1887
  1. Home
  2. Eurosurveillance
  3. Volume 25, Issue 20, 21/May/2020
  4. Article
Research Open Access
Like 0
Download

Abstract

Background

Both long- and short-term epidemiology are fundamental to disease control and require accurate bacterial typing. Genomic data resulting from implementation of whole genome sequencing in many public health laboratories can potentially provide highly sensitive and accurate descriptions of strain relatedness. Previous typing efforts using these data have mainly focussed on outbreak detection.

Aim

We aimed to develop multilevel genome typing (MGT), using consecutive multilocus sequence typing (MLST) schemes of increasing sizes, stepping up from seven-gene MLST to core genome MLST, to allow examination of genetic relatedness at multiple resolution levels.

Methods

The system was applied to serovar Typhimurium. The MLST scheme used at each step (MGT level), defined a given MGT-level specific sequence type (ST). The list of STs generated from all of these increasing MGT levels, was named a genome type (GT). Using MGT, we typed 9,096 previously characterised isolates with publicly available data.

Results

Our approach could identify previously described Typhimurium populations, such as the DT104 multidrug resistance lineage (GT 19-2-11) and two invasive lineages of African isolates (GT 313-2-3 and 313-2-752). Further, we showed that MGT-derived clusters can accurately distinguish five outbreaks from each other and five background isolates.

Conclusion

MGT provides a universal and stable nomenclature at multiple resolutions for . Typhimurium strains and could be implemented as an internationally standardised strain identification system. While established so far only for Typhimurium, the results here suggest that MGT could form the basis for typing systems in other similar microorganisms.

© Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2020.25.20.1900519
2020-05-21
2024-11-13
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2020.25.20.1900519
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/25/20/eurosurv-25-20-3.html?itemId=/content/10.2807/1560-7917.ES.2020.25.20.1900519&mimeType=html&fmt=ahah

References

  1. Köser CU, Holden MT, Ellington MJ, Cartwright EJ, Brown NM, Ogilvy-Stuart AL, et al. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med. 2012;366(24):2267-75.  https://doi.org/10.1056/NEJMoa1109910  PMID: 22693998 
  2. Walker TM, Ip CL, Harrell RH, Evans JT, Kapatai G, Dedicoat MJ, et al. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis. 2013;13(2):137-46.  https://doi.org/10.1016/S1473-3099(12)70277-3  PMID: 23158499 
  3. Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA, Dance D, et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci USA. 2015;112(27):E3574-81.  https://doi.org/10.1073/pnas.1501049112  PMID: 26100894 
  4. Hu D, Liu B, Feng L, Ding P, Guo X, Wang M, et al. Origins of the current seventh cholera pandemic. Proc Natl Acad Sci USA. 2016;113(48):E7730-9.  https://doi.org/10.1073/pnas.1608732113  PMID: 27849586 
  5. Sabat AJ, Budimir A, Nashev D, Sá-Leão R, van Dijl J, Laurent F, et al. Overview of molecular typing methods for outbreak detection and epidemiological surveillance. Euro Surveill. 2013;18(4):20380.  https://doi.org/10.2807/ese.18.04.20380-en  PMID: 23369389 
  6. Wattiau P, Boland C, Bertrand S. Methodologies for Salmonella enterica subsp. enterica subtyping: gold standards and alternatives. Appl Environ Microbiol. 2011;77(22):7877-85.  https://doi.org/10.1128/AEM.05527-11  PMID: 21856826 
  7. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA. 1998;95(6):3140-5.  https://doi.org/10.1073/pnas.95.6.3140  PMID: 9501229 
  8. Achtman M, Wain J, Weill FX, Nair S, Zhou Z, Sangal V, et al. S. Enterica MLST Study Group. Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog. 2012;8(6):e1002776.  https://doi.org/10.1371/journal.ppat.1002776  PMID: 22737074 
  9. Pérez-Losada M, Arenas M, Castro-Nallar E. Microbial sequence typing in the genomic era. Infect Genet Evol. 2018;63:346-59.  https://doi.org/10.1016/j.meegid.2017.09.022  PMID: 28943406 
  10. Yap KP, Ho WS, Gan HM, Chai LC, Thong KL. Global MLST of Salmonella Typhi Revisited in Post-genomic Era: Genetic Conservation, Population Structure, and Comparative Genomics of Rare Sequence Types. Front Microbiol. 2016;7(e1002776):270.  https://doi.org/10.3389/fmicb.2016.00270  PMID: 26973639 
  11. Octavia S, Wang Q, Tanaka MM, Kaur S, Sintchenko V, Lan R. Delineating community outbreaks of Salmonella enterica serovar Typhimurium by use of whole-genome sequencing: insights into genomic variability within an outbreak. J Clin Microbiol. 2015;53(4):1063-71.  https://doi.org/10.1128/JCM.03235-14  PMID: 25609719 
  12. Fu S, Octavia S, Tanaka MM, Sintchenko V, Lan R. Defining the Core Genome of Salmonella enterica Serovar Typhimurium for Genomic Surveillance and Epidemiological Typing. J Clin Microbiol. 2015;53(8):2530-8.  https://doi.org/10.1128/JCM.03407-14  PMID: 26019201 
  13. Mather AE, Reid SW, 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.  https://doi.org/10.1126/science.1240578  PMID: 24030491 
  14. Eyre DW, Cule ML, Wilson DJ, Griffiths D, Vaughan A, O’Connor L, et al. Diverse sources of C. difficile infection identified on whole-genome sequencing. N Engl J Med. 2013;369(13):1195-205.  https://doi.org/10.1056/NEJMoa1216064  PMID: 24066741 
  15. Jolley KA, Maiden MC. BIGSdb: Scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics. 2010;11(1):595.  https://doi.org/10.1186/1471-2105-11-595  PMID: 21143983 
  16. Mellmann A, Harmsen D, Cummings CA, Zentz EB, Leopold SR, Rico A, et al. Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PLoS One. 2011;6(7):e22751.  https://doi.org/10.1371/journal.pone.0022751  PMID: 21799941 
  17. Cody AJ, McCarthy ND, Jansen van Rensburg M, Isinkaye T, Bentley SD, Parkhill J, et al. Real-time genomic epidemiological evaluation of human Campylobacter isolates by use of whole-genome multilocus sequence typing. J Clin Microbiol. 2013;51(8):2526-34.  https://doi.org/10.1128/JCM.00066-13  PMID: 23698529 
  18. Kluytmans-van den Bergh MF, Rossen JW, Bruijning-Verhagen PC, Bonten MJ, Friedrich AW, Vandenbroucke-Grauls CM, et al. Whole-Genome Multilocus Sequence Typing of Extended-Spectrum-Beta-Lactamase-Producing Enterobacteriaceae. J Clin Microbiol. 2016;54(12):2919-27.  https://doi.org/10.1128/JCM.01648-16  PMID: 27629900 
  19. Moura A, Criscuolo A, Pouseele H, Maury MM, Leclercq A, Tarr C, et al. Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat Microbiol. 2016;2(2):16185.  https://doi.org/10.1038/nmicrobiol.2016.185  PMID: 27723724 
  20. Maiden MC, Jansen van Rensburg MJ, Bray JE, Earle SG, Ford SA, Jolley KA, et al. MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol. 2013;11(10):728-36.  https://doi.org/10.1038/nrmicro3093  PMID: 23979428 
  21. Sheppard SK, Jolley KA, Maiden MC. A Gene-By-Gene Approach to Bacterial Population Genomics: Whole Genome MLST of Campylobacter. Genes (Basel). 2012;3(2):261-77.  https://doi.org/10.3390/genes3020261  PMID: 24704917 
  22. Pearce ME, Alikhan NF, Dallman TJ, Zhou Z, Grant K, Maiden MCJ. Comparative analysis of core genome MLST and SNP typing within a European Salmonella serovar Enteritidis outbreak. Int J Food Microbiol. 2018;274:1-11.  https://doi.org/10.1016/j.ijfoodmicro.2018.02.023  PMID: 29574242 
  23. Ashton P, Nair S, Peters T, Tewolde R, Day M, Doumith M, et al. Revolutionising Public Health Reference Microbiology using Whole Genome Sequencing: Salmonella as an exemplar. Preprint at https://wwwbiorxivorg/content/early/2015/11/29/033225. 2015.
  24. Zhou Z, Alikhan N-F, Mohamed K, Achtman M. The user’s guide to comparative genomics with EnteroBase. Three case studies: micro-clades within Salmonella enterica serovar Agama, ancient and modern populations of Yersinia pestis, and core genomic diversity of all Escherichia. bioRxiv. 2019;613554.
  25. Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, et al. 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. 2011;8(8):887-900.  https://doi.org/10.1089/fpd.2010.0787  PMID: 21492021 
  26. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol. 2004;186(5):1518-30.  https://doi.org/10.1128/JB.186.5.1518-1530.2004  PMID: 14973027 
  27. Alikhan NF, Zhou Z, Sergeant MJ, Achtman M. A genomic overview of the population structure of Salmonella. PLoS Genet. 2018;14(4):e1007261.  https://doi.org/10.1371/journal.pgen.1007261  PMID: 29621240 
  28. Desai PT, Porwollik S, Long F, Cheng P, Wollam A, Bhonagiri-Palsikar V, et al. Evolutionary Genomics of Salmonella enterica Subspecies. MBio. 2013;4(2):e00579-12.  https://doi.org/10.1128/mBio.00579-12  PMID: 23462113 
  29. 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.  https://doi.org/10.1093/bioinformatics/btv421  PMID: 26198102 
  30. Caspi R, Billington R, Ferrer L, Foerster H, Fulcher CA, Keseler IM, et al. The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases. Nucleic Acids Res. 2016;44(D1):D471-80.  https://doi.org/10.1093/nar/gkv1164  PMID: 26527732 
  31. Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, et al. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics. 2010;26(13):1608-15.  https://doi.org/10.1093/bioinformatics/btq249  PMID: 20472543 
  32. Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8(10):785-6.  https://doi.org/10.1038/nmeth.1701  PMID: 21959131 
  33. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol. 2001;305(3):567-80.  https://doi.org/10.1006/jmbi.2000.4315  PMID: 11152613 
  34. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, et al. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res. 2005;33(17):5691-702.  https://doi.org/10.1093/nar/gki866  PMID: 16214803 
  35. Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang Y, et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 2016;44(W1):W16-21.  https://doi.org/10.1093/nar/gkw387  PMID: 27141966 
  36. Zhou Y, Liang Y, Lynch KH, Dennis JJ, Wishart DS. PHAST: a fast phage search tool. Nucleic Acids Res. 2011;39(Web Server issue):W347-52.
  37. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999;27(2):573-80.  https://doi.org/10.1093/nar/27.2.573  PMID: 9862982 
  38. Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA. BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics. 2011;12(1):402.  https://doi.org/10.1186/1471-2164-12-402  PMID: 21824423 
  39. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol. 2014;15(3):R46.  https://doi.org/10.1186/gb-2014-15-3-r46  PMID: 24580807 
  40. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114-20.  https://doi.org/10.1093/bioinformatics/btu170  PMID: 24695404 
  41. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 2009;25(14):1754-60.  https://doi.org/10.1093/bioinformatics/btp324  PMID: 19451168 
  42. Magoč T, Salzberg SL. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics. 2011;27(21):2957-63.  https://doi.org/10.1093/bioinformatics/btr507  PMID: 21903629 
  43. Song L, Florea L, Langmead B. Lighter: fast and memory-efficient sequencing error correction without counting. Genome Biol. 2014;15(11):509.  https://doi.org/10.1186/s13059-014-0509-9  PMID: 25398208 
  44. Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014;9(11):e112963.  https://doi.org/10.1371/journal.pone.0112963  PMID: 25409509 
  45. Souvorov A, Agarwala R, Lipman DJ. SKESA: strategic k-mer extension for scrupulous assemblies. Genome Biol. 2018;19(1):153.  https://doi.org/10.1186/s13059-018-1540-z  PMID: 30286803 
  46. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072-5.  https://doi.org/10.1093/bioinformatics/btt086  PMID: 23422339 
  47. 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.  https://doi.org/10.1371/journal.pone.0147101  PMID: 26800248 
  48. Robertson J, Yoshida C, Kruczkiewicz P, Nadon C, Nichani A, Taboada EN, et al. Comprehensive assessment of the quality of Salmonella whole genome sequence data available in public sequence databases using the Salmonella in silico Typing Resource (SISTR). Microb Genom. 2018;4(2).  https://doi.org/10.1099/mgen.0.000151  PMID: 29338812 
  49. Zhou Z, Alikhan NF, Sergeant MJ, Luhmann N, Vaz C, Francisco AP, et al. GrapeTree: visualization of core genomic relationships among 100,000 bacterial pathogens. Genome Res. 2018;28(9):1395-404.  https://doi.org/10.1101/gr.232397.117  PMID: 30049790 
  50. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016;33(7):1870-4.  https://doi.org/10.1093/molbev/msw054  PMID: 27004904 
  51. 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.  https://doi.org/10.1038/ng.2423  PMID: 23023330 
  52. Ashton PM, Owen SV, Kaindama L, Rowe WPM, Lane CR, Larkin L, et al. Public health surveillance in the UK revolutionises our understanding of the invasive Salmonella Typhimurium epidemic in Africa. Genome Med. 2017;9(1):92.  https://doi.org/10.1186/s13073-017-0480-7  PMID: 29084588 
  53. 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.  https://doi.org/10.1128/AEM.03821-15  PMID: 26944846 
  54. Bloomfield SJ, Benschop J, Biggs PJ, Marshall JC, Hayman DTS, Carter PE, et al. Genomic Analysis of Salmonella enterica Serovar Typhimurium DT160 Associated with a 14-Year Outbreak, New Zealand, 1998-2012. Emerg Infect Dis. 2017;23(6):906-13.  https://doi.org/10.3201/eid2306.161934  PMID: 28516864 
  55. Snitkin ES, Zelazny AM, Thomas PJ, Stock F, Henderson DK, Palmore TN, et al. NISC Comparative Sequencing Program Group. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med. 2012;4(148):148ra116.  https://doi.org/10.1126/scitranslmed.3004129  PMID: 22914622 
  56. 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.  https://doi.org/10.1371/currents.outbreaks.2c05a47d292f376afc5a6fcdd8a7a3b6  PMID: 25713745 
Multilevel genome typing: genomics-guided scalable resolution typing of microbial pathogens
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Michael+Payne&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Payne Michael</a>, <a href="/search?value1=Sandeep+Kaur&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Kaur Sandeep</a>, <a href="/search?value1=Qinning+Wang&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Wang Qinning</a>, <a href="/search?value1=Daneeta+Hennessy&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Hennessy Daneeta</a>, <a href="/search?value1=Lijuan+Luo&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Luo Lijuan</a>, <a href="/search?value1=Sophie+Octavia&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Octavia Sophie</a>, <a href="/search?value1=Mark+M.+Tanaka&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Tanaka Mark M.</a>, <a href="/search?value1=Vitali+Sintchenko&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Sintchenko Vitali</a>, <a href="/search?value1=Ruiting+Lan&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lan Ruiting</a></span>. Multilevel genome typing: genomics-guided scalable resolution typing of microbial pathogens. <a href="/content/ecdc">Euro Surveill.</a> 2020;25(20):pii=1900519. <a href="https://doi.org/10.2807/1560-7917.ES.2020.25.20.1900519" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2020.25.20.1900519</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 13 Aug 2019;&nbsp;&nbsp; <span class="generated">Accepted</span>: 12 Nov 2019 </span> </p>
/content/10.2807/1560-7917.ES.2020.25.20.1900519
/content/10.2807/1560-7917.ES.2020.25.20.1900519
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error