MLST revisited: The gene-by-gene approach to bacterial genomics

Nature Reviews Microbiology

Volumn 11, Issue 10, 2013, Pages 728-736

  Maiden, Martin C J ^a   Van Rensburg, Melissa J Jansen ^a   Bray, James E ^a   Earle, Sarah G ^a   Ford, Suzanne A ^a   Jolley, Keith A ^a   McCarthy, Noel D ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

BACILLUS ANTHRACIS; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIUM ISOLATE; GENE SEQUENCE; GENETIC PROCEDURES; GENETIC VARIABILITY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULAR EVOLUTION; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; REVIEW; RNA SEQUENCE; SINGLE NUCLEOTIDE POLYMORPHISM; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS; WHOLE GENOME SEQUENCING; YERSINIA PESTIS;

ALLELES; BACTERIA; BACTERIAL TYPING TECHNIQUES; BASE SEQUENCE; DATABASES, GENETIC; EVOLUTION, MOLECULAR; GENETIC VARIATION; GENOME, BACTERIAL; GENOMICS; MULTILOCUS SEQUENCE TYPING; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S;

BACTERIA (MICROORGANISMS);

EID: 84884290186     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3093     Document Type: Review

References (95)

1. Ciccarelli, F. D. et al. Toward automatic reconstruction of a highly resolved tree of life. Science 311, 1283-1287 (2006). (Pubitemid 43334717)
2. Medini, D. et al. Microbiology in the post-genomic era. Nature Rev. Microbiol. 6, 419-430 (2008). (Pubitemid 351696436)
3. Rusch, D. B. et al. The Sorcerer II Global Ocean Sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol. 5, e77 (2007).
4. Fournier, P. E. & Raoult, D. Prospects for the future using genomics and proteomics in clinical microbiology. Annu. Rev. Microbiol. 65, 169-188 (2011).
5. Stackebrandt, E. et al. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int. J. Syst. Evol. Microbiol. 52, 1043-1047 (2002). (Pubitemid 34591239)
6. Koch, R. An address on bacteriological research. Br. Med. J. 2, 380-383 (1890).
7. Fraser, C., Alm, E. J., Polz, M. F., Spratt, B. G. & Hanage, W. P. The bacterial species challenge: making sense of genetic and ecological diversity. Science 323, 741-746 (2009).
8. Buckee, C. O. et al. Role of selection in the emergence of lineages and the evolution of virulence in Neisseria meningitidis. Proc. Natl Acad. Sci. USA 105, 15082-15087 (2008).
9. Bentley, S. D. & Parkhill, J. Comparative genomic structure of prokaryotes. Annu. Rev. Genet. 38, 771-792 (2004). (Pubitemid 40013745)
10. Tettelin, H., Riley, D., Cattuto, C. & Medini, D. Comparative genomics: the bacterial pan-genome. Curr. Opin. Microbiol. 11, 472-477 (2008).
11. Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms - proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576-4579 (1990).
12. Fox, G. E. et al. The phylogeny of prokaryotes. Science 209, 457-463 (1980). (Pubitemid 10022749)
13. Clarridge, J. E. Impact of 16S rRNA gene sequence analysis for identification of bacteria on clinical microbiology and infectious diseases. Clin. Microbiol. Rev. 17, 840-862 (2004).
14. Vamosi, S. M., Heard, S. B., Vamosi, J. C. & Webb, C. O. Emerging patterns in the comparative analysis of phylogenetic community structure. Mol. Ecol. 18, 572-592 (2009).
15. Hugenholtz, P., Goebel, B. M. & Pace, N. R. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. J. Bacteriol. 180, 4765-4774 (1998). (Pubitemid 28429361)
16. Sabat, A. J. et al. Overview of molecular typing methods for outbreak detection and epidemiological surveillance. Eurosurveillance 18, 17-30 (2013).
17. Maiden, M. C. J. et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl Acad. Sci. USA 95, 3140-3145 (1998). (Pubitemid 28135868)
18. Perez-Losada, M., Cabezas, P., Castro-Nallar, E. & Crandall, K. A. Pathogen typing in the genomics era: MLST and the future of molecular epidemiology. Infection Genet. Evol. 16, 38-53 (2013).
19. Maynard Smith, J., Smith, N. H., O'Rourke, M. & Spratt, B. G. How clonal are bacteria? Proc. Natl Acad. Sci. USA 90, 4384-4388 (1993). (Pubitemid 23148908)
20. Maiden, M. C. J. Multilocus sequence typing of bacteria. Annu. Rev. Microbiol. 60, 561-588 (2006). (Pubitemid 44627961)
21. Selander, R. K. et al. Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl. Environ. Microbiol. 51, 837-884 (1986).
22. Didelot, X. & Maiden, M. C. Impact of recombination on bacterial evolution. Trends Microbiol. 18, 315-322 (2010).
23. Turner, K. M. & Feil, E. J. The secret life of the multilocus sequence type. Int. J. Antimicrob. Agents 29, 129-135 (2007). (Pubitemid 46073677)
24. Do, T. et al. Population structure of Streptococcus oralis. Microbiology 155, 2593-2602 (2009).
25. Webb, K. et al. Development of an unambiguous and discriminatory multilocus sequence typing scheme for the Streptococcus zooepidemicus group. Microbiology 154, 3016-3024 (2008).
26. Coffey, T. J. et al. First insights into the evolution of Streptococcus uberis: a multilocus sequence typing scheme that enables investigation of its population biology. Appl. Environ. Microbiol. 72, 1420-1428 (2006). (Pubitemid 43271255)
27. Enright, M. C. & Spratt, B. G. A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology 144, 3049-3060 (1998). (Pubitemid 28515583)
28. Priest, F. G., Barker, M., Baillie, L. W., Holmes, E. C. & Maiden, M. C. Population structure and evolution of the Bacillus cereus group. J. Bacteriol. 186, 7959-7970 (2004). (Pubitemid 39552507)
29. Achtman, M. et al. Microevolution and history of the plague bacillus, Yersinia pestis. Proc. Natl Acad. Sci. USA 101, 17837-17842 (2004). (Pubitemid 40051973)
30. Jolley, K. A. et al. Resolution of a meningococcal disease outbreak from whole genome sequence data with rapid web-based analysis methods. J. Clin. Microbiol. 50, 3046-3053 (2012).
31. Holt, K. E. et al. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nature Genet. 40, 987-993 (2008).
32. Jolley, K. A., Brehony, C. & Maiden, M. C. Molecular typing of meningococci: recommendations for target choice and nomenclature. FEMS Microbiol. Rev. 31, 89-96 (2007). (Pubitemid 46058824)
33. Dingle, K. E., McCarthy, N. D., Cody, A. J., Peto, T. E. & Maiden, M. C. Extended sequence typing of Campylobacter spp., United Kingdom. Emerg. Infect. Dis. 14, 1620-1622 (2008).
34. Adair, D. M. et al. Diversity in a variable-number tandem repeat from Yersinia pestis. J. Clin. Microbiol. 38, 1516-1519 (2000). (Pubitemid 30216682)
35. Parkhill, J. & Wren, B. W. Bacterial epidemiology and biology - lessons from genome sequencing. Genome Biol. 12, 230 (2011).
36. Pallen, M. J., Loman, N. J. & Penn, C. W. High-throughput sequencing and clinical microbiology: progress, opportunities and challenges. Curr. Opin. Microbiol. 13, 625-631 (2010).
37. Didelot, X., Bowden, R., Wilson, D. J., Peto, T. E. A. & Crook, D. W. Transforming clinical microbiology with bacterial genome sequencing. Nature Rev. Genet. 13, 601-612 (2012).
38. Loman, N. J. et al. High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity. Nature Rev. Microbiol. 10, 599-606 (2012).
39. Junemann, S. et al. Updating benchtop sequencing performance comparison. Nature Biotech. 31, 294-296 (2013).
40. Croucher, N. J., Harris, S. R., Grad, Y. H. & Hanage, W. P. Bacterial genomes in epidemiology-present and future. Philos. Trans. R. Soc. B 368, 20120202 (2013).
41. Köser, C. U. et al. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. New Engl. J. Med. 366, 2267-2275 (2012).
42. Eyre, D. W. et al. A pilot study of rapid benchtop sequencing of Staphylococcus aureus and Clostridium difficile for outbreak detection and surveillance. BMJ Open 2, e001124 (2012).
43. Harris, S. R. et al. Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect. Dis. 31, 130-136 (2012).
44. McAdam, P. R. et al. Molecular tracing of the emergence, adaptation, and transmission of hospital-associated methicillin-resistant Staphylococcus aureus. Proc. Natl Acad. Sci. USA 109, 9107-9112 (2012).
45. Holden, M. T. et al. A genomic portrait of the emergence, evolution and global spread of a methicillin resistant Staphylococcus aureus pandemic. Genome Res. 23, 653-664 (2013).
46. Young, B. C. et al. Evolutionary dynamics of Staphylococcus aureus during progression from carriage to disease. Proc. Natl Acad. Sci. USA 109, 4550-4555 (2012).
47. Mutreja, A. et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477, 462-465 (2011).
48. Bryant, J. M. et al. Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet 381, 1551-1560 (2013).
49. He, M. et al. Evolutionary dynamics of Clostridium difficile over short and long time scales. Proc. Natl Acad. Sci. USA 107, 7527-7532 (2010).
50. Cui, Y. J. et al. Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proc. Natl Acad. Sci. USA 110, 577-582 (2013).
51. Walker, T. M. et al. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect. Dis. 13, 137-146 (2013).
52. Grad, Y. H. et al. Genomic epidemiology of the Escherichia coli O104:H4 outbreaks in Europe, 2011. Proc. Natl Acad. Sci. USA 109, 3065-3070 (2012).
53. Iqbal, Z., Turner, I. & McVean, G. High-throughput microbial population genomics using the Cortex variation assembler. Bioinformatics 29, 275-276 (2013).
54. Jolley, K. A. & Maiden, M. C. Automated extraction of typing information for bacterial pathogens from whole genome sequence data: Neisseria meningitidis as an exemplar. Euro Surveill. 18, 20379 (2013).
55. Sheppard, S. K., Jolley, K. A. & Maiden, M. C. J. A gene-by-gene approach to bacterial population genomics: whole genome MLST of Campylobacter. Genes 3, 261-277 (2012).
56. Bratcher, H. B., Bennett, J. S. & Maiden, M. C. J. Evolutionary and genomic insights into meningococcal biology. Future Microbiol. 7, 873-885 (2012).
57. Konstantinidis, K. T. & Tiedje, J. M. Trends between gene content and genome size in prokaryotic species with larger genomes. Proc. Natl Acad. Sci. USA 101, 3160-3165 (2004). (Pubitemid 38327751)
58. Zerbino, D. R. & Birney, E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18, 821-829 (2008). (Pubitemid 351645072)
59. Chain, P. S. et al. Genomics. Genome project standards in a new era of sequencing. Science 326, 236-237 (2009).
60. Hunt, M. et al. REAPR: a universal tool for genome assembly evaluation. Genome Biol. 14, R47 (2013).
61. Enright, M. C. et al. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc. Natl Acad. Sci. USA 99, 7687-7692 (2002). (Pubitemid 34568752)
62. Harmsen, D., Rothganger, J., Frosch, M. & Albert, J. RIDOM: ribosomal differentiation of medical micro-organisms database. Nucleic Acids Res. 30, 416-417 (2002). (Pubitemid 34679601)
63. Koser, C. U. et al. Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog. 8, e1002824 (2012).
64. Aarestrup, F. M. et al. Integrating genome-based informatics to modernize global disease monitoring, information sharing, and response. Emerg. Infect. Dis. 18, e1 (2012).
65. Carrico, J. A., Sabat, A. J. & Friedrich, A. W., Ramirez, M. & ESCMID Study Group for Epidemiological Markers (ESGEM). Bioinformatics in bacterial molecular epidemiology and public health: databases, tools and the next-generation sequencing revolution. Euro Surveill. 18, 32-40 (2013).
66. Chan, M. S., Maiden, M. C. & Spratt, B. G. Database-driven multi locus sequence typing (MLST) of bacterial pathogens. Bioinformatics 17, 1077-1083 (2001). (Pubitemid 33085617)
67. Jolley, K. A., Chan, M. S. & Maiden, M. C. mlstdbNet - distributed multi-locus sequence typing (MLST) databases. BMC Bioinformatics 5, 86 (2004).
68. Aanensen, D. M. & Spratt, B. G. The multilocus sequence typing network: mlst.net. Nucleic Acids Res. 33, W728-W733 (2005). (Pubitemid 44530019)
69. Jolley, K. A. & Maiden, M. C. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11, 595 (2010).
70. Jolley, K. A. & Maiden, M. C. AgdbNet - antigen sequence database software for bacterial typing. BMC Bioinformatics 7, 314 (2006).
71. Markowitz, V. M. et al. The integrated microbial genomes system: an expanding comparative analysis resource. Nucleic Acids Res. 38, D382-D390 (2010).
72. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402 (1997). (Pubitemid 27359211)
73. Bryant, D. & Moulton, V. Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol. Biol. Evol. 21, 255-265 (2004). (Pubitemid 38314614)
74. Huson, D. H. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14, 68-73 (1998). (Pubitemid 28397727)
75. Jolley, K. A. et al. Ribosomal multi-locus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 158, 1005-1015 (2012).
76. Yutin, N., Puigbo, P., Koonin, E. V. & Wolf, Y. I. Phylogenomics of prokaryotic ribosomal proteins. PLoS ONE 7, e36972 (2012).
77. Wu, M. & Eisen, J. A. A simple, fast, and accurate method of phylogenomic inference. Genome Biol. 9, R151 (2008).
78. Bennett, J. S. et al. A genomic approach to bacterial taxonomy: an examination and proposed reclassification of species within the genus Neisseria. Microbiology 158, 1570-1580 (2012).
79. Cody, A. J. et al. Real-time genomic epidemiology of human Campylobacter isolates using whole genome multilocus sequence typing. J. Clin. Microbiol. 51, 2526-2534 (2013).
80. Stefani, S. et al. Meticillin-resistant Staphylococcus aureus (MRSA): global epidemiology and harmonisation of typing methods. Int. J. Antimicrob. Agents 39, 273-282 (2012).
81. Widerstrom, M., Wistrom, J., Sjostedt, A. & Monsen, T. Coagulase-negative staphylococci: update on the molecular epidemiology and clinical presentation, with a focus on Staphylococcus epidermidis and Staphylococcus saprophyticus. Eur. J. Clin. Microbiol. Infect. Dis. 31, 7-20 (2012).
82. Harris, S. R. et al. Evolution of MRSA during hospital transmission and intercontinental spread. Science 327, 469-474 (2010).
83. Lindsay, J. A. Genomic variation and evolution of Staphylococcus aureus. Int. J. Med. Microbiol. 300, 98-103 (2010).
84. Uhlemann, A. C., Otto, M., Lowy, F. D. & Deleo, F. R. Evolution of community-and healthcare-associated methicillin-resistant Staphylococcus aureus. Infect. Genet. Evol. http://dx.doi.org/10.1016/j.meegid.2013.04.030 (2013).
85. Fitzgerald, J. R. Livestock-associated Staphylococcus aureus: origin, evolution and public health threat. Trends Microbiol. 20, 192-198 (2012).
86. Fitzgerald, J. R. Evolution of Staphylococcus aureus during human colonization and infection. Infect. Genet. Evol. http://dx.doi.org/10.1016/j. meegid.2013.04.020 (2013).
87. Lindsay, J. A. Evolution of Staphylococcus aureus and MRSA during outbreaks. Infect. Genet. Evol. http://dx.doi.org/10.1016/j.meegid.2013.04.017 (2013).
88. Sung, J. S., Chun, J., Choi, S. & Park, W. Genome sequence of the halotolerant Staphylococcus sp. strain OJ82, isolated from Korean traditional salt-fermented seafood. J. Bacteriol. 194, 6353-6354 (2012).
89. Chong, T. M., Tung, H. J., Yin, W. F. & Chan, K. G. Insights from the genome sequence of quorum-quenching Staphylococcus sp. strain AL1, isolated from traditional Chinese soy sauce brine fermentation. J. Bacteriol. 194, 6611-6612 (2012).
90. Holt, D. C. et al. A very early-branching Staphylococcus aureus lineage lacking the carotenoid pigment staphyloxanthin. Genome Biol. Evol. 3, 881-895 (2011).
91. Milkman, R. & McKane, M. in Population Genetics of Bacteria (eds Baumberg, S., Young, J. P. W., Wellington, E. M. H. & Saunders, J. R.) 127-142 (Cambridge Univ. Press, 1995).
92. Lapage, S. P. et al. International Code of Nomenclature of Bacteria: Bacteriological Code, 1990 Revision (American Society for Microbiology, 1992).
93. Maynard Smith, J., Dowson, C. G. & Spratt, B. G. Localized sex in bacteria. Nature 349, 29-31 (1991). (Pubitemid 21912003)
94. Spratt, B. G. Hybrid penicillin-binding proteins in penicillin-resistant strains of Neisseria gonorrhoeae. Nature 332, 173-176 (1988). (Pubitemid 18083565)
95. Fernandez-Suarez, X. M. & Galperin, M. Y. The 2013 nucleic acids research database issue and the online molecular biology database collection. Nucleic Acids Res. 41, D1-D7 (2013).