Haemophilus influenzae: Using comparative genomics to accurately identify a highly recombinogenic human pathogen

BMC Genomics

Volumn 16, Issue 1, 2015, Pages

  Price, Erin P ^a   Sarovich, Derek S ^a   Nosworthy, Elizabeth ^a   Beissbarth, Jemima ^a   Marsh, Robyn L ^a   Pickering, Janessa ^b   Kirkham, Lea Ann S ^b   Keil, Anthony D ^c   Chang, Anne B ^a   Smith Vaughan, Heidi C ^a  

^a MENZIES SCHOOL OF HEALTH RESEARCH   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c KING EDWARD MEMORIAL HOSPITAL   (Australia)

Author keywords

Assay; fucP; Genomics; Haemophilus haemolyticus; Haemophilus influenzae; NTHi; PCR; Real time PCR; Species; TaqMan

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; COMPARATIVE GENOMICS; CONTROLLED STUDY; FUCK GENE; FUCP GENE; GENE LOCUS; GENE SEQUENCE; GENETIC CONSERVATION; GENOME ANALYSIS; GENOMICS; HAEMOPHILUS INFLUENZAE; MEASUREMENT ACCURACY; MOLECULAR PHYLOGENY; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SINGLE NUCLEOTIDE POLYMORPHISM; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETIC RECOMBINATION; GENETICS; HUMAN; PHYLOGENY; PROCEDURES;

BACTERIA (MICROORGANISMS); HAEMOPHILUS; HAEMOPHILUS HAEMOLYTICUS; HAEMOPHILUS INFLUENZAE; PASTEURELLALES;

CLUSTER ANALYSIS; GENOME, BACTERIAL; GENOMICS; HAEMOPHILUS INFLUENZAE; HUMANS; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; RECOMBINATION, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84940192316     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-015-1857-x     Document Type: Article

References (47)

1. US Centers for Disease Control and Prevention. Haemophilus influenzae Type b vaccine. MMWR Morb Mortal Wkly Rep. 1988;36:832.
2. Bisgard KM, Kao A, Leake J, Strebel PM, Perkins BA, Wharton M. Haemophilus influenzae invasive disease in the United States, 1994-1995: near disappearance of a vaccine-preventable childhood disease. Emerg Infect Dis. 1998;4:229-37.
3. Van Eldere J, Slack MP, Ladhani S, Cripps AW. Non-typeable Haemophilus influenzae, an under-recognised pathogen. Lancet Infect Dis. 2014;14:1281-92.
4. Foxwell AR, Kyd JM, Cripps AW. Nontypeable Haemophilus influenzae: pathogenesis and prevention. Microbiol Mol Biol Rev. 1998;62:294-308.
5. Anderson R, Wang X, Briere EC, Katz LS, Cohn AC, Clark TA, et al. Haemophilus haemolyticus isolates causing clinical disease. J Clin Microbiol. 2012;50:2462-5.
6. Morton DJ, Hempel RJ, Whitby PW, Seale TW, Stull TL. An invasive Haemophilus haemolyticus isolate. J Clin Microbiol. 2012;50:1502-3.
7. Lynn DJ, Kane JG, Parker RH. Haemophilus parainfluenzae and influenzae endocarditis: a review of forty cases. Medicine (Baltimore). 1977;56:115-28.
8. US Centers for Disease Control and Prevention. Brazilian purpuric fever: Haemophilus aegyptius bacteremia complicating purulent conjunctivitis. MMWR Morb Mortal Wkly Rep. 1986;35:553-4.
9. Boucher MB, Bedotto M, Couderc C, Gomez C, Reynaud-Gaubert M, Drancourt M. Haemophilus pittmaniae respiratory infection in a patient with siderosis: a case report. J Med Case Rep. 2012;6:120.
10. Le Floch AS, Cassir N, Hraiech S, Guervilly C, Papazian L, Rolain JM. Haemophilus parahaemolyticus septic shock after aspiration pneumonia, France. Emerg Infect Dis. 2013;19:1694-5.
11. Parsons M, Faris I. Empyema of the gallbladder due to Haemophilus parahaemolyticus, with a brief review of its role as a pathogen. J Clin Pathol. 1973;26:604-5.
12. Chen CC, Wang SJ, Fuh JL. Isolation of Haemophilus parahaemolyticus in a patient with cryptogenic brain abscess. Scand J Infect Dis. 2001;33:385-6.
13. Douglas GW, Buck LL, Rosen C. Liver abscess caused by Haemophilus paraphrohaemolyticus. J Clin Microbiol. 1979;9:299-300.
14. Jordan IK, Conley AB, Antonov IV, Arthur RA, Cook ED, Cooper GP, et al. Genome sequences for five strains of the emerging pathogen Haemophilus haemolyticus. J Bacteriol. 2011;193:5879-80.
15. Winn Jr. WC, Allen SD, Janda WJ, Koneman EW, Procop G, Schreckenberger PC. Chapter 9: Miscellaneous fastidious Gram-negative bacilli, p. 448. In Koneman's colour atlas and textbook of diagnostic microbiology, 6th ed. Lippincott Williams & Wilkins, Baltimore, MD. 2005
16. Murphy TF, Brauer AL, Sethi S, Kilian M, Cai X, Lesse AJ. Haemophilus haemolyticus: a human respiratory tract commensal to be distinguished from Haemophilus influenzae. J Infect Dis. 2007;195:81-9.
17. McCrea KW, Xie J, LaCross N, Patel M, Mukundan D, Murphy TF, et al. Relationships of nontypeable Haemophilus influenzae strains to hemolytic and nonhemolytic Haemophilus haemolyticus strains. J Clin Microbiol. 2008;46:406-16.
18. Nørskov-Lauritsen N. Detection of cryptic genospecies misidentified as Haemophilus influenzae in routine clinical samples by assessment of marker genes fucK, hap, and sodC. J Clin Microbiol. 2009;47:2590-2.
19. Nørskov-Lauritsen N, Overballe MD, Kilian M. Delineation of the species Haemophilus influenzae by phenotype, multilocus sequence phylogeny, and detection of marker genes. J Bacteriol. 2009;191:822-31.
20. Prymula R, Kriz P, Kaliskova E, Pascal T, Poolman J, Schuerman L. Effect of vaccination with pneumococcal capsular polysaccharides conjugated to Haemophilus influenzae-derived protein D on nasopharyngeal carriage of Streptococcus pneumoniae and H. influenzae in children under 2 years of age. Vaccine. 2009;28:71-8.
21. Wang X, Mair R, Hatcher C, Theodore MJ, Edmond K, Wu HM, et al. Detection of bacterial pathogens in Mongolia meningitis surveillance with a new real-time PCR assay to detect Haemophilus influenzae. Int J Med Microbiol. 2011;301:303-9.
22. Binks MJ, Temple B, Kirkham LA, Wiertsema SP, Dunne EM, Richmond PC, et al. Molecular surveillance of true nontypeable Haemophilus influenzae: an evaluation of PCR screening assays. PLoS One. 2012;7, e34083.
23. Pickering J, Richmond PC, Kirkham LA. Molecular tools for differentiation of non-typeable Haemophilus influenzae from Haemophilus haemolyticus. Front Microbiol. 2014;5:664.
24. Witherden EA, Bajanca-Lavado MP, Tristram SG, Nunes A. Role of inter-species recombination of the ftsI gene in the dissemination of altered penicillin-binding-protein-3-mediated resistance in Haemophilus influenzae and Haemophilus haemolyticus. J Antimicrob Chemother. 2014;69:1501-9.
25. Smith-Vaughan HC, Chang AB, Sarovich DS, Marsh RL, Grimwood K, Leach AJ, et al. Absence of an important vaccine and diagnostic target in carriage- and disease-related nontypeable Haemophilus influenzae. Clin Vaccine Immunol. 2014;21:250-2.
26. De Chiara M, Hood D, Muzzi A, Pickard DJ, Perkins T, Pizza M, et al. Genome sequencing of disease and carriage isolates of nontypeable Haemophilus influenzae identifies discrete population structure. Proc Natl Acad Sci U S A. 2014;111:5439-44.
27. Pickering J, Binks MJ, Beissbarth J, Hare KM, Kirkham LA, Smith-Vaughan H. A PCR-high-resolution melt assay for rapid differentiation of nontypeable Haemophilus influenzae and Haemophilus haemolyticus. J Clin Microbiol. 2014;52:663-7.
28. Smith-Vaughan H, Byun R, Nadkarni M, Jacques NA, Hunter N, Halpin S, et al. Measuring nasal bacterial load and its association with otitis media. BMC Ear Nose Throat Disord. 2006;6:10.
29. Sarovich DS, Price EP. SPANDx: a genomics pipeline for comparative analysis of large haploid whole genome re-sequencing datasets. BMC Res Notes. 2014;7:618.
30. Huang W, Li L, Myers JR, Marth GT. ART: a next-generation sequencing read simulator. Bioinformatics. 2012;28:593-4.
31. Harrison A, Dyer DW, Gillaspy A, Ray WC, Mungur R, Carson MB, et al. Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae: comparative study with H. influenzae serotype d, strain KW20. J Bacteriol. 2005;187:4627-36.
32. Swofford DL. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Sunderland, MA: Sinauer Associates [Version 4]. 2003.
33. Price EP, Dale JL, Cook JM, Sarovich DS, Seymour ML, Ginther JL, et al. Development and validation of Burkholderia pseudomallei-specific real-time PCR assays for clinical, environmental or forensic detection applications. PLoS One. 2012;7:e37723.
34. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841-2.
35. Price EP, Sarovich DS, Webb JR, Ginther JL, Mayo M, Cook JM, et al. Accurate and rapid identification of the Burkholderia pseudomallei near-neighbour, Burkholderia ubonensis, using real-time PCR. PLoS One. 2013;8:e71647.
36. Maaroufi Y, De Bruyne JM, Heymans C, Crokaert F. Real-time PCR for determining capsular serotypes of Haemophilus influenzae. J Clin Microbiol. 2007;45:2305-8.
37. Abdeldaim GM, Stralin K, Kirsebom LA, Olcen P, Blomberg J, Herrmann B. Detection of Haemophilus influenzae in respiratory secretions from pneumonia patients by quantitative real-time polymerase chain reaction. Diagn Microbiol Infect Dis. 2009;64:366-73.
38. Blackall PJ, Christensen H, Beckenham T, Blackall LL, Bisgaard M. Reclassification of Pasteurella gallinarum, [Haemophilus] paragallinarum, Pasteurella avium and Pasteurella volantium as Avibacterium gallinarum gen. nov., comb. nov., Avibacterium paragallinarum comb. nov., Avibacterium avium comb. nov. and Avibacterium volantium comb. nov. Int J Syst Evol Microbiol. 2005;55:353-62.
39. Kroll JS, Wilks KE, Farrant JL, Langford PR. Natural genetic exchange between Haemophilus and Neisseria: intergeneric transfer of chromosomal genes between major human pathogens. Proc Natl Acad Sci U S A. 1998;95:12381-5.
40. Ridderberg W, Fenger MG, Norskov-Lauritsen N. Haemophilus influenzae may be untypable by the multilocus sequence typing scheme due to a complete deletion of the fucose operon. J Med Microbiol. 2010;59:740-2.
41. Dang S, Sun L, Huang Y, Lu F, Liu Y, Gong H, et al. Structure of a fucose transporter in an outward-open conformation. Nature. 2010;467:734-8.
42. Stahl M, Friis LM, Nothaft H, Liu X, Li J, Szymanski CM, et al. L-fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc Natl Acad Sci U S A. 2011;108:7194-9.
43. Hare KM, Binks MJ, Grimwood K, Chang AB, Leach AJ, Smith-Vaughan H. Culture and PCR detection of Haemophilus influenzae and Haemophilus haemolyticus in Australian Indigenous children with bronchiectasis. J Clin Microbiol. 2012;50:2444-5.
44. Theodore MJ, Anderson RD, Wang X, Katz LS, Vuong JT, Bell ME, et al. Evaluation of new biomarker genes for differentiating Haemophilus influenzae from Haemophilus haemolyticus. J Clin Microbiol. 2012;50:1422-4.
45. Croxtall JD, Keating GM. Pneumococcal polysaccharide protein D-conjugate vaccine (Synflorix; PHiD-CV). Paediatr Drugs. 2009;11:349-57.
46. Norskov-Lauritsen N, Overballe MD, Kilian M. Delineation of the species Haemophilus influenzae by phenotype, multilocus sequence phylogeny, and detection of marker genes. J Bacteriol. 2009;191:822-31.
47. Meats E, Feil EJ, Stringer S, Cody AJ, Goldstein R, Kroll JS, et al. Characterization of encapsulated and noncapsulated Haemophilus influenzae and determination of phylogenetic relationships by multilocus sequence typing. J Clin Microbiol. 2003;41:1623-36.