Genomic perspectives on the evolution and spread of bacterial pathogens

Proceedings of the Royal Society B: Biological Sciences

Volumn 282, Issue 1821, 2015, Pages

  Bentley, Stephen D ^a   Parkhill, Julian ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Bacterial evolution; Bacterial genomics; Bacterial transmission

Indexed keywords

ADAPTATION; BACTERIUM; BIODEGRADATION; DISEASE TRANSMISSION; EVOLUTIONARY BIOLOGY; GENETIC ANALYSIS; GENOMICS; HOST-PATHOGEN INTERACTION; IMMUNE SYSTEM; MICROBIOLOGY; PHYLOGENETICS; VIRULENCE;

BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE;

VIRULENCE FACTOR;

BACTERIAL GENOME; BACTERIAL INFECTIONS; BACTERIUM; COMMUNICABLE DISEASES; EPIDEMIC; GENETICS; GENOMICS; HOST PATHOGEN INTERACTION; HUMAN; MICROBIOLOGY; MOLECULAR EVOLUTION; PATHOGENICITY; PHYLOGENY; TRANSMISSION;

BACTERIA; BACTERIAL INFECTIONS; COMMUNICABLE DISEASES; DISEASE OUTBREAKS; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; GENOMICS; HOST-PATHOGEN INTERACTIONS; HUMANS; PHYLOGENY; VIRULENCE FACTORS;

EID: 84951931347     PISSN: 09628452     EISSN: 14712954     Source Type: Journal    
DOI: 10.1098/rspb.2015.0488     Document Type: Review

References (76)

1. Sabat AJ et al. 2013 Overview of molecular typing methods for outbreak detection and epidemiological surveillance. Euro Surveill. 18, 20380.
2. Maiden MC et al. 1998 Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl Acad. Sci. USA 95, 3140-3145. (doi:10. 1073/pnas.95.6.3140)
3. Binnewies TT et al. 2006 Ten years of bacterial genome sequencing: comparative-genomics-based discoveries. Funct. Integr. Genomics 6, 165-185. (doi:10.1007/s10142-006-0027-2)
4. Fraser-Liggett CM. 2005 Insights on biology and evolution from microbial genome sequencing. Genome Res. 15, 1603-1610. (doi:10.1101/gr. 3724205)
5. Nierman W, Eisen JA, Fraser CM. 2000 Microbial genome sequencing 2000: new insights into physiology, evolution and expression analysis. Res. Microbiol. 151, 79-84. (doi:10.1016/S0923- 2508(00)00125-X)
6. Sanger F, Nicklen S, Coulson AR. 1992 DNA sequencing with chain-terminating inhibitors. Biotechnology 24, 104-108.
7. Quail MA, Smith ME, Coupland P, Otto TD, Harris SR, Connor TR, Bertoni A, Swerdlow HP, Gu Y. 2012 A tale of three next generation sequencing platforms: comparison of ion torrent, Pacific biosciences and Illumina MiSeq sequencers. BMC Genomics 13, 341. (doi:10.1186/1471-2164-13-341)
8. Hacker J, Kaper JB. 2000 Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54, 641-679. (doi:10.1146/annurev.micro.54.1.641)
9. Perna NT et al. 2001 Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409, 529-533. (doi:10.1038/35054089)
10. Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R. 2005 The microbial pan-genome. Curr. Opin. Genet. Dev. 15, 589-594. (doi:10.1016/j.gde. 2005.09.006)
11. Vernikos G, Medini D, Riley DR, Tettelin H. 2015 Ten years of pan-genome analyses. Curr. Opin. Microbiol. 23C, 148-154. (doi:10.1016/j.mib.2014.11.016)
12. Parkhill J et al. 2001 Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523-527. (doi:10.1038/35097083)
13. Parkhill J et al. 2003 Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat. Genet. 35, 32-40. (doi:10. 1038/ng1227)
14. Parkhill J et al. 2001 Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413, 848-852. (doi:10.1038/ 35101607)
15. Cummings CA, Brinig MM, Lepp PW, van de Pas S, Relman DA. 2004 Bordetella species are distinguished by patterns of substantial gene loss and host adaptation. J. Bacteriol. 186, 1484-1492. (doi:10.1128/JB.186.5.1484-1492.2004)
16. Nierman WC et al. 2004 Structural flexibility in the Burkholderia mallei genome. Proc. Natl Acad. Sci. USA 101, 14 246-14 251. (doi:10.1073/pnas. 0403306101)
17. Lee BM et al. 2005 The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res. 33, 577-586. (doi:10.1093/nar/gki206)
18. Mira A, Pushker R, Rodriguez-Valera F. 2006 The Neolithic revolution of bacterial genomes. Trends Microbiol. 14, 200-206. (doi:10.1016/j.tim. 2006.03.001)
19. Rasko DA et al. 2011 Bacillus anthracis comparative genome analysis in support of the Amerithrax investigation. Proc. Natl Acad. Sci. USA 108, 5027-5032. (doi:10.1073/pnas.1016657108)
20. Ochman H, Elwyn S, Moran NA. 1999 Calibrating bacterial evolution. Proc. Natl Acad. Sci. USA 96, 12 638-12 643. (doi:10.1073/pnas.96.22.12638)
21. Ochman H, Wilson AC. 1987 Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J. Mol. Evol. 26, 74-86. (doi:10.1007/ BF02111283)
22. Harris SR et al. 2010 Evolution of MRSA during hospital transmission and intercontinental spread. Science 327, 469-474. (doi:10.1126/science. 1182395)
23. Croucher NJ et al. 2011 Rapid pneumococcal evolution in response to clinical interventions. Science 331, 430-434. (doi:10.1126/science. 1198545)
24. Mutreja A et al. 2011 Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477, 462-465. (doi:10.1038/ nature10392)
25. von Mentzer A et al. 2014 Identification of enterotoxigenic Escherichia coli (ETEC) clades with long-term global distribution. Nat. Genet. 46, 1321-1326. (doi:10.1038/ng.3145)
26. Sack DA, Sack RB, Nair GB, Siddique AK. 2004 Cholera. Lancet 363, 223-233. (doi:10.1016/S0140- 6736(03)15328-7)
27. Feng L et al. 2008 A recalibrated molecular clock and independent origins for the cholera pandemic clones. PLoS ONE 3, e4053. (doi:10.1371/journal. pone.0004053)
28. Frerichs RR, Keim PS, Barrais R, Piarroux R. 2012 Nepalese origin of cholera epidemic in Haiti. Clin. Microbiol. Infect. 18, E158-E163. (doi:10.1111/j. 1469-0691.2012.03841.x)
29. Hendriksen RS et al. 2011 Population genetics of Vibrio cholerae from Nepal in 2010: evidence on the origin of the Haitian outbreak. mBio 2, e00157. (doi:10.1128/mBio.00157-11)
30. Azarian T et al. 2014 Phylodynamic analysis of clinical and environmental Vibrio cholerae isolates from Haiti reveals diversification driven by positive selection. mBio 5, e01824. (doi:10.1128/mBio. 01824-14)
31. Eppinger M et al. 2014 Genomic epidemiology of the Haitian cholera outbreak: a single introduction followed by rapid, extensive, and continued spread characterized the onset of the epidemic. mBio 5, e01721. (doi:10.1128/mBio.01721-14)
32. Katz LS et al. 2013 Evolutionary dynamics of Vibrio cholerae O1 following a single-source introduction to Haiti. mBio 4, e00398. (doi:10.1128/ mBio.00398-13)
33. Selezska K, Kazmierczak M, Müsken M, Garbe J, Schobert M, Häussler S, Wiehlmann L, Rohde C, Sikorski J. 2012 Pseudomonas aeruginosa population structure revisited under environmental focus: impact of water quality and phage pressure. Environ. Microbiol. 14, 1952-1967. (doi:10.1111/j. 1462-2920.2012.02719.x)
34. Wiehlmann L et al. 2007 Population structure of Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 104, 8101-8106. (doi:10.1073/pnas.0609213104)
35. Dettman JR, Rodrigue N, Aaron SD, Kassen R. 2012 Evolutionary genomics of epidemic and nonepidemic strains of Pseudomonas aeruginosa. Proc. Natl Acad. Sci. USA 110, 21 065-21 070. (doi:10.1073/pnas.1307862110)
36. Drevinek P, Mahenthiralingam E. 2010 Burkholderia cenocepacia in cystic fibrosis: epidemiology and molecular mechanisms of virulence. Clin. Microbiol. Infect. 16, 821-830. (doi:10.1111/j.1469-0691. 2010.03237.x)
37. Bryant JM et al. 2013 Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet 381, 1551-1560. (doi:10. 1016/S0140-6736(13)60632-7)
38. McGee L et al. 2001 Nomenclature of major antimicrobial-resistant clones of Streptococcus pneumoniae defined by the pneumococcal molecular epidemiology network. J. Clin. Microbiol. 39, 2565-2571. (doi:10.1128/JCM.39.7.2565-2571.2001)
39. Munoz R et al. 1991 Intercontinental spread of a multiresistant clone of serotype 23F Streptococcus pneumoniae. J. Infect. Dis. 164, 302-306. (doi:10. 1093/infdis/164.2.302)
40. Croucher NJ et al. 2014 Evidence for soft selective sweeps in the evolution of pneumococcal multidrug resistance and vaccine escape. Genome Biol. Evol. 6, 1589-1602. (doi:10.1093/gbe/evu120)
41. Croucher NJ et al. 2014 Variable recombination dynamics during the emergence, transmission and 'disarming' of a multidrug-resistant pneumococcal clone. BMC Biol. 12, 49. (doi:10.1186/1741-7007-12-49)
42. Croucher NJ et al. 2013 Dominant role of nucleotide substitution in the diversification of serotype 3 pneumococci over decades and during a single infection. PLoS Genet. 9, e1003868. (doi:10.1371/ journal.pgen.1003868)
43. Holden MT et al. 2013 A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic. Genome Res. 23, 653-664. (doi:10. 1101/gr.147710.112)
44. McAdam PR et al. 2012 Molecular tracing of the emergence, adaptation, and transmission of hospital-associated methicillin-resistant Staphylococcus aureus. Proc. Natl Acad. Sci. USA 109, 9107-9112. (doi:10.1073/pnas.1202869109)
45. Ward MJ, Gibbons CL, McAdam PR, van Bunnik BAD, Girvan EK, Edwards GF, Fitzgerald JR, Woolhouse MEJ. 2014 Time-scaled evolutionary analysis of the transmission and antibiotic resistance dynamics of Staphylococcus aureus CC398. Appl. Environ. Microbiol. 23, 7275-7282. (doi:10.1128/AEM.01777-14)
46. Brosch R et al. 2002 A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc. Natl Acad. Sci. USA 99, 3684-3689. (doi:10.1073/pnas. 052548299)
47. Comas I et al. 2013 Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat. Genet. 45, 1176-1182. (doi:10.1038/ng.2744)
48. Bos KI et al. 2014 Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis. Nature 514, 494-497. (doi:10. 1038/nature13591)
49. Frank C et al. 2011 Epidemic profile of Shiga-toxinproducing Escherichia coli O104: H4 outbreak in Germany. N. Engl. J. Med. 365, 1771-1780. (doi:10.1056/NEJMoa1106483)
50. Rohde H et al. 2011 Open-source genomic analysis of Shiga-toxin-producing E. coli O104: H4. N. Engl. J. Med. 365, 718-724. (doi:10.1056/NEJMoa1107643)
51. Grad YH et al. 2013 Comparative genomics of recent Shiga toxin-producing Escherichia coli O104:H4: short-term evolution of an emerging pathogen. mBio 4, e00452-00412. (doi:10.1128/mBio.00452-12)
52. den Bakker HC et al. 2014 Rapid whole-genome sequencing for surveillance of Salmonella enterica serovar enteritidis. Emerg. Infect. Dis. 20, 1306-1314. (doi:10.3201/eid2008.131399)
53. Lienau EK et al. 2011 Identification of a salmonellosis outbreak by means of molecular sequencing. N. Engl. J. Med. 364, 981-982. (doi:10.1056/NEJMc1100443)
54. Harris SR et al. 2013 Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet 13, 130-136. (doi:10.1016/S1473- 3099(12)70268-2)
55. Snitkin ES, Zelazny AM, Thomas PJ, Stock F, NISC Comparative Sequencing Program, Henderson DK, Palmore TN, Segre JA. 2012 Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci. Transl. Med. 4, 148ra116. (doi:10.1126/scitranslmed.3004129)
56. Halachev MR, Chan J, Constantinidou CI, Cumley N, Bradley C, Smith-Banks M, Oppenheim B, Pallen MJ. 2014 Genomic epidemiology of a protracted hospital outbreak caused by multidrug-resistant Acinetobacter baumannii in Birmingham, England. Genome Med. 6, 70 (doi:10.1186/s13073-014-0070-x)
57. Worby CJ, Lipsitch M, Hanage WP. 2014 Within-host bacterial diversity hinders accurate reconstruction of transmission networks from genomic distance data. PLoS Comput. Biol. 10, e1003549. (doi:10.1371/ journal.pcbi.1003549)
58. Golubchik T et al. 2013 Within-host evolution of Staphylococcus aureus during asymptomatic carriage. PLoS ONE 8, e61319. (doi:10.1371/journal. pone.0061319)
59. Tong SY et al. 2014 Genome sequencing defines phylogeny and spread of methicillin-resistant Staphylococcus aureus in a high transmission setting. Genome Res. 25, 111-118. (doi:10.1101/ gr.174730.114)
60. Eyre DW et al. 2013 Diverse sources of C. difficile infection identified on whole-genome sequencing. N. Engl. J. Med. 369, 1195-1205. (doi:10.1056/ NEJMoa1216064)
61. Walker TM et al. 2013 Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet 13, 137-146. (doi:10.1016/S1473-3099(12)70277-3)
62. Bryant JM et al. 2013 Whole-genome sequencing to establish relapse or re-infection with Mycobacterium tuberculosis: a retrospective observational study. Lancet 1, 786-792. (doi:10.1016/S2213- 2600(13)70231-5)
63. Guerra-Assuncao JA et al. 2014 Recurrence due to relapse or reinfection with Mycobacterium tuberculosis: a whole-genome sequencing approach in a large, population-based cohort with a high HIV infection prevalence and active follow-up. J. Infect. Dis. 211, 1154-1163. (doi:10.1093/infdis/jiu574)
64. Gardy JL et al. 2011 Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N. Engl. J. Med. 364, 730-739. (doi:10.1056/ NEJMoa1003176)
65. Marston BJ, Lipman HB, Breiman RF. 1994 Surveillance for Legionnaires' disease: risk factors for morbidity and mortality. Arch. Intern. Med. 154, 2417-2422. (doi:10.1001/archinte.1994. 00420210049006)
66. Bull M, Hall IM, Leach S, Robesyn E. 2012 The application of geographic information systems and spatial data during Legionnaires disease outbreak responses. Euro Surveill. 17, 20331.
67. McAdam PR et al. 2014 Gene flow in environmental Legionella pneumophila leads to genetic and pathogenic heterogeneity within a Legionnaires' disease outbreak. Genome Biol. 15, 504. (doi:10. 1186/PREACCEPT-1675723368141690)
68. Johansson A et al. 2014 An outbreak of respiratory tularemia caused by diverse clones of Francisella tularensis. Clin. Infect. Dis. 59, 1546-1553. (doi:10. 1093/cid/ciu621)
69. Didelot X, Bowden R, Wilson DJ, Peto TE, Crook DW. 2012 Transforming clinical microbiology with bacterial genome sequencing. Nat. Rev. Genet. 13, 601-612. (doi:10.1038/nrg3226)
70. Koser CU et al. 2012 Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog. 8, e1002824. (doi:10. 1371/journal.ppat.1002824)
71. Chewapreecha C et al. 2014 Comprehensive identification of single nucleotide polymorphisms associated with beta-lactam resistance within pneumococcal mosaic genes. PLoS Genet. 10, e1004547. (doi:10.1371/journal.pgen.1004547)
72. Farhat MR et al. 2013 Genomic analysis identifies targets of convergent positive selection in drugresistant Mycobacterium tuberculosis. Nat. Genet. 45, 1183-1189. (doi:10.1038/ng.2747)
73. Sheppard SK et al. 2013 Genome-wide association study identifies vitamin B5 biosynthesis as a host specificity factor in Campylobacter. Proc. Natl Acad. Sci. USA 110, 11 923-11 927. (doi:10.1073/pnas. 1305559110)
74. Ashton PM, Nair S, Dallman T, Rubino S, Rabsch W, Mwaigwisya S, Wain J, O'Grady J. 2014 MinION nanopore sequencing identifies the position and structure of a bacterial antibiotic resistance island. Nat. Biotechnol. 33, 296-300. (doi:10.1038/nbt.3103)
75. Plucain J et al. 2014 Epistasis and allele specificity in the emergence of a stable polymorphism in Escherichia coli. Science 343, 1366-1369. (doi:10. 1126/science.1248688)
76. Manso AS et al. 2014 A random six-phase switch regulates pneumococcal virulence via global epigenetic changes. Nat. Commun. 5, 5055. (doi:10. 1038/ncomms6055)