pickard D, Vandelannoote K, Heinz E, Barbe B, de Block T, et al. An African Salmonella Typhimurium ST313 sublineage with extensive drug-resistance and signatures of host adaptation. Nat Commun. 2019;10(1):4280. Epub 2019/09/21. doi: 10.1038/s41467-019-11844-z 31537784; PubMed Central PMCID: PMC6753159.

36. Boyd D, Peters GA, Cloeckaert A, Boumedine KS, Chaslus-Dancla E, Imberechts H, et al. Complete nucleotide sequence of a 43-kilobase genomic island associated with the multidrug resistance region of Salmonella enterica serovar Typhimurium DT104 and its identification in phage type DT120 and serovar Agona. J Bacteriol. 2001;183(19):5725–32. Epub 2001/09/07. doi: 10.1128/JB.183.19.5725-5732.2001 11544236; PubMed Central PMCID: PMC95465.

37. Branchu P, Charity OJ, Bawn M, Thilliez G, Dallman TJ, Petrovska L, et al. SGI-4 in Monophasic Salmonella Typhimurium ST34 Is a Novel ICE That Enhances Resistance to Copper. Front Microbiol. 2019;10:1118. Epub 2019/06/11. doi: 10.3389/fmicb.2019.01118 31178839; PubMed Central PMCID: PMC6543542.

38. Owen SV, Wenner N, Canals R, Makumi A, Hammarlof DL, Gordon MA, et al. Characterization of the Prophage Repertoire of African Salmonella Typhimurium ST313 Reveals High Levels of Spontaneous Induction of Novel Phage BTP1. Front Microbiol. 2017;8:235. doi: 10.3389/fmicb.2017.00235 28280485; PubMed Central PMCID: PMC5322425.

39. Summer EJ, Gonzalez CF, Carlisle T, Mebane LM, Cass AM, Savva CG, et al. Burkholderia cenocepacia phage BcepMu and a family of Mu-like phages encoding potential pathogenesis factors. J Mol Biol. 2004;340(1):49–65. Epub 2004/06/09. doi: 10.1016/j.jmb.2004.04.053 15184022.

40. Gymoese P, Sorensen G, Litrup E, Olsen JE, Nielsen EM, Torpdahl M. Investigation of Outbreaks of Salmonella enterica Serovar Typhimurium and Its Monophasic Variants Using Whole-Genome Sequencing, Denmark. Emerg Infect Dis. 2017;23(10):1631–9. Epub 2017/09/21. doi: 10.3201/eid2310.161248 28930002; PubMed Central PMCID: PMC5621559.

41. Sun J, Ke B, Huang Y, He D, Li X, Liang Z, et al. The molecular epidemiological characteristics and genetic diversity of salmonella typhimurium in Guangdong, China, 2007–2011. PLoS One. 2014;9(11):e113145. Epub 2014/11/08. doi: 10.1371/journal.pone.0113145 25380053; PubMed Central PMCID: PMC4224511.

42. Alikhan NF, Zhou Z, Sergeant MJ, Achtman M. A genomic overview of the population structure of Salmonella. PLoS Genet. 2018;14(4):e1007261. Epub 2018/04/06. doi: 10.1371/journal.pgen.1007261 29621240; PubMed Central PMCID: PMC5886390.

43. Lan R, Reeves PR, Octavia S. Population structure, origins and evolution of major Salmonella enterica clones. Infect Genet Evol. 2009;9(5):996–1005. Epub 2009/04/28. doi: 10.1016/j.meegid.2009.04.011 19393770.

44. Zhang S, Li S, Gu W, den Bakker H, Boxrud D, Taylor A, et al. Zoonotic Source Attribution of Salmonella enterica Serotype Typhimurium Using Genomic Surveillance Data, United States. Emerg Infect Dis. 2019;25(1):82–91. Epub 2018/12/19. doi: 10.3201/eid2501.180835 30561314; PubMed Central PMCID: PMC6302586.

45. Mather AE, Phuong TLT, Gao Y, Clare S, Mukhopadhyay S, Goulding DA, et al. New Variant of Multidrug-Resistant Salmonella enterica Serovar Typhimurium Associated with Invasive Disease in Immunocompromised Patients in Vietnam. mBio. 2018;9(5). Epub 2018/09/06. doi: 10.1128/mBio.01056-18 30181247; PubMed Central PMCID: PMC6123440.

46. Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, et al. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci U S A. 2015;112(18):5649–54. Epub 2015/03/21. doi: 10.1073/pnas.1503141112 25792457; PubMed Central PMCID: PMC4426470.

47. McEwen SA, Fedorka-Cray PJ. Antimicrobial use and resistance in animals. Clin Infect Dis. 2002;34 Suppl 3:S93–S106. Epub 2002/05/04. doi: 10.1086/340246 11988879.

48. Horton RA, Wu G, Speed K, Kidd S, Davies R, Coldham NG, et al. Wild birds carry similar Salmonella enterica serovar Typhimurium strains to those found in domestic animals and livestock. Res Vet Sci. 2013;95(1):45–8. doi: 10.1016/j.rvsc.2013.02.008 23481141.

49. Parsons BN, Humphrey S, Salisbury AM, Mikoleit J, Hinton JC, Gordon MA, et al. Invasive non-typhoidal Salmonella typhimurium ST313 are not host-restricted and have an invasive phenotype in experimentally infected chickens. PLoS Negl Trop Dis. 2013;7(10):e2487. doi: 10.1371/journal.pntd.0002487 24130915; PubMed Central PMCID: PMC3794976.

50. Okoro CK, Barquist L, Connor TR, Harris SR, Clare S, Stevens MP, et al. Signatures of adaptation in human invasive Salmonella Typhimurium ST313 populations from sub-Saharan Africa. PLoS Negl Trop Dis. 2015;9(3):e0003611. Epub 2015/03/25. doi: 10.1371/journal.pntd.0003611 25803844; PubMed Central PMCID: PMC4372345.

51. Carden SE, Walker GT, Honeycutt J, Lugo K, Pham T, Jacobson A, et al. Pseudogenization of the Secreted Effector Gene sseI Confers Rapid Systemic Dissemination of S. Typhimurium ST313 within Migratory Dendritic Cells. Cell Host Microbe. 2017;21(2):182–94. Epub 2017/02/10. doi: 10.1016/j.chom.2017.01.009 28182950; PubMed Central PMCID: PMC5325708.

52. Singletary LA, Karlinsey JE, Libby SJ, Mooney JP, Lokken KL, Tsolis RM, et al. Loss of Multicellular Behavior in Epidemic African Nontyphoidal Salmonella enterica Serovar Typhimurium ST313 Strain D23580. mBio. 2016;7(2):e02265. doi: 10.1128/mBio.02265-15 26933058; PubMed Central PMCID: PMC4810497.

53. Feasey NA, Hadfield J, Keddy KH, Dallman TJ, Jacobs J, Deng X, et al. Distinct Salmonella Enteritidis lineages associated with enterocolitis in high-income settings and invasive disease in low-income settings. Nat Genet. 2016;48(10):1211–7. Epub 2016/08/23. doi: 10.1038/ng.3644 27548315; PubMed Central PMCID: PMC5047355.

54. Abraham S, O'Dea M, Trott DJ, Abraham RJ, Hughes D, Pang S, et al. Isolation and plasmid characterization of carbapenemase (IMP-4) producing Salmonella enterica Typhimurium from cats. Sci Rep. 2016;6:35527. Epub 2016/10/22. doi: 10.1038/srep35527 27767038; PubMed Central PMCID: PMC5073282 Neoculi. All other authors have none to declare.

55. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D, Wain J, et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature. 2001;413(6858):848–52. doi: 10.1038/35101607 11677608.

56. Holt KE, Thomson NR, Wain J, Langridge GC, Hasan R, Bhutta ZA, et al. Pseudogene accumulation in the evolutionary histories of Salmonella enterica serovars Paratyphi A and Typhi. BMC Genomics. 2009;10:36. doi: 10.1186/1471-2164-10-36 19159446.

57. Zhou Z, McCann A, Weill FX, Blin C, Nair S, Wain J, et al. Transient Darwinian selection in Salmonella enterica serovar Paratyphi A during 450 years of global spread of enteric fever. Proc Natl Acad Sci U S A. 2014;111(33):12199–204. Epub 2014/08/06. doi: 10.1073/pnas.1411012111 25092320; PubMed Central PMCID: PMC4143038.

58. Threlfall EJ. Epidemic Salmonella typhimurium DT 104—a truly international multiresistant clone. Journal of Antimicrobial Chemotherapy. 2000;46(1):7–10. doi: 10.1093/jac/46.1.7 WOS:000089125100002. 10882682

59. Collier-Hyams LS, Zeng H, Sun J, Tomlinson AD, Bao ZQ, Chen H, et al. Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J Immunol. 2002;169(6):2846–50. Epub 2002/09/10. doi: 10.4049/jimmunol.169.6.2846 12218096.

60. Yang Z, Soderholm A, Lung TW, Giogha C, Hill MM, Brown NF, et al. SseK3 Is a Salmonella Effector That Binds TRIM32 and Modulates the Host's NF-kappaB Signalling Activity. PLoS One. 2015;10(9):e0138529. Epub 2015/09/24. doi: 10.1371/journal.pone.0138529 26394407; PubMed Central PMCID: PMC4579058.

61. Geng S, Wang Y, Xue Y, Wang H, Cai Y, Zhang J, et al. The SseL protein inhibits the intracellular NF-kappaB pathway to enhance the virulence of Salmonella Pullorum in a chicken model. Microb Pathog. 2019;129:1–6. Epub 2019/02/01. doi: 10.1016/j.micpath.2019.01.035 30703474.

62. Nuccio S-P, Bäumler AJ. Comparative Analysis of Salmonella Genomes Identifies a Metabolic Network for Escalating Growth in the Inflamed Gut. mBio. 2014;5(2). doi: 10.1128/mBio.00929-14 24643865

63. Johnson R, Mylona E, Frankel G. Typhoidal Salmonella: Distinctive virulence factors and pathogenesis. Cell Microbiol. 2018;20(9):e12939. Epub 2018/07/22. doi: 10.1111/cmi.12939 30030897.

64. Kingsley RA, Humphries AD, Weening EH, De Zoete MR, Winter S, Papaconstantinopoulou A, et al. Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype typhimurium: identification of intestinal colonization and persistence determinants. Infect Immun. 2003;71(2):629–40. doi: 10.1128/iai.71.2.629-640.2003 12540539.

65. Bäumler AJ, Tsolis RM, Bowe F, Kusters JG, Hoffmann S, Heffron F. The pef fimbrial operon mediates adhesion to murine small intestine and is necessary for fluid accumulation in infant mice. Infect Immun. 1996;64:61–8. 8557375

66. Weening EH, Barker JD, Laarakker MC, Humphries AD, Tsolis RM, Baumler AJ. The Salmonella enterica serotype Typhimurium lpf, bcf, stb, stc, std, and sth fimbrial operons are required for intestinal persistence in mice. Infect Immun. 2005;73(6):3358–66. doi: 10.1128/IAI.73.6.3358-3366.2005 15908362.

67. Winter SE, Thiennimitr P, Winter MG, Butler BP, Huseby DL, Crawford RW, et al. Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature. 2010;467(7314):426–9. Epub 2010/09/25. doi: 10.1038/nature09415 [pii] 20864996; PubMed Central PMCID: PMC2946174.

68. Rivera-Chavez F, Lopez CA, Zhang LF, Garcia-Pastor L, Chavez-Arroyo A, Lokken KL, et al. Energy Taxis toward Host-Derived Nitrate Supports a Salmonella Pathogenicity Island 1-Independent Mechanism of Invasion. mBio. 2016;7(4). Epub 2016/07/21. doi: 10.1128/mBio.00960-16 27435462; PubMed Central PMCID: PMC4958259.

69. Bourret TJ, Liu L, Shaw JA, Husain M, Vazquez-Torres A. Magnesium homeostasis protects Salmonella against nitrooxidative stress. Sci Rep. 2017;7(1):15083. Epub 2017/11/10. doi: 10.1038/s41598-017-15445-y 29118452; PubMed Central PMCID: PMC5678156.

70. MacKenzie KD, Wang Y, Musicha P, Hansen EG, Palmer MB, Herman DJ, et al. Parallel evolution leading to impaired biofilm formation in invasive Salmonella strains. PLoS Genet. 2019;15(6):e1008233. Epub 2019/06/25. doi: 10.1371/journal.pgen.1008233 31233504; PubMed Central PMCID: PMC6611641.

71. Gonzales AM, Wilde S, Roland KL. New Insights into the Roles of Long Polar Fimbriae and Stg Fimbriae in Salmonella Interactions with Enterocytes and M Cells. Infect Immun. 2017;85(9). Epub 2017/06/21. doi: 10.1128/iai.00172-17 28630073; PubMed Central PMCID: PMC5563581.

72. Bäumler AJ, Tsolis RM, Heffron F. The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer's patches. Proc Natl Acad Sci USA. 1996;93:279–83. doi: 10.1073/pnas.93.1.279 8552622

73. Lloyd SJ, Ritchie JM, Rojas-Lopez M, Blumentritt CA, Popov VL, Greenwich JL, et al. A double, long polar fimbria mutant of Escherichia coli O157:H7 expresses Curli and exhibits reduced in vivo colonization. Infect Immun. 2012;80(3):914–20. Epub 2012/01/11. doi: 10.1128/IAI.05945-11 22232190; PubMed Central PMCID: PMC3294650.

74. Ledeboer NA, Frye JG, McClelland M, Jones BD. Salmonella enterica Serovar Typhimurium Requires the Lpf, Pef, and Tafi Fimbriae for Biofilm Formation on HEp-2 Tissue Culture Cells and Chicken Intestinal Epithelium. Infection and Immunity. 2006;74(6):3156–69. doi: 10.1128/IAI.01428-05 PMC1479237. 16714543

75. Nakato G, Fukuda S, Hase K, Goitsuka R, Cooper MD, Ohno H. New approach for m-cell-specific molecules screening by comprehensive transcriptome analysis. DNA Res. 2009;16(4):227–35. Epub 2009/08/14. doi: 10.1093/dnares/dsp013 19675110; PubMed Central PMCID: PMC2725790.

76. Kozuka Y, Nasu T, Murakami T, Yasuda M. Comparative studies on the secondary lymphoid tissue areas in the chicken bursa of Fabricius and calf ileal Peyer's patch. Vet Immunol Immunopathol. 2010;133(2–4):190–7. Epub 2009/09/09. doi: 10.1016/j.vetimm.2009.08.003 19735947.

77. Spano S, Galan JE. A Rab32-dependent pathway contributes to Salmonella typhi host restriction. Science. 2012;338(6109):960–3. Epub 2012/11/20. doi: 10.1126/science.1229224 23162001; PubMed Central PMCID: PMC3693731.

78. Wu H, Jones RM, Neish AS. The Salmonella effector AvrA mediates bacterial intracellular survival during infection in vivo. Cell Microbiol. 2012;14(1):28–39. Epub 2011/09/09. doi: 10.1111/j.1462-5822.2011.01694.x 21899703; PubMed Central PMCID: PMC3240734.

79. Du F, Galan JE. Selective inhibition of type III secretion activated signaling by the Salmonella effector AvrA. PLoS Pathog. 2009;5(9):e1000595. Epub 2009/09/26. doi: 10.1371/journal.ppat.1000595 19779561; PubMed Central PMCID: PMC2742890.

80. Günster RA, Matthews SA, Holden DW, Thurston TLM. SseK1 and SseK3 Type III Secretion System Effectors Inhibit NF-κB Signaling and Necroptotic Cell Death in <span class = "named-content genus-species" id = "named-content-1">Salmonella-Infected Macrophages. Infection and Immunity. 2017;85(3).

81. Rodriguez-Valera F, Martin-Cuadrado AB, Rodriguez-Brito B, Pasic L, Thingstad TF, Rohwer F, et al. Explaining microbial population genomics through phage predation. Nat Rev Microbiol. 2009;7(11):828–36. Epub 2009/10/17. doi: 10.1038/nrmicro2235 19834481.

82. Mottawea W, Duceppe MO, Dupras AA, Usongo V, Jeukens J, Freschi L, et al. Salmonella enterica Prophage Sequence Profiles Reflect Genome Diversity and Can Be Used for High Discrimination Subtyping. Front Microbiol. 2018;9:836. Epub 2018/05/22. doi: 10.3389/fmicb.2018.00836 29780368; PubMed Central PMCID: PMC5945981.

83. Figueroa-Bossi N, Uzzau S, Maloriol D, Bossi L. Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. Mol Microbiol. 2001;39(2):260–72. doi: 10.1046/j.1365-2958.2001.02234.x 11136448

84. Bossi L, Fuentes JA, Mora G, Figueroa-Bossi N. Prophage contribution to bacterial population dynamics. J Bacteriol. 2003;185(21):6467–71. Epub 2003/10/18. doi: 10.1128/jb.185.21.6467-6471.2003 14563883; PubMed Central PMCID: PMC219396.

85. Hawkey J, Edwards DJ, Dimovski K, Hiley L, Billman-Jacobe H, Hogg G, et al. Evidence of microevolution of Salmonella Typhimurium during a series of egg-associated outbreaks linked to a single chicken farm. BMC Genomics. 2013;14:800. Epub 2013/11/20. doi: 10.1186/1471-2164-14-800 24245509; PubMed Central PMCID: PMC3870983.

86. Zeder MA. Domestication and early agriculture in the Mediterranean Basin: Origins, diffusion, and impact. Proc Natl Acad Sci U S A. 2008;105(33):11597–604. Epub 2008/08/14. doi: 10.1073/pnas.0801317105 18697943; PubMed Central PMCID: PMC2575338.

87. Petrovska L, Mather AE, AbuOun M, Branchu P, Harris SR, Connor T, et al. Microevolution of Monophasic Salmonella Typhimurium during Epidemic, United Kingdom, 2005–2010. Emerging Infectious Diseases. 2016;22(4):617–24. doi: 10.3201/eid2204.150531 PMC4806966. 26982594

88. Kroger C, Dillon SC, Cameron AD, Papenfort K, Sivasankaran SK, Hokamp K, et al. The transcriptional landscape and small RNAs of Salmonella enterica serovar Typhimurium. Proc Natl Acad Sci U S A. 2012;109(20):E1277–86. Epub 2012/04/28. doi: 10.1073/pnas.1201061109 22538806; PubMed Central PMCID: PMC3356629.

89. Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE, Gordon MA, et al. Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome research. 2009;19(12):2279–87. Epub 2009/11/11. doi: 10.1101/gr.091017.109 19901036; PubMed Central PMCID: PMC2792184.

90. Kingsley RA, Kay S, Connor T, Barquist L, Sait L, Holt KE, et al. Genome and transcriptome adaptation accompanying emergence of the definitive type 2 host-restricted Salmonella enterica serovar Typhimurium pathovar. MBio. 2013;4(5):e00565–13. Epub 2013/08/29. doi: 10.1128/mBio.00565-13 23982073; PubMed Central PMCID: PMC3760250.

91. Makendi C, Page AJ, Wren BW, Le Thi Phuong T, Clare S, Hale C, et al. A Phylogenetic and Phenotypic Analysis of Salmonella enterica Serovar Weltevreden, an Emerging Agent of Diarrheal Disease in Tropical Regions. PLoS Negl Trop Dis. 2016;10(2):e0004446. Epub 2016/02/13. doi: 10.1371/journal.pntd.0004446 26867150; PubMed Central PMCID: PMC4750946.

92. Zerbino D, Birney E. Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Research. 2008;18(5):821–9. velvet-2008. doi: 10.1101/gr.074492.107 18349386

93. Zerbino DR. Using the Velvet de novo assembler for short-read sequencing technologies. Current protocols in bioinformatics. 2010;Chapter 11:Unit 11.5. Epub 2010/09/14. doi: 10.1002/0471250953.bi1105s31 20836074; PubMed Central PMCID: PMC2952100.

94. Page AJ, De Silva N, Hunt M, Quail MA, Parkhill J, Harris SR, et al. Robust high-throughput prokaryote de novo assembly and improvement pipeline for Illumina data. Microb Genom. 2016;2(8):e000083. Epub 2017/03/30. doi: 10.1099/mgen.0.000083 28348874; PubMed Central PMCID: PMC5320598.

95. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics. 2011;27(4):578–9. Epub 2010/12/15. doi: 10.1093/bioinformatics/btq683 21149342.

96. Nadalin F, Vezzi F, Policriti A. GapFiller: a de novo assembly approach to fill the gap within paired reads. BMC Bioinformatics. 2012;13(14):1–16. doi: 10.1186/1471-2105-13-s14-s8 23095524

97. Kolmogorov M, Raney B, Paten B, Pham S. Ragout-a reference-assisted assembly tool for bacterial genomes. Bioinformatics. 2014;30(12):i302–9. Epub 2014/06/17. doi: 10.1093/bioinformatics/btu280 24931998; PubMed Central PMCID: PMC4058940.

98. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–9. doi: 10.1093/bioinformatics/btu153 24642063

99. Li H. Minimap and miniasm: fast mapping and de novo assembly for noisy long sequences. Bioinformatics. 2016;32(14):2103–10. doi: 10.1093/bioinformatics/btw152 27153593

100. Sommer DD, Delcher AL, Salzberg SL, Pop M. Minimus: a fast, lightweight genome assembler. BMC Bioinformatics. 2007;8(1):64. doi: 10.1186/1471-2105-8-64 17324286

101. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T, Keane JA, et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom. 2016;2(4):e000056. Epub 2017/03/30. doi: 10.1099/mgen.0.000056 28348851; PubMed Central PMCID: PMC5320690.

102. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22(21):2688–90. raxml-2006. doi: 10.1093/bioinformatics/btl446 16928733

103. Almeida F, Seribelli AA, Medeiros MIC, Rodrigues DdP, MelloVarani Ad, Luo Y, et al. Phylogenetic and antimicrobial resistance gene analysis of Salmonella Typhimurium strains isolated in Brazil by whole genome sequencing. PLOS ONE. 2018;13(8):e0201882. doi: 10.1371/journal.pone.0201882 30102733

104. Hayden HS, Matamouros S, Hager KR, Brittnacher MJ, Rohmer L, Radey MC, et al. Genomic Analysis of Salmonella enterica Serovar Typhimurium Characterizes Strain Diversity for Recent U.S. Salmonellosis Cases and Identifies Mutations Linked to Loss of Fitness under Nitrosative and Oxidative Stress. mBio. 2016;7(2). doi: 10.1128/mBio.00154-16 26956590

105. Hunt M, Mather AE, Sánchez-Busó L, Page AJ, Parkhill J, Keane JA, et al. ARIBA: rapid antimicrobial resistance genotyping directly from sequencing reads. 2017. doi: 10.1101/118000

106. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67(11):2640–4. Epub 2012/07/12. doi: 10.1093/jac/dks261 22782487; PubMed Central PMCID: PMC3468078.

107. Chen L, Zheng D, Liu B, Yang J, Jin Q. VFDB 2016: hierarchical and refined dataset for big data analysis—10 years on. Nucleic Acids Res. 2016;44(D1):D694–7. Epub 2015/11/19. doi: 10.1093/nar/gkv1239 26578559; PubMed Central PMCID: PMC4702877.

108. Carattoli A, Zankari E, Garcia-Fernandez A, Voldby Larsen M, Lund O, Villa L, et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58(7):3895–903. Epub 2014/04/30. doi: 10.1128/AAC.02412-14 24777092; PubMed Central PMCID: PMC4068535.

109. Inouye M, Dashnow H, Raven LA, Schultz MB, Pope BJ, Tomita T, et al. SRST2: Rapid genomic surveillance for public health and hospital microbiology labs. Genome Med. 2014;6(11):90. Epub 2014/11/26. doi: 10.1186/s13073-014-0090-6 25422674; PubMed Central PMCID: PMC4237778.

110. Otto TD, Dillon GP, Degrave WS, Berriman M. RATT: Rapid Annotation Transfer Tool. Nucleic Acids Res. 2011;39(9):e57. Epub 2011/02/11. doi: 10.1093/nar/gkq1268 21306991; PubMed Central PMCID: PMC3089447.

111. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. ACT: the Artemis Comparison Tool. Bioinformatics. 2005;21(16):3422–3. doi: 10.1093/bioinformatics/bti553 15976072.

112. El-Gebali S, Mistry J, Bateman A, Eddy SR, Luciani A, Potter SC, et al. The Pfam protein families database in 2019. Nucleic Acids Research. 2018:gky995–gky. doi: 10.1093/nar/gky995 30357350

113. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res. 2011;39(Web Server issue):W29–37. Epub 2011/05/20. doi: 10.1093/nar/gkr367 21593126; PubMed Central PMCID: PMC3125773.

114. Arndt D, Marcu A, Liang Y, Wishart DS. PHAST, PHASTER and PHASTEST: Tools for finding prophage in bacterial genomes. Brief Bioinform. 2017. Epub 2017/10/14. doi: 10.1093/bib/bbx121 29028989.

115. Croucher NJ, Page AJ, Connor TR, Delaney AJ, Keane JA, Bentley SD, et al. Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Research. 2015;43(3):e15–e. doi: 10.1093/nar/gku1196 25414349

116. Hadfield J, Croucher NJ, Goater RJ, Abudahab K, Aanensen DM, Harris SR. Phandango: an interactive viewer for bacterial population genomics. Bioinformatics. 2017. Epub 2017/10/14. doi: 10.1093/bioinformatics/btx610 29028899; PubMed Central PMCID: PMC5860215.

117. Didelot X, Wilson DJ. ClonalFrameML: Efficient Inference of Recombination in Whole Bacterial Genomes. PLOS Computational Biology. 2015;11(2):e1004041. doi: 10.1371/journal.pcbi.1004041 25675341

118. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MT, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31(22):3691–3. Epub 2015/07/23. doi: 10.1093/bioinformatics/btv421 26198102; PubMed Central PMCID: PMC4817141.

119. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, et al. Versatile and open software for comparing large genomes. Genome Biol. 2004;5(2):R12. doi: 10.1186/gb-2004-5-2-r12 14759262.

120. Adriaenssens E, Brister JR. How to Name and Classify Your Phage: An Informal Guide. Viruses. 2017;9(4). Epub 2017/04/04. doi: 10.3390/v9040070 28368359; PubMed Central PMCID: PMC5408676.

121. Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28(23):3150–2. doi: 10.1093/bioinformatics/bts565 23060610; PubMed Central PMCID: PMC3516142.

122. Agren J, Sundstrom A, Hafstrom T, Segerman B. Gegenees: fragmented alignment of multiple genomes for determining phylogenomic distances and genetic signatures unique for specified target groups. PLoS One. 2012;7(6):e39107. Epub 2012/06/23. doi: 10.1371/journal.pone.0039107 22723939; PubMed Central PMCID: PMC3377601.

123. Bin Jang H, Bolduc B, Zablocki O, Kuhn JH, Roux S, Adriaenssens EM, et al. Taxonomic assignment of uncultivated prokaryotic virus genomes is enabled by gene-sharing networks. Nat Biotechnol. 2019;37(6):632–9. Epub 2019/05/08. doi: 10.1038/s41587-019-0100-8 31061483.

124. O'Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res. 2016;44(D1):D733–45. Epub 2015/11/11. doi: 10.1093/nar/gkv1189 26553804; PubMed Central PMCID: PMC4702849.

125. Buchfink B, Xie C, Huson DH. Fast and sensitive protein alignment using DIAMOND. Nature methods. 2015;12(1):59–60. Epub 2014/11/18. doi: 10.1038/nmeth.3176 25402007.

126. Enright AJ, Van Dongen S, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 2002;30(7):1575–84. doi: 10.1093/nar/30.7.1575 11917018; PubMed Central PMCID: PMC101833.

127. Nepusz T, Yu H, Paccanaro A. Detecting overlapping protein complexes in protein-protein interaction networks. Nat Methods. 2012;9(5):471–2. Epub 2012/03/20. doi: 10.1038/nmeth.1938 22426491; PubMed Central PMCID: PMC3543700.

128. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13(11):2498–504. Epub 2003/11/05. doi: 10.1101/gr.1239303 14597658; PubMed Central PMCID: PMC403769.

129. Antipov D, Hartwick N, Shen M, Raiko M, Lapidus A, Pevzner PA. plasmidSPAdes: assembling plasmids from whole genome sequencing data. Bioinformatics. 2016;32(22):3380–7. Epub 2016/07/29. doi: 10.1093/bioinformatics/btw493 27466620.

130. Yoshida CE, Kruczkiewicz P, Laing CR, Lingohr EJ, Gannon VP, Nash JH, et al. The Salmonella In Silico Typing Resource (SISTR): An Open Web-Accessible Tool for Rapidly Typing and Subtyping Draft Salmonella Genome Assemblies. PLoS One. 2016;11(1):e0147101. Epub 2016/01/23. doi: 10.1371/journal.pone.0147101 26800248; PubMed Central PMCID: PMC4723315.

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