High-throughput sequencing for the study of bacterial pathogen biology

Current Opinion in Microbiology

Volumn 19, Issue 1, 2014, Pages 106-113

  McAdam, Paul ^a   Richardson, Emily ^a   Fitzgerald, Ross ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL INFECTION; BACTERIAL LOAD; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL TRANSMISSION; BACTERIAL VIRULENCE; BACTERIUM IDENTIFICATION; EPIDEMIC; EPIDEMIOLOGICAL MONITORING; EVOLUTION; GENETIC ASSOCIATION; HIGH THROUGHPUT SEQUENCING; HOST PATHOGEN INTERACTION; HUMAN; INFECTION CONTROL; MOLECULAR CLONING; MOLECULAR PATHOLOGY; NONHUMAN; PATHOGENESIS; REVIEW; BACTERIUM; CLASSIFICATION; DNA SEQUENCE; GENETICS; PATHOGENICITY; PROCEDURES;

BACTERIA; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; SEQUENCE ANALYSIS, DNA;

EID: 84904281211     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2014.06.002     Document Type: Review

References (76)

1. Loman N.J., Constantinidou C., Chan J.Z.M., Halachev M., Sergeant M., Penn C.W., Robinson E.R., Pallen M.J. High-throughput bacterial genome sequencing: an embarrassment of choice, a world of opportunity. Nat Rev Microbiol 2012, 10:599-606.
2. Loman N.J., Misra R.V., Dallman T.J., Constantinidou C., Gharbia S.E., Wain J., Pallen M.J. Performance comparison of benchtop high-throughput sequencing platforms. Nat Biotechnol 2012, 30:434-439.
3. Eyre D.W., Golubchik T., Gordon N.C., Bowden R., Piazza P., Batty E.M., Ip C.L.C., Wilson D.J., Didelot X., O'Connor L., et al. A pilot study of rapid benchtop sequencing of Staphylococcus aureus and Clostridium difficile for outbreak detection and surveillance. BMJ Open 2012, 2.
4. Filiatrault M.J. Progress in prokaryotic transcriptomics. Curr Opin Microbiol 2011, 14:579-586.
5. Croucher N.J., Thomson N.R. Studying bacterial transcriptomes using RNA-seq. Curr Opin Microbiol 2010, 13:619-624.
6. Van Opijnen T., Bodi K.L., Camilli A. Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms. Nat Methods 2009, 6:767-772.
7. Langridge G.C., Phan M.D., Turner D.J., Perkins T.T., Parts L., Haase J., Charles I., Maskell D.J., Peters S.E., Dougan G., et al. Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Res 2009, 19:2308-2316.
8. Goodman A.L., McNulty N.P., Zhao Y., Leip D., Mitra R.D., Lozupone C.A., Knight R., Gordon J.I. Identifying genetic determinants needed to establish a human gut symbiont in its habitat. Cell Host Microbe 2009, 6:279-289.
9. Gawronski J.D., Wong S.M.S., Giannoukos G., Ward D.V., Akerley B.J. Tracking insertion mutants within libraries by deep sequencing and a genome-wide screen for Haemophilus genes required in the lung. Proc Natl Acad Sci U S A 2009, 106:16422-16427.
10. Van Opijnen T., Camilli A. Transposon insertion sequencing: a new tool for systems-level analysis of microorganisms. Nat Rev Microbiol 2013, 11.
11. Barquist L., Boinett C.J., Cain A.K. Approaches to querying bacterial genomes with transposon-insertion sequencing. RNA Biol 2013, 10:1161-1169.
12. Bryant J.M., Grogono D.M., Greaves D., Foweraker J., Roddick I., Inns T., Reacher M., Haworth C.S., Curran M.D., Harris S.R., et al. Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet 2013, 381:1551-1560.
13. Golubchik T., Batty E.M., Miller R.R., Farr H., Young B.C., Larner-Svensson H., Fung R., Godwin H., Knox K., Votintseva A., et al. Within-host evolution of Staphylococcus aureus during asymptomatic carriage. PLoS ONE 2013, 8:e61319.
14. Young B.C., Golubchik T., Batty E.M., Fung R., Larner-Svensson H., Votintseva A.A., Miller R.R., Godwin H., Knox K., Everitt R.G., et al. Evolutionary dynamics of Staphylococcus aureus during progression from carriage to disease. Proc Natl Acad Sci U S A 2012, 10.1073/pnas.1113219109.
15. Lieberman T.D., Michel J.-B., Aingaran M., Potter-Bynoe G., Roux D., Davis M.R., Skurnik D., Leiby N., LiPuma J.J., Goldberg J.B., et al. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 2011, 43:1275-1280.
16. Ford C.B., Lin P.L., Chase M.R., Shah R.R., Iartchouk O., Galagan J., Mohaideen N., Ioerger T.R., Sacchettini J.C., Lipsitch M., et al. Use of whole genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection. Nat Genet 2011, 43:482-486.
17. Harris S.R., Cartwright E.J., Török M.E., Holden M.T., Brown N.M., Ogilvy-Stuart A.L., Ellington M.J., Quail M.A., Bentley S.D., Parkhill J., et al. Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect Dis 2013, 13:130-136.
18. McAdam P.R., Holmes A., Templeton K.E., Fitzgerald J.R. Adaptive evolution of Staphylococcus aureus during chronic endobronchial infection of a cystic fibrosis patient. PLoS ONE 2011, 6:e24301.
19. Lieberman T.D., Flett K.B., Yelin I., Martin T.R., McAdam A.J., Priebe G.P., Kishony R. Genetic variation of a bacterial pathogen within individuals with cystic fibrosis provides a record of selective pressures. Nat Genet 2013, 46(1):82-87.
20. Kreutzfeldt K.M., McAdam P.R., Claxton P., Holmes A., Seagar A.L., Laurenson I.F., Fitzgerald J.R. Molecular longitudinal tracking of Mycobacterium abscessus spp. during chronic infection of the human lung. PLoS ONE 2013, 8:e63237.
21. Pawlik A., Garnier G., Orgeur M., Tong P., Lohan A., Le Chevalier F., Sapriel G., Roux A.-L., Conlon K., Honoré N., et al. Identification and characterization of the genetic changes responsible for the characteristic smooth-to-rough morphotype alterations of clinically persistent Mycobacterium abscessus. Mol Microbiol 2013, 10.1111/mmi.12387.
22. Mwangi M.M., Wu S.W., Zhou Y., Sieradzki K., de Lencastre H., Richardson P., Bruce D., Rubin E., Myers E., Siggia E.D., et al. Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc Natl Acad Sci U S A 2007, 104:9451-9456.
23. Howden B.P., McEvoy C.R., Allen D.L., Chua K., Gao W., Harrison P.F., Bell J., Coombs G., Bennett-Wood V., Porter J.L., et al. Evolution of multidrug resistance during Staphylococcus aureus infection involves mutation of the essential two component regulator WalKR. PLoS Pathog 2011, 7:e1002359.
24. Zdziarski J., Brzuszkiewicz E., Wullt B., Liesegang H., Biran D., Voigt B., Grönberg-Hernandez J., Ragnarsdottir B., Hecker M., Ron E.Z., et al. Host imprints on bacterial genomes-rapid, divergent evolution in individual patients. PLoS Pathog 2010, 6:e1001078.
25. Salipante S.J., Sengupta D.J., Rosenthal C., Costa G., Spangler J., Sims E.H., Jacobs M.A., Miller S.I., Hoogestraat D.R., Cookson B.T., et al. Rapid 16S rRNA next-generation sequencing of polymicrobial clinical samples for diagnosis of complex bacterial infections. PLoS ONE 2013, 8:e65226.
26. Blainey P.C., Milla C.E., Cornfield D.N., Quake S.R. Quantitative analysis of the human airway microbial ecology reveals a pervasive signature for cystic fibrosis. Sci Transl Med 2012, 4:153ra130.
27. Willner D., Furlan M., Haynes M., Schmieder R., Angly F.E., Silva J., Tammadoni S., Nosrat B., Conrad D., Rohwer F. Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS ONE 2009, 4:e7370.
28. Modi S.R., Lee H.H., Spina C.S., Collins J.J. Antibiotic treatment expands the resistance reservoir and ecological network of the phage metagenome. Nature 2013, 499:219-222.
29. Fancello L., Desnues C., Raoult D., Rolain J.M. Bacteriophages and diffusion of genes encoding antimicrobial resistance in cystic fibrosis sputum microbiota. J Antimicrob Chemother 2011, 66:2448-2454.
30. Dethlefsen L., Relman D.A. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci U S A 2011, 108(Suppl):4554-4561.
31. Jorth P., Trivedi U., Rumbaugh K., Whiteley M. Probing bacterial metabolism during infection using high-resolution transcriptomics. J Bacteriol 2013, 195:4991-4998.
32. Langereis J.D., Zomer A., Stunnenberg H.G., Burghout P., Hermans P.W.M. Nontypeable Haemophilus influenzae carbonic anhydrase is important for environmental and intracellular survival. J Bacteriol 2013, 195:2737-2746.
33. Perkins T.T., Davies M.R., Klemm E.J., Rowley G., Wileman T., James K., Keane T., Maskell D., Hinton J.C.D., Dougan G., et al. ChIP-seq and transcriptome analysis of the OmpR regulon of Salmonella enterica serovars Typhi and Typhimurium reveals accessory genes implicated in host colonization. Mol Microbiol 2013, 87:526-538.
34. Zhao H.Q., Chen C., Xiong Y.W., Xu X.F., Lan R.T., Wang H.Y., Yao X.Y., Bai X.N., Liu X.T., Meng Q., et al. Global transcriptional and phenotypic analyses of Escherichia coli O157:H7 strain Xuzhou21 and its pO157_Sal cured mutant. PLoS ONE 2013, 8.
35. Barquist L., Langridge G.C., Turner D.J., Phan M.D., Turner A.K., Bateman A., Parkhill J., Wain J., Gardner P.P. A comparison of dense transposon insertion libraries in the Salmonella serovars Typhi and Typhimurium. Nucleic Acids Res 2013, 41:4549-4564.
36. Van Opijnen T., Camilli A. A fine scale phenotype-genotype virulence map of a bacterial pathogen. Genome Res 2012, 22:2541-2551.
37. De Vries S.P.W., Eleveld M.J., Hermans P.W.M., Bootsma H.J. Characterization of the molecular interplay between Moraxella catarrhalis and human respiratory tract epithelial cells. PLoS ONE 2013, 8.
38. Wong S.M., Bernui M., Shen H., Akerley B.J. Genome-wide fitness profiling reveals adaptations required by Haemophilus in coinfection with influenza A virus in the murine lung. Proc Natl Acad Sci U S A 2013, 110:15413-15418.
39. Köser C.U., Ellington M.J., Cartwright E.J.P., Gillespie S.H., Brown N.M., Farrington M., Holden M.T.G., Dougan G., Bentley S.D., Parkhill J., et al. Routine use of microbial whole genome sequencing in diagnostic and public health microbiology. PLoS Pathog 2012, 8:e1002824.
40. Köser C.U., Holden M.T.G., Ellington M.J., Cartwright E.J.P., Brown N.M., Ogilvy-Stuart A.L., Hsu L.Y., Chewapreecha C., Croucher N.J., Harris S.R., et al. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 2012, 366:2267-2275.
41. Lewis T., Loman N.J., Bingle L., Jumaa P., Weinstock G.M., Mortiboy D., Pallen M.J. High-throughput whole-genome sequencing to dissect the epidemiology of Acinetobacter baumannii isolates from a hospital outbreak. J Hosp Infect 2010, 75:37-41.
42. McAdam P.R., Templeton K.E., Edwards G.F., Holden M.T.G., Feil E.J., Aanensen D.M., Bargawi H.J.A., Spratt B.G., Bentley S.D., Parkhill J., et al. Molecular tracing of the emergence, adaptation, and transmission of hospital-associated methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 2012, 109:1-6.
43. Holden M.T.G., Hsu L.-Y., Kurt K., Weinert L.A., Mather A.E., Harris S.R., Strommenger B., Layer F., Witte W., de Lencastre H., et al. A genomic portrait of the emergence, evolution, and global spread of a methicillin-resistant Staphylococcus aureus pandemic. Genome Res 2013, 23:653-664.
44. Gardy J.L., Johnston J.C., Ho Sui S.J., Cook V.J., Shah L., Brodkin E., Rempel S., Moore R., Zhao Y., Holt R., et al. Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N Engl J Med 2011, 364:730-739.
45. Baker S., Holt K.E., Clements A.C.A., Karkey A., Arjyal A., Boni M.F., Dongol S., Hammond N., Koirala S., Duy P.T., et al. Combined high-resolution genotyping and geospatial analysis reveals modes of endemic urban typhoid fever transmission. Open Biol 2011, 1:110008.
46. Holt K.E., Thieu Nga T.V., Thanh D.P., Vinh H., Kim D.W., Vu Tra M.P., Campbell J.I., Hoang N.V.M., Vinh N.T., Minh P.V., et al. Tracking the establishment of local endemic populations of an emergent enteric pathogen. Proc Natl Acad Sci U S A 2013, 110:17522-17527.
47. Holt K.E., Baker S., Weill F.-X., Holmes E.C., Kitchen A., Yu J., Sangal V., Brown D.J., Coia J.E., Kim D.W., et al. Shigella sonnei genome sequencing and phylogenetic analysis indicate recent global dissemination from Europe. Nat Genet 2012, 44:1056-1059.
48. Reuter S., Harrison T.G., Köser C.U., Ellington M.J., Smith G.P., Parkhill J., Peacock S.J., Bentley S.D., Török M.E. A pilot study of rapid whole-genome sequencing for the investigation of a Legionella outbreak. BMJ Open 2013, 3.
49. Eyre D.W., Cule M.L., Griffiths D., Crook D.W., Peto T.E.A., Walker A.S., Wilson D.J. Detection of mixed infection from bacterial whole genome sequence data allows assessment of its role in Clostridium difficile transmission. PLoS Comput Biol 2013, 9:e1003059.
50. Gray R.R., Tatem A.J., Johnson J.A., Alekseyenko A.V., Pybus O.G., Suchard M.A., Salemi M. Testing spatiotemporal hypothesis of bacterial evolution using methicillin-resistant Staphylococcus aureus ST239 genome-wide data within a Bayesian framework. Mol Biol Evol 2011, 28:1593-1603.
51. Spoor L.E., McAdam P.R., Weinert L.A., Rambaut A., Hasman H., Aarestrup F.M., Kearns A.M., Larsen A.R., Skov R.L., Fitzgerald J.R. Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus. MBio 2013, 4. e00356-13.
52. Mutreja A., Kim D.W., Thomson N.R., Connor T.R., Lee J.H., Kariuki S., Croucher N.J., Choi S.Y., Harris S.R., Lebens M., et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 2011, 10.1038/nature10392.
53. Okoro C.K., Kingsley R.A., Connor T.R., Harris S.R., Parry C.M., Al-Mashhadani M.N., Kariuki S., Msefula C.L., Gordon M.A., de Pinna E., et al. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet 2012, 10.1038/ng.2423.
54. Mather A.E., Reid S.W.J., Maskell D.J., Parkhill J., Fookes M.C., Harris S.R., Brown D.J., Coia J.E., Mulvey M.R., Gilmour M.W., et al. Distinguishable epidemics of multidrug-resistant Salmonella Typhimurium DT104 in different hosts. Science 2013, 341:1514-1517.
55. Hendriksen R.S., Price L.B., Schupp J.M., Gillece J.D., Kaas R.S., Engelthaler D.M., Bortolaia V., Pearson T., Waters A.E., Prasad Upadhyay B., et al. Population genetics of Vibrio cholerae from Nepal in 2010: evidence on the origin of the Haitian outbreak. MBio 2011, 2. e00157-11.
56. Katz L.S., Petkau A., Beaulaurier J., Tyler S., Antonova E.S., Turnsek M.A., Guo Y., Wang S., Paxinos E.E., Orata F., et al. Evolutionary dynamics of Vibrio cholerae O1 following a single-source introduction to Haiti. MBio 2013, 4. e00398-13.
57. Croucher N.J., Harris S.R., Fraser C., Quail M.A., Burton J., van der Linden M., McGee L., von Gottberg A., Song J.H., Ko K.S., et al. Rapid pneumococcal evolution in response to clinical interventions. Science 2011, 331:430-434.
58. Golubchik T., Brueggemann A.B., Street T., Gertz R.E., Spencer C.C.A., Ho T., Giannoulatou E., Link-Gelles R., Harding R.M., Beall B., et al. Pneumococcal genome sequencing tracks a vaccine escape variant formed through a multi-fragment recombination event. Nat Genet 2012, 44:352-355.
59. Croucher N.J., Finkelstein J.A., Pelton S.I., Mitchell P.K., Lee G.M., Parkhill J., Bentley S.D., Hanage W.P., Lipsitch M. Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat Genet 2013, 45:656-663.
60. Frank C., Werber D., Cramer J.P., Askar M., Faber M., an der Heiden M., Bernard H., Fruth A., Prager R., Spode A., et al. Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med 2011, 365:1771-1780.
61. Rasko D.A., Webster D.R., Sahl J.W., Bashir A., Boisen N., Scheutz F., Paxinos E.E., Sebra R., Chin C.-S., Iliopoulos D., et al. Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med 2011, 365:709-717.
62. Rohde H., Qin J., Cui Y., Li D., Loman N.J., Hentschke M., Chen W., Pu F., Peng Y., Li J., et al. Open-source genomic analysis of Shiga-toxin-producing E. coli O104:H4. N Engl J Med 2011, 365:718-724.
63. Price L.B., Stegger M., Hasman H., Aziz M., Larsen J., Andersen P.S., Pearson T., Waters A.E., Foster J.T., Schupp J., et al. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 2012, 3.
64. Harrison E.M., Paterson G.K., Holden M.T.G., Larsen J., Stegger M., Larsen A.R., Petersen A., Skov R.L., Christensen J.M., Bak Zeuthen A., et al. Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC. EMBO Mol Med 2013, 5:509-515.
65. Lebreton F., van Schaik W., McGuire A.M., Godfrey P., Griggs A., Mazumdar V., Corander J., Cheng L., Saif S., Young S., et al. Emergence of epidemic multidrug-resistant Enterococcus faecium from animal and commensal strains. MBio 2013, 4. e00534-13.
66. Lowder B.V., Guinane C.M., Ben Zakour N.L., Weinert L.A., Conway-Morris A., Cartwright R.A., Simpson A.J., Rambaut A., Nübel U., Fitzgerald J.R. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad Sci U S A 2009, 106:19545-19550.
67. Sheppard S.K., Didelot X., Meric G., Torralbo A., Jolley K.A., Kelly D.J., Bentley S.D., Maiden M.C.J., Parkhill J., Falush D. Genome-wide association study identifies vitamin B5 biosynthesis as a host specificity factor in Campylobacter. Proc Natl Acad Sci U S A 2013, 110:11923-11927.
68. Chaudhuri R.R., Morgan E., Peters S.E., Pleasance S.J., Hudson D.L., Davies H.M., Wang J.H., van Diemen P.M., Buckley A.M., Bowen A.J., et al. Comprehensive assignment of roles for Salmonella Typhimurium genes in intestinal colonization of food-producing animals. PLoS Genet 2013, 9.
69. Kingsley R.A., Kay S., Connor T., Barquist L., Sait L., Holt K.E., Sivaraman K., Wileman T., Goulding D., Clare S., et al. Genome and transcriptome adaptation accompanying emergence of the definitive type 2 host-restricted Salmonella enterica serovar Typhimurium pathovar. MBio 2013, 4. e00565-13.
70. Chin C.-S., Alexander D.H., Marks P., Klammer A.A., Drake J., Heiner C., Clum A., Copeland A., Huddleston J., Eichler E.E., et al. Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nat Methods 2013, 10:563-569.
71. Loman N.J., Constantinidou C., Christner M., Rohde H., Chan J.Z.M., Quick J., Weir J.C., Quince C., Smith G.P., Betley J.R., et al. A culture-independent sequence-based metagenomics approach to the investigation of an outbreak of Shiga-toxigenic Escherichia coli. JAMA 2013, 309:1502.
72. Seth-Smith H.M.B., Harris S.R., Skilton R.J., Radebe F.M., Golparian D., Shipitsyna E., Duy P.T., Scott P., Cutcliffe L.T., O'Neill C., et al. Whole-genome sequences of Chlamydia trachomatis directly from clinical samples without culture. Genome Res 2013, 10.1101/gr.150037.112.
73. Westermann A.J., Gorski S.A., Vogel J. Dual RNA-seq of pathogen and host. Nat Rev Microbiol 2012, 10:618-630.
74. Falush D., Bowden R. Genome-wide association mapping in bacteria?. Trends Microbiol 2006, 14:353-355.
75. Priest N.K., Rudkin J.K., Feil E.J., van den Elsen J.M.H., Cheung A., Peacock S.J., Laabei M., Lucks D.A., Recker M., Massey R.C. From genotype to phenotype: can systems biology be used to predict Staphylococcus aureus virulence?. Nat Rev Microbiol 2012, 10:791-797.
76. Laabei M., Recker M., Rudkin J.K., Aldeljawi M., Gulay Z., Sloan T.J., Williams P., Endres J.L., Bayles K.W., Fey P.D., et al. Predicting the virulence of MRSA from its genome sequence. Genome Res 2014, 24:839-849.