Skip to main content
SpringerLink
Log in

Genomic Analysis of Bacterial Outbreaks

  • Chapter
  • First Online:
Evolutionary Biology

  • 2046 Accesses

Abstract

The study of outbreaks of infectious diseases has been revolutionized by the current availability of fast and efficient, high-throughput methods capable of yielding the nucleotide sequence of complete genomes of viruses and bacteria within a few days, or even hours. These methods are replacing previous molecular techniques which have been used for the past 30 years, although many of them are still the usual approach for many such investigations. Here we review the major technologies currently in use for high-throughput sequencing of bacterial genomes emphasizing their advantages and drawbacks for the analysis of outbreaks. The use of more efficient methods does not necessarily mean that all the problems in the study of outbreaks are automatically solved. In fact, because these methods are capable of revealing genetic variation at an unprecedented level and scale they also pose new challenges for the interpretation of the resulting data. We analyze some of these new challenges, especially those in which the short term evolution of microorganism plays an important role in understanding and interpreting the results and, quite often, in reconciling them with those derived from classical epidemiological analyses. Finally, we exemplify the advantages of using complete genome analysis with two cases, involving outbreaks of Mycobacterium tuberculosis and Legionella pneumophila.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Achtman M (2008) Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol 62:53–70

    Article  CAS  PubMed  Google Scholar 

  • Achtman M (2012) Insights from genomic comparisons of genetically monomorphic bacterial pathogens. Phil Trans R Soc B 367:860–867

    Article  PubMed  PubMed Central  Google Scholar 

  • Ahmed SA, Awosika J, Baldwin C, Bishop-Lilly KA, Biswas B, Broomall S, Chain PSG, Chertkov O, Chokoshvili O, Coyne S, Davenport K, Detter JC, Dorman W, Erkkila TH, Folster JP, Frey KG, George M, Gleasner C, Henry M, Hill KK, Hubbard K, Insalaco J, Johnson S, Kitzmiller A, Krepps M, Lo CC, Luu T, McNew LA, Minogue T, Munk CA, Osborne B, Patel M, Reitenga KG, Rosenzweig CN, Shea A, Shen X, Strockbine N, Tarr C, Teshima H, Van Gieson E, Verratti K, Wolcott M, Xie G, Sozhamannan S, Gibbons HS, Threat Characterization Consortium (2012) Genomic comparison of Escherichia coli O104: H4 isolates from 2009 and 2011 reveals plasmid, and prophage heterogeneity, including shiga toxin encoding phage stx2. PLoS ONE 7:e48228

    Google Scholar 

  • Allard MW, Luo Y, Strain E, Li C, Keys CE, Son I, Stones R, Musser SM, Brown EW (2012) High resolution clustering of Salmonella enterica serovar Montevideo strains using a next-generation sequencing approach. BMC Genom 13:1

    Article  CAS  Google Scholar 

  • Allard MW, Luo Y, Strain E, Pettengill J, Timme R, Wang C, Li C, Keys CE, Zheng J, Stones R, Wilson MR, Musser SM, Brown EW (2013) On the evolutionary history, population genetics and diversity among isolates of Salmonella enteritidis PFGE pattern JEGX01.0004. PLoS ONE 8:e55254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azarian T, Cook RL, Johnson JA, Guzman N, McCarter YS, Gomez N, Rathore MH, Morris JGJ, Salemi M (2015) Whole-genome sequencing for outbreak investigations of Methicillin-resistant Staphylococcus aureus in the neonatal intensive care unit: time for routine practice? Infect Control Hosp Epidemiol 36:777–785

    Article  PubMed  PubMed Central  Google Scholar 

  • Barnes PF, Cave MD (2003) Molecular epidemiology of tuberculosis. N Engl J Med 349:1149–1156

    Article  CAS  PubMed  Google Scholar 

  • Bartley PB, Ben Zakour NL, Stanton-Cook M, Muguli R, Prado L, Garnys V, Taylor K, Barnett TC, Pinna G, Robson J, Paterson DL, Walker MJ, Schembri MA, Beatson SA (2016) Hospital-wide eradication of a nosocomial Legionella pneumophila serogroup 1 outbreak. Clin Infect Dis 62:273–279

    Article  PubMed  Google Scholar 

  • Bekal S, Berry C, Reimer AR, Van Domselaar G, Beaudry G, Fournier E, Doualla-Bell F, Levac E, Gaulin C, Ramsay D, Huot C, WAlker M, Sieffert C, Tremblay C (2016) Usefulness of high-quality core genome single-nucleotide variant analysis for subtyping the highly clonal and the most prevalent Salmonella enterica serovar Heidelberg clone in the context of outbreak investigations. J Clin Microbiol 54:289–295

    Google Scholar 

  • Bennett JS, Jolley KA, Earle SG, Corton C, Bentley SD, Parkhill J, Maiden MCJ (2012) A genomic approach to bacterial taxonomy: an examination and proposed reclassification of species within the genus Neisseria. Microbiology 158:1570–1580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biek R, Pybus OG, Lloyd-Smith JO, Didelot X (2015) Measurably evolving pathogens in the genomic era. Trends Ecol Evol 30:306–313

    Article  PubMed  PubMed Central  Google Scholar 

  • Blouin Y, Cazajous G, Dehan C, Soler C, Vong R, Hassan MO, Hauck Y, Boulais C, Andriamanantena D, Martinaud C, Martin É, Pourcel C, Vergnaud G (2014) Progenitor “Mycobacterium canettii” clone responsible for lymph node tuberculosis epidemic, Djibouti. Emerg Infect Dis 20:21–28

    Article  PubMed  PubMed Central  Google Scholar 

  • Bos KI, Harkins KM, Herbig A, Coscolla M, Weber N, Comas I, Forrest SA, Bryant JM, Harris SR, Schuenemann VJ (2014) Pre-columbian mycobacterial genomes reveal seals as a source of new world human tuberculosis. Nature 514:494–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bos KI, Herbig A, Sahl J, Waglechner N, Fourment M, Forrest SA, Klunk J, Schuenemann VJ, Poinar D, Kuch M, Golding GB, Dutour O, Keim P, Wagner DM, Holmes EC, Krause J, Poinar HN (2016) Eighteenth century Yersinia pestis genomes reveal the long-term persistence of an historical plague focus. eLife Sci e12994

    Google Scholar 

  • Bryant J, Schurch A, Van Deutekom H, Harris S, de Beer J, de Jager V, Kremer K, Van Hijum S, Siezen R, Borgdorff M, Bentley S, Parkhill J, Van Soolingen D (2013a) Inferring patient to patient transmission of Mycobacterium tuberculosis from whole genome sequencing data. BMC Infect Dis 13:110

    Article  PubMed  PubMed Central  Google Scholar 

  • Bryant JM, Grogono DM, Greaves D, Foweraker J, Roddick I, Inns T, Reacher M, Haworth CS, Curran MD, Harris SR, Peacock SJ, Parkhill J, Floto RA (2013b) Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. The Lancet 381:1551–1560

    Article  CAS  Google Scholar 

  • Brzuszkiewicz E, Thürmer A, Schuldes J, Leimbach A, Liesegang H, Meyer FD, Boelter J, Petersen H, Gottschalk G, Daniel R (2011) Genome sequence analyses of two isolates from the recent Escherichia coli outbreak in Germany reveal the emergence of a new pathotype: Entero-Aggregative-Haemorrhagic Escherichia coli (EAHEC). Arch Microbiol 193:883–891

    Google Scholar 

  • Cao G, Meng J, Strain E, Stones R, Pettengill J, Zhao S, McDermott P, Brown E, Allard M (2013) Phylogenetics and differentiation of Salmonella newport lineages by whole genome sequencing. PLoS ONE 8:e55687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casali N, Nikolayevskyy V, Balabanova Y, Ignatyeva O, Kontsevaya I, Harris SR, Bentley SD, Parkhill J, Nejentsev S, Hoffner SE, Horstmann RD, Brown T, Drobniewski F (2012) Microevolution of extensively drug-resistant tuberculosis in Russia. Genome Res 22:735–745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casali N, Nikolayevskyy V, Balabanova Y, Harris SR, Ignatyeva O, Kontsevaya I, Corander J, Bryant J, Parkhill J, Nejentsev S, Horstmann RD, Brown T, Drobniewski F (2014) Evolution and transmission of drug resistant tuberculosis in a Russian population. Nat Genet 46:279–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Casey G, Conti D, Haile R, Duggan D (2013) Next generation sequencing and a new era of medicine. Gut 62:920–932

    Article  CAS  PubMed  Google Scholar 

  • Chewapreecha C, Harris SR, Croucher NJ, Turner C, Marttinen P, Cheng L, Pessia A, Aanensen DM, Mather AE, Page AJ, Salter SJ, Harris D, Nosten F, Goldblatt D, Corander J, Parkhill J, Turner P, Bentley SD (2014) Dense genomic sampling identifies highways of pneumococcal recombination. Nat Genet 46:305–309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chin CS, Sorenson J, Harris JB, Robins WP, Charles RC, Jean-Charles RR, Bullard J, Webster DR, Kasarskis A, Peluso P, Paxinos EE, Yamaichi Y, Calderwood SB, Mekalanos JJ, Schadt EE, Waldor MK (2011) The origin of the Haitian cholera outbreak strain. N Engl J Med 364:33–42

    Article  CAS  PubMed  Google Scholar 

  • Cody AJ, McCarthy ND, Jansen van Rensburg M, Isinkaye T, Bentley SD, Parkhill J, Dingle KE, Bowler ICJW, Jolley KA, Maiden MCJ (2013) Real-time genomic epidemiological evaluation of human Campylobacter isolates by use of whole-genome multilocus sequence typing. J Clin Microbiol 51:2526–2534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Comas I, Borrell S, Roetzer A, Rose G, Malla B, Kato-Maeda M, Galagan J, Niemann S, Gagneux S (2012) Whole-genome sequencing of rifampicin-resistant Mycobacterium tuberculosis strains identifies compensatory mutations in RNA polymerase genes. Nat Genet 44:106–110

    Article  CAS  Google Scholar 

  • Comas I, Coscolla M, Luo T, Borrell S, Holt KE, Kato-Maeda M, Parkhill J, Malla B, Berg S, Thwaites G, Yeboah-Manu D, Bothamley G, Mei J, Wei L, Bentley S, Harris SR, Niemann S, Diel R, Aseffa A, Gao Q, Young D, Gagneux S (2013) Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet 45:1176–1182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corander J, Tang J (2007) Bayesian analysis of population structure based on linked molecular information. Math Biosci 205:19–31

    Article  PubMed  Google Scholar 

  • Correia AM, Ferreira JS, Borges V, Nunes A, Gomes B, Capucho R, Gonçalves J, Antunes DM, Almeida S, Mendes A, Guerreiro M, Sampaio DA, Vieira L, Machado J, Simões MJ, Gonçalves P, Gomes JP (2016) Probable person-to-person transmission of Legionnaires’ disease. N Engl J Med 374:497–498

    Article  PubMed  Google Scholar 

  • Coscollá M, Fenollar J, Escribano I, González-Candelas F (2010) Legionellosis outbreak associated with asphalt paving machine, Spain, 2009. Emerg Infect Dis 16:1381–1387

    Article  PubMed  PubMed Central  Google Scholar 

  • Coscollá M, Barry PM, Oeltmann JE, Koshinsky H, Shaw T, Cilnis M, Posey J, Rose J, Weber T, Fofanov VY, Gagneux S, Kato-Maeda M, Metcalfe JZ (2015) Genomic epidemiology of multidrug-resistant Mycobacterium tuberculosis during transcontinental spread. J Infect Dis

    Google Scholar 

  • Cowley D, Govender D, February B, Wolfe M, Steyn L, Evans J, Wilkinson RJ, Nicol MP (2008) Recent and rapid emergence of W-Beijing strains of Mycobacterium tuberculosis in Cape Town, South Africa. Clin Infect Dis 47:1252–1259

    Article  PubMed  Google Scholar 

  • Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, Van der Linden M, McGee L, von Gottberg A, Song JH, Ko KS, Pichon B, Baker S, Parry CM, Lambertsen LM, Shahinas D, Pillai DR, Mitchell TJ, Dougan G, Tomasz A, Klugman KP, Parkhill J, Hanage WP, Bentley SD (2011) Rapid pneumococcal evolution in response to clinical interventions. Science 331:430–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croucher NJ, Finkelstein JA, Pelton SI, Mitchell PK, Lee GM, Parkhill J, Bentley SD, Hanage WP, Lipsitch M (2013) Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat Genet 45:656–663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui Y, Yu C, Yan Y, Li D, Li Y, Jombart T, Weinert LA, Wang Z, Guo Z, Xu L, Zhang Y, Zheng H, Qin N, Xiao X, Wu M, Wang X, Zhou D, Qi Z, Du Z, Wu H, Yang X, Cao H, Wang H, Wang J, Yao S, Rakin A, Li Y, Falush D, Balloux F, Achtman M, Song Y, Wang J, Yang R (2013) Historical variations in mutation rate in an epidemic pathogen, Yersinia pestis. Proc Nat Acad Sci U.S.A. 110:577–582

    Article  CAS  Google Scholar 

  • Davidson RM, Hasan NA, de Moura VCN, Duarte RS, Jackson M, Strong M (2013) Phylogenomics of Brazilian epidemic isolates of Mycobacterium abscessus subsp. bolletii reveals relationships of global outbreak strains. Infect Genet Evol 20:292–297

    Article  PubMed  Google Scholar 

  • De Been M, Pinholt M, Top J, Bletz S, Mellmann A, Van Schaik W, Brouwer E, Rogers M, Kraat Y, Bonten M, Corander J, Westh H, Harmsen D, Willems RJL (2015) Core genome multilocus sequence typing scheme for high-resolution typing of Enterococcus faecium. J Clin Microbiol 53:3788–3797

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Jong BC, Antonio M, Gagneux S (2010) Mycobacterium africanum—review of an important cause of human tuberculosis in West Africa. PLoS Negl Trop Dis 4:e744

    Article  PubMed  PubMed Central  Google Scholar 

  • Devault AM, Golding GB, Waglechner N, Enk JM, Kuch M, Tien JH, Shi M, Fisman DN, Dhody AN, Forrest S, Bos KI, Earn DJD, Holmes EC, Poinar HN (2014) Second-pandemic strain of Vibrio cholerae from the Philadelphia cholera outbreak of 1849. N Engl J Med 370:334–340

    Article  CAS  PubMed  Google Scholar 

  • Didelot X, Maiden MCJ (2010) Impact of recombination on bacterial evolution. Trends Microbiol 18:315–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Didelot X, Eyre D, Cule M, Ip C, Ansari A, Griffiths D, Vaughan A, O’Connor L, Golubchik T, Batty E, Piazza P, Wilson D, Bowden R, Donnelly P, Dingle K, Wilcox M, Walker S, Crook D, Peto T, Harding R (2012a) Microevolutionary analysis of Clostridium difficile genomes to investigate transmission. Genome Biol 13:R118

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Didelot X, Meric G, Falush D, Darling A (2012b) Impact of homologous and non-homologous recombination in the genomic evolution of Escherichia coli. BMC Genom 13:256

    Article  Google Scholar 

  • Didelot X, Walker AS, Peto TE, Crook DW, Wilson DJ (2016) Within-host evolution of bacterial pathogens. Nat Rev Micro 14:150–162

    Article  CAS  Google Scholar 

  • Doolittle WF (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14:307–311

    Article  CAS  PubMed  Google Scholar 

  • Drummond AJ, Pybus OG, Rambaut A, Forsberg R, Rodrigo AG (2003) Measurably evolving populations. Trends Ecol Evol 18:481–488

    Article  Google Scholar 

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ekblom R, Wolf JBW (2014) A field guide to whole-genome sequencing, assembly and annotation. Evol Appl 7:1026–1042

    Article  PubMed  PubMed Central  Google Scholar 

  • Engelthaler DM, Chiller T, Schupp JA, Colvin J, Beckstrom-Sternbergg SM, Driebe EM, Moses T, Tembe W, Sinari S, Beckstrom-Sternbergg JS, Christoforides A, Pearson JV, Capten J, Keim P, Peterson A, Tersahita D, Arunmozhi B (2011) Next-generation sequencing of Coccidioides immitis isolated during cluster investigation. Emerg Infect Dis 17:227–232

    Article  PubMed  PubMed Central  Google Scholar 

  • Espedido BA, Steen JA, Ziochos H, Grimmond SM, Cooper MA, Gosbell IB, Van Hal SJ, Jensen SO (2013) Whole genome sequence analysis of the first australian OXA-48-producing outbreak-associated Klebsiella pneumoniae isolates: the resistome and in vivo evolution. PLoS ONE 8:e59920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eyre DW, Golubchik T, Gordon NC, Bowden R, Piazza P, Batty EM, Ip CL, Wilson DJ, Didelot X, O’Connor L (2012) A pilot study of rapid benchtop sequencing of Staphylococcus aureus and Clostridium difficile for outbreak detection and surveillance. BMJ Open 2:e001124

    Article  PubMed  PubMed Central  Google Scholar 

  • Eyre DW, Cule ML, Griffiths D, Crook DW, Peto TEA, Walker AS, Wilson DJ (2013a) Detection of mixed infection from bacterial whole genome sequence data allows assessment of its role in Clostridium difficile transmission. PLoS Comput Biol 9:e1003059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eyre DW, Cule ML, Wilson DJ, Griffiths D, Vaughan A, O’Connor L, Ip CLC, Golubchik T, Batty EM, Finney JM, Wyllie DH, Didelot X, Piazza P, Bowden R, Dingle KE, Harding RM, Crook DW, Wilcox MH, Peto TEA, Walker AS (2013b) Diverse sources of C. difficile infection identified on whole-genome sequencing. N Engl J Med 369:1195–1205

    Article  CAS  PubMed  Google Scholar 

  • Farhat MR, Shapiro BJ, Kieser KJ, Sultana R, Jacobson KR, Victor TC et al (2013) Genomic analysis identifies targets of convergent positive selection in drug-resistant Mycobacterium tuberculosis. Nat Genet 45:1183–1189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feil EJ, Holmes EC, Bessen DE, Chan MS, Day NPJ, Enright MC, Goldstein R, Hood DW, Kalia A, Moore CE, Zhou J, Spratt BG (2001) Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc Nat Acad Sci U.S.A. 98:182–187

    Article  CAS  Google Scholar 

  • Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG (2004) eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 186:1518–1530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fields BS, Benson RF, Besser RE (2002) Legionella and Legionnaires’ disease: 25 years of investigation. Clin Microbiol Rev 15:506–526

    Article  PubMed  PubMed Central  Google Scholar 

  • Fittipaldi N, Tyrrell GJ, Low DE, Martin I, Lin D, Hari KL, Musser JM (2013) Integrated whole-genome sequencing and temporospatial analysis of a continuing group A Streptococcus epidemic. Emerg Microbes Infect 2:e13

    Article  PubMed  PubMed Central  Google Scholar 

  • Fitzpatrick MA, Ozer EA, Hauser AR (2016) Utility of whole-genome sequencing in characterizing Acinetobacter epidemiology and analyzing hospital outbreaks. J Clin Microbiol 54:593–612

    Article  PubMed  PubMed Central  Google Scholar 

  • Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, Sharrar RG, Harris J, Mallison GF, Martin SM, McDade JE, Shepard CC, Brachman PS (1977) Legionnaires’ disease: description of an epidemic of pneumonia. N Engl J Med 297:1189–1197

    Article  CAS  PubMed  Google Scholar 

  • Fraser C, Donnelly CA, Cauchemez S, Hanage WP, Van Kerkhove MD, Hollingsworth TD, Griffin J, Baggaley RF, Jenkins HE, Lyons EJ (2009) Pandemic potential of a strain of influenza A (H1N1): early findings. Science 324:1557–1561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaia V, Fry NK, Harrison TJ, Peduzzi R (2003) Sequence-based typing of Legionella pneumophila serogroup 1 offers the potential for true portability in legionellosis outbreak investigation. J Clin Microbiol 41:2932–2939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaia V, Fry NK, Afshar B, Luck PC, Meugnier H, Etienne J, Peduzzi R, Harrison TJ (2005) Consensus sequence-based scheme for epidemiological typing of clinical and environmental isolates of Legionella pneumophila. J Clin Microbiol 43:2047–2052

    Article  PubMed  PubMed Central  Google Scholar 

  • Gardy JL, Johnston JC, Sui SJH, Cook VJ, Shah L, Brodkin E, Rempel S, Moore R, Zhao Y, Holt R, Varhol R, Birol I, Lem M, Sharma MK, Elwood K, Jones SJM, Brinkman FSL, Brunham RC, Tang P (2011) Whole-genome squencing and social-network analysis of a tuberculosis outbreak. N Engl J Med 364:730–739

    Article  CAS  PubMed  Google Scholar 

  • General Directorate of Epidemiology MoHM, Pan American Health Organization, World Health Organization, Public Health Agency of Canada, CDC (United States) (2009) Outbreak of swine-origin Influenza A (H1N1) virus infection-Mexico, March–April 2009. Morb Mortal Wkly Rep 58:467–470

    Google Scholar 

  • Ghai R, Martin-Cuadrado AB, Molto AG, Heredia IG, Cabrera R, Martin J, Verdu M, Deschamps P, Moreira D, Lopez-Garcia P, Mira A, Rodriguez-Valera F (2010) Metagenome of the Mediterranean deep chlorophyll maximum studied by direct and fosmid library 454 pyrosequencing. ISME J 4:1154–1166

    Article  CAS  PubMed  Google Scholar 

  • Gilmour M, Graham M, Van Domselaar G, Tyler S, Kent H, Trout-Yakel K, Larios O, Allen V, Lee B, Nadon C (2010) High-throughput genome sequencing of two Listeria monocytogenes clinical isolates during a large foodborne outbreak. BMC Genom 11:120

    Article  CAS  Google Scholar 

  • Grad YH, Lipsitch M, Feldgarden M, Arachchi HM, Cerqueira GC, FitzGerald M, Godfrey P, Haas BJ, Murphy CI, Russ C (2012) Genomic epidemiology of the Escherichia coli O104: H4 outbreaks in Europe, 2011. Proc Nat Acad Sci U.S.A. 109:3065–3070

    Article  CAS  Google Scholar 

  • Grad YH, Godfrey P, Cerquiera GC, Mariani-Kurkdjian P, Gouali M, Bingen E, Shea TP, Haas BJ, Griggs A, Young S, Zeng Q, Lipsitch M, Waldor MK, Weill FX, Wortman JR, Hanage WP (2013) Comparative genomics of recent shiga toxin-producing Escherichia coli O104: H4: short-term evolution of an emerging pathogen. mBio 4

    Google Scholar 

  • Grad YH, Kirkcaldy RD, Trees D, Dordel J, Harris SR, Goldstein E, Weinstock H, Parkhill J, Hanage WP, Bentley S, Lipsitch M (2014) Genomic epidemiology of Neisseria gonorrhoeae with reduced susceptibility to cefixime in the USA: a retrospective observational study. Lancet Infect Dis 14:220–226

    Article  PubMed  PubMed Central  Google Scholar 

  • Guerra-Assunção JA, Crampin AC, Houben RMGJ, Mzembe T, Mallard K, Coll F, Khan P, Banda L, Chiwaya A, Pereira RPA, McNerney R, Fine PEM, Parkhill J, Clark TG, Glynn JR (2015) Large-scale whole genome sequencing of M. tuberculosis provides insights into transmission in a high prevalence area. eLife Sci 4:e05166

    Google Scholar 

  • Harris SR, Feil EJ, Holden MTG, Quail MA, Nickerson EK, Chantratita N, Gardete S, Tavares A, Day N, Lindsay JA, Edgeworth JD, de Lencastre H, Parkhill J, Peacock SJ, Bentley SD (2010) Evolution of MRSA during hospital transmission and intercontinental spread. Science 327:469–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harris SR, Clarke IN, Seth-Smith HMB, Solomon AW, Cutcliffe LT, Marsh P, Skilton RJ, Holland MJ, Mabey D, Peeling RW, Lewis DA, Spratt BG, Unemo M, Persson K, Bjartling C, Brunham R, de Vries HJC, Morre SA, Speksnijder A, Bebear CM, Clerc M, de Barbeyrac B, Parkhill J, Thomson NR (2012) Whole-genome analysis of diverse Chlamydia trachomatis strains identifies phylogenetic relationships masked by current clinical typing. Nat Genet 44:413–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harris SR, Cartwright EJ, Török ME, Holden MT, Brown NM, Ogilvy-Stuart AL, Ellington MJ, Quail MA, Bentley SD, Parkhill J, Peacock SJ (2013) Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect Dis 13:130–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasan NA, Choi SY, Eppinger M, Clark PW, Chen A, Alam M, Haley BJ, Taviani E, Hine E, Su Q, Tallon LJ, Prosper JB, Furth K, Hoq MM, Li H, Fraser-Liggett CM, Cravioto A, Huq A, Ravel J, Cebula TA, Colwell RR (2012) Genomic diversity of 2010 Haitian cholera outbreak strains. PNAS 109:E2010–E2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He M, Miyajima F, Roberts P, Ellison L, Pickard DJ, Martin MJ, Connor TR, Harris SR, Fairley D, Bamford KB, D’Arc S, Brazier J, Brown D, Coia JE, Douce G, Gerding D, Kim HJ, Koh TH, Kato H, Senoh M, Louie T, Michell S, Butt E, Peacock SJ, Brown NM, Riley T, Songer G, Wilcox M, Pirmohamed M, Kuijper E, Hawkey P, Wren BW, Dougan G, Parkhill J, Lawley TD (2013) Emergence and global spread of epidemic healthcare-associated Clostridium difficile. Nat Genet 45:109–113

    Article  CAS  PubMed  Google Scholar 

  • Hendriksen RS, Price LB, Schupp JM, Gillece JD, Kaas RS, Engelthaler DM, Bortolaia V, Pearson T, Waters AE, Upadhyay BP (2011) Population genetics of Vibrio cholerae from Nepal in 2010: evidence on the origin of the Haitian outbreak. mBio 2:e00157–11

    Google Scholar 

  • Holden MTG, Hauser H, Sanders M, Ngo TH, Cherevach I, Cronin A, Goodhead I, Mungall K, Quail MA, Price C, Rabbinowitsch E, Sharp S, Croucher NJ, Chieu TB, Thi Hoang Mai N, Diep TS, Chinh NT, Kehoe M, Leigh JA, Ward PN, Dowson CG, Whatmore AM, Chanter N, Iversen P, Gottschalk M, Slater JD, Smith HE, Spratt BG, Xu J, Ye C, Bentley S, Barrell BG, Schultsz C, Maskell DJ, Parkhill J (2009) Rapid evolution of virulence and drug resistance in the emerging zoonotic pathogen Streptococcus suis. PLoS ONE 4:e6072

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Holden MTG, Hsu LY, Kurt K, Weinert LA, Mather AE, Harris SR, Strommenger B, Layer F, Witte W, de Lencastre H, Skov R, Westh H, Zemlickova H, Coombs G, Kearns AM, Hill RLR, Edgeworth J, Gould I, Gant V, Cooke J, Edwards GF, McAdam PR, Templeton KE, McCann A, Zhou Z, Castillo-Ramirez S, Feil EJ, Hudson LO, Enright MC, Balloux F, Aanensen DM, Spratt BG, Fitzgerald JR, Parkhill J, Achtman M, Bentley SD, Nübel U (2013) A genomic portrait of the emergence, evolution and global spread of a methicillin resistant Staphylococcus aureus pandemic. Genome Res 23:653–664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holmes A, Allison L, Ward M, Dallman TJ, Clark R, Fawkes A, Murphy L, Hanson M (2015) Utility of whole-genome sequencing of Escherichia coli O157 for outbreak detection and epidemiological surveillance. J Clin Microbiol 53:3565–3573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holt KE, Parkhill J, Mazzoni CJ, Roumagnac P, Weill FX, Goodhead I, Rance R, Baker S, Maskell DJ, Wain J, Dolecek C, Achtman M, Dougan G (2008) High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Genet 40:987–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holt KE, Baker S, Weill FX, Holmes EC, Kitchen A, Yu J, Sangal V, Brown DJ, Coia JE, Kim DW, Choi SY, Kim SH, da Silveira WD, Pickard DJ, Farrar JJ, Parkhill J, Dougan G, Thomson NR (2012) Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat Genet 44:1056–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holt KE, Thieu Nga TV, Thanh DP, Vinh H, Kim DW, Vu Tra MP, Campbell JI, Hoang NVM, Vinh NT, Minh PV, Thuy CT, Nga TTT, Thompson C, Dung TTN, Nhu NTK, Vinh PV, Tuyet PTN, Phuc HL, Lien NTN, Phu BD, Ai NTT, Tien NM, Dong N, Parry CM, Hien TT, Farrar JJ, Parkhill J, Dougan G, Thomson NR, Baker S (2013) Tracking the establishment of local endemic populations of an emergent enteric pathogen. Proc Nat Acad Sci U.S.A. 110:17522–17527

    Article  CAS  Google Scholar 

  • Hornsey M, Loman N, Wareham DW, Ellington MJ, Pallen MJ, Turton JF, Underwood A, Gaulton T, Thomas CP, Doumith M (2011) Whole-genome comparison of two Acinetobacter baumannii isolates from a single patient, where resistance developed during tigecycline therapy. J Antimicrob Chemother 66:1499–1503

    Article  CAS  PubMed  Google Scholar 

  • Ioerger TR, Feng Y, Chen X, Dobos KM, Victor TC, Streicher EM, Warren RM, Van Pittius NCG, Helden PD, Sacchettini JC (2010) The non-clonality of drug resistance in Beijing-genotype isolates of Mycobacterium tuberculosis from the Western Cape of South Africa. BMC Genom 11:1

    Article  CAS  Google Scholar 

  • Jolley KA, Hill DMC, Bratcher HB, Harrison OB, Feavers IM, Parkhill J, Maiden MCJ (2012) Resolution of a meningococcal disease outbreak from whole-genome sequence data with rapid web-based analysis methods. J Clin Microbiol 50:3046–3053

    Article  PubMed  PubMed Central  Google Scholar 

  • Ju W, Cao G, Rump L, Strain E, Luo Y, Timme R, Allard M, Zhao S, Brown E, Meng J (2012) Phylogenetic analysis of non-O157 Shiga toxin-producing Escherichia coli by whole genome sequencing. J Clin Microbiol

    Google Scholar 

  • Kanamori H, Parobek CM, Weber DJ, Van Duin D, Rutala WA, Cairns BA, Juliano JJ (2016) Next-generation sequencing and comparative analysis of sequential outbreaks caused by multidrug-resistant Acinetobacter baumannii at a large academic burn center. Antimicrob Agents Chemother 60:1249–1257

    Article  CAS  PubMed Central  Google Scholar 

  • Kato-Maeda M, Ho C, Passarelli B, Banaei N, Grinsdale J, Flores L, Anderson J, Murray M, Rose G, Kawamura LM, Pourmand N, Tariq MA, Gagneux S, Hopewell PC (2013) Use of whole genome sequencing to determine the microevolution of Mycobacterium tuberculosis during an outbreak. PLoS ONE 8:e58235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kennemann L, Didelot X, Aebischer T, Kuhn S, Drescher B, Droege M, Reinhardt R, Correa P, Meyer TF, Josenhans C, Falush D, Suerbaum S (2011) Helicobacter pylori genome evolution during human infection. Proc Nat Acad Sci U.S.A. 108:5033–5038

    Article  CAS  Google Scholar 

  • Kinnevey PM, Shore AC, Mac Aogáin M, Creamer E, Brennan GI, Humphreys H, Rogers TR, O’Connell B, Coleman DC (2016) Enhanced tracking of nosocomial transmission of endemic sequence type 22 methicillin-resistant Staphylococcus aureus type iv isolates among patients and environmental sites by use of whole-genome sequencing. J Clin Microbiol 54:445–448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knetsch CW, Connor TR, Mutreja A, Van Dorp SM, Sanders IM, Browne HP, Harris D, Lipman L, Keessen EC, Corver J (2014) Whole genome sequencing reveals potential spread of Clostridium difficile between humans and farm animals in the Netherlands, 2002 to 2011. EuroSurveillance 19:30–41

    Article  Google Scholar 

  • Köser CU, Holden MTG, Ellington MJ, Cartwright EJP, Brown NM, Ogilvy-Stuart AL, Hsu LY, Chewapreecha C, Croucher NJ, Harris SR (2012) Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 366:2267–2275

    Article  PubMed  PubMed Central  Google Scholar 

  • Köser CU, Bryant JM, Becq J, Török ME, Ellington MJ, Marti-Renom MA, Carmichael AJ, Parkhill J, Smith GP, Peacock SJ (2013) Whole-genome sequencing for rapid susceptibility testing of M. tuberculosis. N Engl J Med 369:290–292

    Article  PubMed  CAS  Google Scholar 

  • Kwong JC, Mercoulia K, Tomita T, Easton M, Li HY, Bulach DM, Stinear TP, Seemann T, Howden BP (2016) Prospective whole-genome sequencing enhances national surveillance of Listeria monocytogenes. J Clin Microbiol 54:333–342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee RS, Radomski N, Proulx JF, Manry J, McIntosh F, Desjardins F, Soualhine H, Domenech P, Reed MB, Menzies D, Behr MA (2015) Reemergence and amplification of tuberculosis in the Canadian Arctic. J Infect Dis 211:1905–1914

    Article  PubMed  Google Scholar 

  • Lévesque S, Plante PL, Mendis N, Cantin P, Marchand G, Charest H, Raymond F, Huot C, Goupil-Sormany I, Desbiens F (2014) Genomic characterization of a large outbreak of Legionella pneumophila serogroup 1 strains in Quebec City, 2012. PLoS ONE 9:e103852

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lewis T, Loman NJ, Bingle L, Jumaa P, Weinstock GM, Mortiboy D, Pallen MJ (2010) High-throughput whole-genome sequencing to dissect the epidemiology of Acinetobacter baumannii isolates from a hospital outbreak. J Hosp Infect 75:37–41

    Article  CAS  PubMed  Google Scholar 

  • Lienau EK, Strain E, Wang C, Zheng J, Ottesen AR, Keys CE, Hammack TS, Musser SM, Brown EW, Allard MW, Cao G, Meng J, Stones R (2011) Identification of a salmonellosis outbreak by means of molecular sequencing. N Engl J Med 364:981–982

    Article  CAS  PubMed  Google Scholar 

  • Liu Q, Via LE, Luo T, Liang L, Liu X, Wu S, Shen Q, Wei W, Ruan X, Yuan X, Zhang G, Barry CE, Gao Q (2015) Within patient microevolution of Mycobacterium tuberculosis correlates with heterogeneous responses to treatment. Scientific reports 5:17507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loman NJ, Constantinidou C (2013) A culture-independent sequence-based metagenomics approach to the investigation of an outbreak of shiga-toxigenic Escherichia coli O104: H4. JAMA 309:1502–1510

    Article  CAS  PubMed  Google Scholar 

  • Loman NJ, Pallen MJ (2015). Twenty years of bacterial genome sequencing. Nat Rev Micro

    Google Scholar 

  • Loman NJ, Gladstone RA, Constantinidou C, Tocheva AS, Jefferies JM, Faust SN, OΓÇÖConnor L, Chan J, Pallen MJ, Clarke SC (2013) Clonal expansion within pneumococcal serotype 6C after use of seven-valent vaccine. PLoS ONE 8:e64731

    Google Scholar 

  • Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA, Feavers IM, Achtman M, Spratt BG (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Nat Acad Sci U.S.A. 95:3140–3145

    Article  CAS  Google Scholar 

  • Maixner F, Krause-Kyora B, Turaev D, Herbig A, Hoopmann MR, Hallows JL, Kusebauch U, Vigl EE, Malfertheiner P, Megraud F, OΓÇÖSullivan N, Cipollini G, Coia V, Samadelli M, Engstrand L, Linz B, Moritz RL, Grimm R, Krause J, Nebel A, Moodley Y, Rattei T, Zink A (2016) The 5300-year-old Helicobacter pylori genome of the Iceman. Science 351:162–165

    Google Scholar 

  • Mathers AJ, Peirano G, Pitout JDD (2015) The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant enterobacteriaceae. Clin Microbiol Rev 28:565–591

    Article  PubMed  PubMed Central  Google Scholar 

  • McAdam PR, Templeton KE, Edwards GF, Holden MTG, Feil EJ, Aanensen DM, Bargawi HJA, Spratt BG, Bentley SD, Parkhill J, Enright MC, Holmes A, Girvan EK, Godfrey PA, Feldgarden M, Kearns AM, Rambaut A, Robinson DA, Fitzgerald JR (2012) Molecular tracing of the emergence, adaptation, and transmission of hospital-associated methicillin-resistant Staphylococcus aureus. Proc Nat Acad Sci U.S.A. 109:9107–9112

    Article  CAS  Google Scholar 

  • McAdam P, Vander broek C, Lindsay D, Ward M, Hanson M, Gillies M, Watson M, Stevens J, Edwards G, Fitzgerald R (2014) Gene flow in environmental Legionella pneumophila leads to genetic and pathogenic heterogeneity within a Legionnaires’ disease outbreak. Genome Biol 15:504

    Google Scholar 

  • McDonnell J, Dallman T, Atkin S, Turbitt DA, Connor TR, Grant KA, Thomson NR, Jenkins C (2013) Retrospective analysis of whole genome sequencing compared to prospective typing data in further informing the epidemiological investigation of an outbreak of Shigella sonnei in the UK. Epidemiol Infect 141:2568–2575

    Google Scholar 

  • Medini D, Serruto D, Parkhill J, Relman DA, Donati C, Moxon R, Falkow S, Rappuoli R (2008) Microbiology in the post-genomic era. Nat Rev Micro 6:419–430

    CAS  Google Scholar 

  • Mellmann A, Harmsen D, Cummings CA, Zentz EB, Leopold SR, Rico A, Prior K, Szczepanowski R, Ji Y, Zhang W (2011) Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104: H4 outbreak by rapid next generation sequencing technology. PLoS ONE 6:e22751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mendum T, Schuenemann V, Roffey S, Taylor G, Wu H, Singh P, Tucker K, Hinds J, Cole S, Kierzek A, Nieselt K, Krause J, Stewart G (2014) Mycobacterium leprae genomes from a British medieval leprosy hospital: towards understanding an ancient epidemic. BMC Genom 15:270

    Article  Google Scholar 

  • Metzker ML (2010) Sequencing technologies—the next generation. Nat Rev Genet 11:31–46

    Article  CAS  PubMed  Google Scholar 

  • Mortimer PP (2003) Five postulates for resolving outbreaks of infectious disease. J Med Microbiol 52:447–451

    Article  PubMed  Google Scholar 

  • Mutreja A, Kim DW, Thomson NR, Connor TR, Lee JH, Kariuki S, Croucher NJ, Choi SY, Harris SR, Lebens M, Niyogi SK, Kim EJ, Ramamurthy T, Chun J, Wood JLN, Clemens JD, Czerkinsky C, Nair GB, Holmgren J, Parkhill J, Dougan G (2011) Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477:462–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mwangi MM, Wu SW, Zhou Y, Sieradzki K, de Lencastre H, Richardson P, Bruce D, Rubin E, Myers E, Siggia ED, Tomasz A (2007) Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc Nat Acad Sci U.S.A. 104:9451–9456

    Article  CAS  Google Scholar 

  • Niemann S, Köser CU, Gagneux S, Plinke C, Homolka S, Bignell H, Carter RJ, Cheetham RK, Cox A, Gormley NA, Kokko-Gonzales P, Murray LJ, Rigatti R, Smith VP, Arends FPM, Cox HS, Smith G, Archer JAC (2009) Genomic diversity among drug sensitive and multidrug resistant isolates of Mycobacterium tuberculosis with identical DNA fingerprints. PLoS ONE 4:e7407

    Google Scholar 

  • Nübel U, Nachtnebel M, Falkenhorst G, Benzler J, Hecht J, Kube M, Bröcker F, Moelling K, Bührer C, Gastmeier P, Piening B, Behnke M, Dehnert M, Layer F, Witte W, Eckmanns T (2013) MRSA transmission on a neonatal intensive care unit: epidemiological and genome-based phylogenetic analyses. PLoS ONE 8:e54898

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Okoro CK, Kingsley RA, Connor TR, Harris SR, Parry CM, Al-Mashhadani MN, Kariuki S, Msefula CL, Gordon MA, de Pinna E (2012) Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet 44:1215–1223

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Onori R, Gaiarsa S, Comandatore F, Pongolini S, Brisse S, Colombo A, Cassani G, Marone P, Grossi P, Minoja G, Bandi C, Sassera D, Toniolo A (2015) Tracking nosocomial Klebsiella pneumoniae infections and outbreaks by whole-genome analysis: small-scale Italian scenario within a single hospital. J Clin Microbiol 53:2861–2868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parwati I, Van Crevel R, Van Soolingen D (2010) Possible underlying mechanisms for successful emergence of the Mycobacterium tuberculosis Beijing genotype strains. Lancet Infect Dis 10:103–111

    Article  PubMed  Google Scholar 

  • Paterson GK, Harrison EM, Murray GGR, Welch JJ, Warland JH, Holden MTG, Morgan FJE, Ba X, Koop G, Harris SR, Maskell DJ, Peacock SJ, Herrtage ME, Parkhill J, Holmes MA (2015) Capturing the cloud of diversity reveals complexity and heterogeneity of MRSA carriage, infection and transmission. Nat Commun 6:6560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez-Lago L, Comas I, Navarro Y, González-Candelas F, Herranz M, Bouza E, García de Viedma D (2014) Whole genome sequencing analysis of intrapatient microevolution in Mycobacterium tuberculosis: potential impact on the inference of tuberculosis transmission. J Infect Dis 209:98–108

    Article  PubMed  Google Scholar 

  • Pérez-Lago L, Martínez Lirola M, Herranz M, Comas I, Bouza E, García-de-Viedma D (2015) Fast and low-cost decentralized surveillance of transmission of tuberculosis based on strain-specific PCRs tailored from whole genome sequencing data: a pilot study. Clin Microbiol Infect 21:249

    PubMed  Google Scholar 

  • Pinholt M, Larner-Svensson H, Littauer P, Moser CE, Pedersen M, Lemming LE, Ejlertsen T, Söndergaard TS, Holzknecht BJ, Justesen US, Dzajic E, Olsen SS, Nielsen JB, Worning P, Hammerum AM, Westh H, Jakobsen L (2015) Multiple hospital outbreaks of vanA Enterococcus faecium in Denmark, 2012–13, investigated by WGS, MLST and PFGE. J Antimicrob Chemother 70:2474–2482

    Article  CAS  PubMed  Google Scholar 

  • Price JR, Golubchik T, Cole K, Wilson DJ, Crook DW, Thwaites GE, Bowden R, Sarah Walker A, Peto TEA, Paul J, Llewelyn MJ (2014) Whole-genome sequencing shows that patient-to-patient transmission rarely accounts for acquisition of Staphylococcus aureus on an intensive care unit. Clin Infect Dis 58:609–618

    Article  PubMed  Google Scholar 

  • Qin T, Zhang W, Liu W, Zhou H, Ren H, Shao Z, Lan R, Xu J (2016) Population structure and minimum core genome typing of Legionella pneumophila. Sci Rep 6:21356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quick J, Ashton P, Calus S, Chatt C, Gossain S, Hawker J, Nair S, Neal K, Nye K, Peters T, de Pinna E, Robinson E, Struthers K, Webber M, Catto A, Dallman T, Hawkey P, Loman N (2015) Rapid draft sequencing and real-time nanopore sequencing in a hospital outbreak of Salmonella. Genome Biol 16:114

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Quick J, Loman NJ, Duraffour S, Simpson JT, Severi E, Cowley L, Bore JA, Koundouno R, Dudas G, Mikhail A, Ouédraogo N, Afrough B, Bah A, Baum JHJ, Becker-Ziaja B, Boettcher JP, Cabeza-Cabrerizo M, Camino-Sánchez Á, Carter LL, Doerrbecker J, Enkirch T, Dorival IGa, Hetzelt N, Hinzmann J, Holm T, Kafetzopoulou LE, Koropogui M, Kosgey A, Kuisma E, Logue CH, Mazzarelli A, Meisel S, Mertens M, Michel J, Ngabo D, Nitzsche K, Pallasch E, Patrono LV, Portmann J, Repits JG, Rickett NY, Sachse A, Singethan K, Vitoriano Is, Yemanaberhan RL, Zekeng EG, Racine T, Bello A, Sall AA, Faye O, Faye O, Magassouba N, Williams CV, Amburgey V, Winona L, Davis E, Gerlach J, Washington F, Monteil V, Jourdain M, Bererd M, Camara A, Somlare H, Camara A, Gerard M, Bado G, Baillet B, Delaune D, Nebie KY, Diarra A, Savane Y, Pallawo RB, Gutierrez GJ, Milhano N, Roger I, Williams CJ, Yattara F, Lewandowski K, Taylor J, Rachwal P, Turner J, Pollakis G, Hiscox JA, Matthews DA, Shea MKO, Johnston AM, Wilson D, Hutley E, Smit E, Di Caro A, Wölfel R, Stoecker K, Fleischmann E, Gabriel M, Weller SA, Koivogui L, Diallo B, Keïta S, Rambaut A, Formenty P, Günther S, Carroll MW (2016). Real-time, portable genome sequencing for Ebola surveillance. Nature

    Google Scholar 

  • Rasmussen S, Allentoft ME, Nielsen K, Orlando L, Sikora M, Sjögren KG, Pedersen AG, Schubert M, Van Dam A, Kapel CMO, Nielsen HB, Brunak S, Avetisyan P, Epimakhov A, Khalyapin MV, Gnuni A, Kriiska A, Lasak I, Metspalu M, Moiseyev V, Gromov A, Pokutta D, Saag L, Varul L, Yepiskoposyan L, Sicheritz-Pontén T, Foley RA, Lahr MM, Nielsen R, Kristiansen K, Willerslev E (2015) Early divergent strains of Yersinia pestis in Eurasia 5000 years ago. Cell 163:571–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Read TD, Salzberg SL, Pop M, Shumway M, Umayam L, Jiang L, Holtzapple E, Busch JD, Smith KL, Schupp JM, Solomon D, Keim P, Fraser CM (2002) Comparative genome sequencing for discovery of novel polymorphisms in Bacillus anthracis. Science 296:2028–2033

    Article  CAS  PubMed  Google Scholar 

  • Reuter S, Ellington MJ, Cartwright EP (2013a) Rapid bacterial whole-genome sequencing to enhance diagnostic and public health microbiology. JAMA Intern Med 173:1397–1404

    Article  PubMed  PubMed Central  Google Scholar 

  • Reuter S, Harrison TG, Köser CU, Ellington MJ, Smith GP, Parkhill J, Peacock SJ, Bentley SD, Török ME (2013b) A pilot study of rapid whole-genome sequencing for the investigation of a Legionella outbreak. BMJ Open 3

    Google Scholar 

  • Reuter S, Török ME, Holden MTG, Reynolds R, Raven KE, Blane B, Donker T, Bentley SD, Aanensen DM, Grundmann H, Feil EJ, Spratt BG, Parkhill J, Peacock SJ (2016) Building a genomic framework for prospective MRSA surveillance in the United Kingdom and the Republic of Ireland. Genome Res 26:263–270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rinder H, Mieskes KT, Löscher T (2001) Heteroresistance in Mycobacterium tuberculosis. Int J Tuberc Lung Dis 5:339–345

    CAS  PubMed  Google Scholar 

  • Roetzer A, Diel R, Kohl TA, Rückert C, Nübel U, Blom J, Wirth T, Jaenicke S, Schuback S, Rüsch-Gerdes S, Supply P, Kalinowski J, Niemann S (2013) Whole genome sequencing versus traditional genotyping for investigation of a Mycobacterium tuberculosis outbreak: a longitudinal molecular epidemiological study. PLoS Med 10:e1001387

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosenberg NA, Pritchard JK, Weber JL, Cann HM, Kidd KK, Zhivotovsky LA, Feldman MW (2002) Genetic structure of human populations. Science 298:2381–2385

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Busó L, Comas I, Jorques G, González-Candelas F (2014) Recombination drives genome evolution in outbreak-related Legionella pneumophila isolates. Nat Genet 46:1205–1211

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Busó L, Guiral S, Crespi S, Moya V, Camaró ML, Olmos P, Adrián F, Morera V, González Morán F, Vanaclocha H, González-Candelas F (2016) Genomic investigation of a legionellosis outbreak in a persistently colonized hotel. Front Microbiol 6:1556

    Article  PubMed  PubMed Central  Google Scholar 

  • Sandegren L, Groenheit R, Koivula T, Ghebremichael S, Advani A, Castro E, Pennhag A, Hoffner S, Mazurek J, Pawlowski A, Kan B, Bruchfeld J, Melefors Ö, Källenius G (2011) Genomic stability over 9 Years of an Isoniazid resistant Mycobacterium tuberculosis outbreak strain in Sweden. PLoS ONE 6:e16647

    Google Scholar 

  • Schlüter A, Bekel T, Diaz NN, Dondrup M, Eichenlaub R, Gartemann KH, Krahn I, Krause L, Krömeke H, Kruse O, Mussgnug JH, Neuweger H, Niehaus K, Pühler A, Runte KJ, Szczepanowski R, Tauch A, Tilker A, Viehöver P, Goesmann A (2008a) The metagenome of a biogas-producing microbial community of a production-scale biogas plant fermenter analysed by the 454-pyrosequencing technology. J Biotechnol 136:77–90

    Article  PubMed  CAS  Google Scholar 

  • Schlüter A, Krause L, Szczepanowski R, Goesmann A, Pühler A (2008b) Genetic diversity and composition of a plasmid metagenome from a wastewater treatment plant. J Biotechnol 136:65–76

    Article  PubMed  CAS  Google Scholar 

  • Schmid D, Allerberger F, Huhulescu S, Pietzka A, Amar C, Kleta S, Prager R, Preussel K, Aichinger E, Mellmann A (2014) Whole genome sequencing as a tool to investigate a cluster of seven cases of listeriosis in Austria and Germany, 2011–2013. Clin Microbiol Infect 20:431–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuenemann VJ, Singh P, Mendum TA, Krause-Kyora B, Jäger G, Bos KI, Herbig A, Economou C, Benjak A, Busso P, Nebel A, Boldsen JL, Kjellström A, Wu H, Stewart GR, Taylor GM, Bauer P, Lee OYC, Wu HHT, Minnikin DE, Besra GS, Tucker K, Roffey S, Sow SO, Cole ST, Nieselt K, Krause J (2013) Genome-wide comparison of medieval and modern Mycobacterium leprae. Science 341:179–183

    Article  CAS  PubMed  Google Scholar 

  • Schürch AC, Kremer K, Kiers A, Daviena O, Boeree MJ, Siezen RJ, Smith NH, Van Soolingen D (2010) The tempo and mode of molecular evolution of Mycobacterium tuberculosis at patient-to-patient scale. Infect Genet Evol 10:108–114

    Article  PubMed  Google Scholar 

  • Senn L, Clerc O, Zanetti G, Basset P, Prod’hom G, Gordon NC, Sheppard AE, Crook DW, James R, Thorpe HA, Feil EJ, Blanc DS (2016) The stealthy superbug: the role of asymptomatic enteric carriage in maintaining a long-term hospital outbreak of ST228 Methicillin-Resistant Staphylococcus aureus. mBio 7

    Google Scholar 

  • Seth-Smith HMB, Harris SR, Skilton RJ, Radebe FM, Golparian D, Shipitsyna E, Duy PT, Scott P, Cutcliffe LT, O’Neill C, Parmar S, Pitt R, Baker S, Ison CA, Marsh P, Jalal H, Lewis DA, Unemo M, Clarke IN, Parkhill J, Thomson NR (2013) Whole-genome sequences of Chlamydia trachomatis directly from clinical samples without culture. Genome Res 23:855–866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shah MA, Mutreja A, Thimson N, Baker S, Parkhill J, Dougan G, Bokhari H, Wren BW (2014) Genomic epidemiology of Vibrio cholerae O1 associated with floods, Pakistan, 2010. Emerg Infect Dis 20:13–20

    Article  PubMed  PubMed Central  Google Scholar 

  • Smit PW, Vasankari T, Aaltonen H, Haanperä M, Casali N, Marttila H, Marttila J, Ojanen P, Ruohola A, Ruutu P, Drobniewski F, Lyytikäinen O, Soini H (2015) Enhanced tuberculosis outbreak investigation using whole genome sequencing and IGRA. Eur Respir J 45:276–279

    Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Snyder LA, Loman NJ, Faraj LA, Levi K, Weinstock G, Boswell TC, Pallen MJ, Ala’Aldeen A (2013) Epidemiological investigation of Pseudomonas aeruginosa isolates from a six-year-long hospital outbreak using high-throughput whole genome sequencing. EuroSurveillance 18:20611

    Article  PubMed  Google Scholar 

  • Stucki D, Ballif M, Bodmer T, Coscolla M, Maurer AM, Droz S, Butz C, Borrell S, Längle C, Feldmann J, Furrer H, Mordasini C, Helbling P, Rieder HL, Egger M, Gagneux S, Fenner L (2015) Tracking a tuberculosis outbreak over 21 years: strain-specific single-nucleotide polymorphism typing combined with targeted whole-genome sequencing. J Infect Dis 211:1306–1316

    PubMed  Google Scholar 

  • Sun G, Luo T, Yang C, Dong X, Li J, Zhu Y, Zheng H, Tian W, Wang S, Barry CE, Mei J, Gao Q (2012) Dynamic population changes in Mycobacterium tuberculosis during acquisition and fixation of drug resistance in patients. J Infect Dis 206:1724–1733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor AJ, Lappi V, Wolfgang WJ, Lapierre P, Palumbo MJ, Medus C, Boxrud D (2015) Characterization of foodborne outbreaks of Salmonella enterica serovar enteritidis with whole-genome sequencing single nucleotide polymorphism-based analysis for surveillance and outbreak detection. J Clin Microbiol 53:3334–3340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Török ME, Peacock SJ (2012) Rapid whole-genome sequencing of bacterial pathogens in the clinical microbiology laboratory-pipe dream or reality? J Antimicrob Chemother 67:2307–2308

    Article  PubMed  CAS  Google Scholar 

  • Török ME, Reuter S, Bryant J, Köser CU, Stinchcombe SV, Nazareth B, Ellington MJ, Bentley SD, Smith GP, Parkhill J, Peacock SJ (2013) Rapid whole-genome sequencing for investigation of a suspected tuberculosis outbreak. J Clin Microbiol 51:611–614

    Article  PubMed  PubMed Central  Google Scholar 

  • Underwood A, Jones G, Mentasti M, Fry N, Harrison T (2013a) Comparison of the Legionella pneumophila population structure as determined by sequence-based typing and whole genome sequencing. BMC Microbiol 13:302

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Underwood AP, Dallman T, Thomson NR, Williams M, Harker K, Perry N, Adak B, Willshaw G, Cheasty T, Green J (2013b) Public health value of next-generation DNA sequencing of enterohemorrhagic Escherichia coli isolates from an outbreak. J Clin Microbiol 51:232–237

    Article  PubMed  PubMed Central  Google Scholar 

  • Urwin R, Maiden MCJ (2003) Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol 11:479–487

    Article  CAS  PubMed  Google Scholar 

  • Vos M, Didelot X (2009) A comparison of homologous recombination rates in bacteria and archaea. ISME J 3:199–208

    Article  CAS  PubMed  Google Scholar 

  • Wagner DM, Klunk J, Harbeck M, Devault A, Waglechner N, Sahl JW, Enk J, Birdsell DN, Kuch M, Lumibao C, Poinar D, Pearson T, Fourment M, Golding B, Riehm JM, Earn DJD, DeWitte S, Rouillard JM, Grupe G, Wiechmann I, Bliska JB, Keim PS, Scholz HC, Holmes EC, Poinar H (2014) Yersinia pestis and the Plague of Justinian 541–543 AD: a genomic analysis. Lancet Infect Dis 14:319–326

    Article  PubMed  Google Scholar 

  • Walker MJ, Beatson SA (2012) Outsmarting outbreaks. Science 338:1161–1162

    Article  PubMed  Google Scholar 

  • Walker TM, Monk P, Grace Smith E, Peto TEA (2013a) Contact investigations for outbreaks of Mycobacterium tuberculosis: advances through whole genome sequencing. Clin Microbiol Infect 19:796–802

    Article  CAS  PubMed  Google Scholar 

  • Walker TM, Ip CL, Harrell RH, Evans JT, Kapatai G, Dedicoat MJ, Eyre DW, Wilson DJ, Hawkey PM, Crook DW, Parkhill J, Harris D, Walker AS, Bowden R, Monk P, Smith EG, Peto TE (2013b) Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis 13:137–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walker TM, Lalor MK, Broda A, Ortega LS, Morgan M, Parker L, Churchill S, Bennett K, Golubchik T, Giess AP, Del Ojo Elias C, Jeffery KJ, Bowler ICJW, Laurenson IF, Barrett A, Drobniewski F, McCarthy ND, Anderson LF, Abubakar I, Thomas HL, Monk P, Smith EG, Walker AS, Crook DW, Peto TEA, Conlon CP (2014) Assessment of Mycobacterium tuberculosis transmission in Oxfordshire, UK, 2007–12, with whole pathogen genome sequences: an observational study. Lancet Respir Med 2:285–292

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 clonal complex 398. Appl Environ Microbiol 80:7275–7282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • WHO (2014). Global tubreculosis report, 2014

    Google Scholar 

  • Witney AA, Gould KA, Pope CF, Bolt F, Stoker NG, Cubbon MD, Bradley CR, Fraise A, Breathnach AS, Butcher PD, Planche TD, Hinds J (2014) Genome sequencing and characterization of an XDR ST111 serotype O12 hospital outbreak strain of Pseudomonas aeruginosa. Clin Microbiol Infect

    Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yates TA, Khan PY, Knight GM, Taylor JG, McHugh TD, Lipman M, White RG, Cohen T, Cobelens FG, Wood R, Moore DAJ, Abubakar I (2016) The transmission of Mycobacterium tuberculosis in high burden settings. Lancet Infect Dis 16:227–238

    Article  PubMed  Google Scholar 

  • Young BC, Golubchik T, Batty EM, Fung R, Larner-Svensson H, Votintseva AA, Miller RR, Godwin H, Knox K, Everitt RG (2012) Evolutionary dynamics of Staphylococcus aureus during progression from carriage to disease. Proc Nat Acad Sci U.S.A. 109:4550–4555

    Article  CAS  Google Scholar 

  • Zakour NLB, Venturini C, Beatson SA, Walker MJ (2012) Analysis of a Streptococcus pyogenes puerperal sepsis cluster by use of whole-genome sequencing. J Clin Microbiol 50:2224–2228

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou Y, Gao H, Mihindukulasuriya K, Rosa P, Wylie K, Vishnivetskaya T, Podar M, Warner B, Tarr P, Nelson D, Fortenberry JD, Holland M, Burr S, Shannon W, Sodergren E, Weinstock G (2013) Biogeography of the ecosystems of the healthy human body. Genome Biol 14:R1

    Google Scholar 

Download references

Acknowledgements

We thank Dr. Pierre Pontarotti for his kind invitation to write this chapter. This work has been funded by project BFU2014-58656-R from MINECO (Spanish Government) to FGC. IC is supported by Ramón y Cajal Spanish research grant RYC-2012-10627, MINECO research grant SAF2013-43521-R, and the European Research Council (ERC) (638553-TB-ACCELERATE). BB has been recipient of a Beca de Colaboración from the Spanish Ministerio de Educación y Cultura.

Author information

Authors and Affiliations

  1. Unidad Mixta “Infección y Salud Pública” FISABIO/CSISP—Universidad de Valencia/Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Valencia, Spain

    Leonor Sánchez-Busó, Iñaki Comas, Beatriz Beamud, Neris García-González, Marta Pla-Díaz & Fernando González-Candelas

  2. CIBER en Epidemiología y Salud Pública, Valencia, Spain

    Iñaki Comas & Fernando González-Candelas

  3. Pathogen Genomics, The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Cambridgeshire, UK

    Leonor Sánchez-Busó

  4. Instituto de Biomedicina, CSCIC, Valencia, Spain

    Iñaki Comas

  5. Evolución y Salud—Instituto Cavanilles Biodiversidad y Biología Evolutiva, Universidad de Valencia, c/Catedrático José Beltrán 2, 46980, Valencia, Paterna, Spain

    Fernando González-Candelas

Authors
  1. Leonor Sánchez-Busó
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Iñaki Comas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Beatriz Beamud
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Neris García-González
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marta Pla-Díaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fernando González-Candelas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fernando González-Candelas .

Editor information

Editors and Affiliations

  1. CNRS, Laboratoire Evolution Biologique et Modélisation, Université d’Aix-Marseille, Marseille, France

    Pierre Pontarotti

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Sánchez-Busó, L., Comas, I., Beamud, B., García-González, N., Pla-Díaz, M., González-Candelas, F. (2016). Genomic Analysis of Bacterial Outbreaks. In: Pontarotti, P. (eds) Evolutionary Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-41324-2_13

Download citation

Publish with us

Policies and ethics

Search

Navigation