Design and validation of a supragenome array for determination of the genomic content of Haemophilus influenzae isolates

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Eutsey, Rory A ^a   Hiller, N Luisa ^a,b   Earl, Joshua P ^a   Janto, Benjamin A ^a,c   Dahlgren, Margaret E ^a   Ahmed, Azad ^a   Powell, Evan ^a   Schultz, Matthew P ^a   Gilsdorf, Janet R ^d,e   Zhang, Lixin ^d   Smith, Arnold ^f   Murphy, Timothy F ^g   Sethi, Sanjay ^g   Shen, Kai ^a,c   Post, J Christopher ^a,c   Hu, Fen Z ^a,c   Ehrlich, Garth D ^a,c  

^a ALLEGHENY GENERAL HOSPITAL   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF MICHIGAN   (United States)

^e UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

^f SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^g UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLELE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; GENE CLUSTER; GENE SEQUENCE; HAEMOPHILUS INFLUENZAE; HYBRIDIZATION; MENINGITIS; NONHUMAN; OTITIS MEDIA; OTORRHEA; PAPUA NEW GUINEA; PNEUMONIA; SEPSIS; SUPRAGENOME HYBRIDIZATION;

GENES, BACTERIAL; GENOMICS; HAEMOPHILUS INFLUENZAE; MOLECULAR SEQUENCE ANNOTATION; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEQUENCE ANALYSIS;

HAEMOPHILUS INFLUENZAE;

EID: 84880182043     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-484     Document Type: Article

References (55)

1. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D, Ward NL, Angiuoli SV, Crabtree J, Jones AL, Durkin AS, Deboy RT, Davidsen TM, Mora M, Scarselli M, YRos MI, Peterson JD, Hauser CR, Sundaram JP, Nelson WC, Madupu R, Brinkac LM, Dodson RJ, Rosovitz MJ, Sullivan SA, Daugherty SC, Haft DH, Selengut J, Gwinn ML, Zhou L, Zafar N, et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". Proc Natl Acad Sci U S A 2005, 102:13950-13955.
2. Hogg JS, Hu FZ, Janto B, Boissy R, Hayes J, Keefe R, Post JC, Ehrlich GD. Characterization and modeling of the Haemophilus influenzae core and supragenomes based on the complete genomic sequences of Rd and 12 clinical nontypeable strains. Genome Biol 2007, 8:R103.
3. Hiller NL, Janto B, Hogg JS, Boissy R, Yu S, Powell E, Keefe R, Ehrlich NE, Shen K, Hayes J, Barbadora K, Klimke W, Dernovoy D, Tatusova T, Parkhill J, Bentley SD, Post JC, Ehrlich GD, Hu FZ. Comparative genomic analyses of seventeen Streptococcus pneumoniae strains: insights into the pneumococcal supragenome. J Bacteriol 2007, 189:8186-8195.
4. Donati C, Hiller NL, Tettelin H, Muzzi A, Croucher NJ, Angiuoli SV, Oggioni M, Dunning Hotopp JC, Hu FZ, Riley DR, Covacci A, Mitchell TJ, Bentley SD, Kilian M, Ehrlich GD, Rappuoli R, Moxon ER, Masignani V. Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. Genome Biol 2010, 11:R107.
5. Boissy R, Ahmed A, Janto B, Earl J, Hall BG, Hogg JS, Pusch GD, Hiller LN, Powell E, Hayes J, Yu S, Kathju S, Stoodley P, Post JC, Ehrlich GD, Hu FZ. Comparative supragenomic analyses among the pathogens Staphylococcus aureus, Streptococcus pneumoniae, and Haemophilus influenzae using a modification of the finite supragenome model. BMC Genomics 2011, 12:187.
6. Davie JJ, Earl J, de Vries SP, Ahmed A, Hu FZ, Bootsma HJ, Stol K, Hermans PW, Wadowsky RM, Ehrlich GD, Hays JP, Campagnari AA. Comparative analysis and supragenome modeling of twelve Moraxella catarrhalis clinical isolates. BMC Genomics 2011, 12:70.
7. Ahmed A, Earl J, Retchless A, Hillier SL, Rabe LK, Cherpes TL, Powell E, Janto B, Eutsey R, Hiller NL, Boissy R, Dahlgren ME, Hall BG, Costerton JW, Post JC, Hu FZ, Ehrlich GD. Comparative Genomic Analyses of 17 Clinical Isolates of Gardnerella vaginalis Provide Evidence of Multiple Genetically Isolated Clades Consistent with Subspeciation into Genovars. J Bacteriol 2012, 194:3922-3937.
8. Borneman AR, McCarthy JM, Chambers PJ, Bartowsky EJ. Comparative analysis of the Oenococcus oeni pan genome reveals genetic diversity in industrially-relevant pathways. BMC Genomics 2012, 13:373.
9. He M, Sebaihia M, Lawley TD, Tabler RA S, Dawson LF, Martin MJ, Holt KE, Seth-Smith HM, Quail MA, Rance R, Brooks K, Churcher C, Harris D, Bentley SD, Burrows C, Clark L, Corton C, Murray V, Rose G, Thurston S, van Tonder A, Walker D, Wren BW, Dougan G, Parkhill J. Evolutionary dynamics of Clostridium difficile over short and long time scales. Proc Natl Acad Sci U S A 2010, 107:7527-7532.
10. Conlan S, Mijares LA, Comp Seq Program N, Becker J, Blakesley RR, Bouffard GG, Brooks S, Coleman HL, Gupta J, Gurson N, Park M, Schmidt B, Thomas PJ, Young A, Otto M, Kong HH, Murray PR, Segre JA. Staphylococcus epidermidis pan-genome sequence analysis reveals diversity of skin commensal and hospital infection-associated isolates. Genome Biol 2012, 13:R64.
11. Ehrlich GD, Hu FZ, Shen K, Stoodley P, Post JC. Bacterial Plurality as a General Mechanism Driving Persistence in Chronic Infections. Clin Orthop Relat Res 2005, 437:20-24.
12. Ehrlich GD, Ahmed A, Earl J, Hiller NL, Costerton JW, Stoodley P, Post JC, DeMeo P, Hu FZ. The distributed genome hypothesis as a rubric for understanding evolution in situ during chronic bacterial biofilm infectious processes. FEMS Immunol Med Microbiol 2010, 59:269-279.
13. Shen K, Wang X, Post JC, Ehrlich GD. Molecular and Translational Research Approaches for the study of Bacterial Pathogenesis in Otitis Media. Evidence-based Otitis Media 2003, 91-119. Hamilton: B.C. Decker Inc, Rosenfeld R, Bluestone CD, 2.
14. Rasko DA, Rosovitz MJ, Myers GS, Mongodin EF, Fricke WF, Gajer P, Crabtree J, Sebaihia M, Thomson NR, Chaudhuri R, Henderson IR, Sperandio V, Ravel J. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 2008, 190:6881-6893.
15. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, Calteau A, Chiapello H, Clermont O, Cruveiller S, Danchin A, Diard M, Dossat C, Karoui ME, Frapy E, Garry L, Ghigo JM, Gilles AM, Johnson J, Le Bouguénec C, Lescat M, Mangenot S, Martinez-Jéhanne V, Matic I, Nassif X, Oztas S, et al. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 2009, 5:e1000344.
16. Buchinsky FJ, Forbes ML, Hayes JD, Shen K, Ezzo S, Compliment J, Hogg J, Hiller NL, Hu FZ, Post JC, Ehrlich GD. Virulence phenotypes of low-passage clinical isolates of nontypeable Haemophilus influenzae assessed using the chinchilla laniger model of otitis media. BMC Microbio 2007, 7:56.
17. Forbes ML, Horsey E, Hiller NL, Buchinsky FJ, Hayes JD, Compliment JM, Hillman T, Ezzo S, Shen K, Keefe R, Barbadora K, Post JC, Hu FZ, Ehrlich GD. Strain-specific virulence phenotypes of Streptococcus pneumoniae assessed using the Chinchilla laniger model of otitis media. PLoS One 2008, 3:e1969.
18. Hall-Stoodley L, Nistico L, Sambanthamoorthy K, Dice B, Nguyen D, Mershon WJ, Johnson C, Hu FZ, Stoodley P, Ehrlich GD, Post JC. Characterization of biofilm matrix, degradation by DNase treatment and evidence of capsule downregulation in Streptococcus pneumoniae clinical isolates. BMC Microbiol 2008, 8:173.
19. Ehrlich GD, Hiller NL, Hu FZ. What makes pathogens pathogenic. Genome Biol 2008, 9:225.
20. Schwarz S, Morelli G, Kusecek B, Manica A, Balloux F, Owen RJ, Graham DY, van der Merwe S, Achtman M, Suerbaum S. Horizontal versus familial transmission of Helicobacter pylori. PLoS Pathog 2008, 4:e1000180.
21. Hiller NL, Ahmed A, Powell E, Martin DP, Eutsey R, Earl J, Janto B, Boissy RJ, Hogg J, Barbadora K, Sampath R, Lonergan S, Post JC, Hu FZ, Ehrlich GD. Generation of genic diversity among Streptococcus pneumoniae strains via horizontal gene transfer during a chronic polyclonal pediatric infection. PLoS Pathog 2010, 6:e1001108.
22. MacNeil JR, Cohn AC, Farley M, Mair R, Baumbach J, Bennett N, Gershman K, Harrison LH, Lynfield R, Petit S, Reingold A, Schaffner W, Thomas A, Coronado F, Zell ER, Mayer LW, Clark TA, Messonnier NE. Current epidemiology and trends in invasive Haemophilus influenzae disease-United States, 1989-2008. Clin Infect Dis 2011, 53:1230-1236.
23. Agrawal A, Murphy TF. Haemophilus Influenzae infections in the H. influenza type b conjugate vaccine era. J Clin Microbiol 2011, 49:3728-3732.
24. Döring G, Parameswaran IG, Murphy TF. Differential adaptation of microbial pathogens to airways of patients with cystic fibrosis and chronic obstructive pulmonary disease. FEMS Microbiol Rev 2011, 35:124-146.
25. Tsang RS, Sill ML, Skinner SJ, Law DK, Zhou J, Wylie J. Characterization of invasive Haemophilus influenzae disease in Manitoba, Canada, 2000-2006: invasive disease due to non-type b strains. Clin Infect Dis 2007, 44:1611-1614.
26. Shuel M, Law D, Skinner S, Wylie J, Karlowsky J, Tsang RS. Characterization of nontypeable Haemophilus influenzae collected from respiratory infections and invasive disease cases in Manitoba, Canada. FEMS Immunol Med Microbiol 2010, 58:277-284.
27. Kelly L, Tsang RS, Morgan A, Jamieson FB, Ulanova M. Invasive disease caused by Haemophilus influenzae type a in Northern Ontario First Nations communities. J Med Microbiol 2011, 60:384-390.
28. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM, McKenney K, Sutton G, FitzHugh W, Fields C, Gocayne JD, Soctt J, Shirley R, Liu L, Glodek A, Kelley JM, Weidman JF, Phillips CA, Spriggs T, Hedblom E, Cotton MD, Utterback TR, Hanna MC, Nguyen DT, Saudek DM, Brandon RC, et al. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 1995, 269:496-512.
29. Erwin AL, Nelson KL, Mhlanga-Mutangadura T, Bonthuis PJ, Geelhood JL, Morlin G, Unrath WC, Campos J, Crook DW, Farley MM. Characterization of genetic and phenotypic diversity of invasive nontypeable Haemophilus influenzae. Infect Immun 2005, 73:5853-5863.
30. Harrison A, Dyer DW, Gillaspy A, Ray WC, Mungur R, Carson MB, Zhong H, Gipson J, Gipson M, Johnson LS, Lewis L, Bakaletz LO, Munson RS. Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae: comparative study with H. influenzae serotype d, strain KW20. J Bacteriol 2005, 187:4627-4636.
31. Haemophilus Influenzae 10810 genome sequencing project http://www.ncbi.nlm.nih.gov/genome/165?project_id=86647.
32. Sauver JL, Marrs C, Foxman B, Somsel P, Madera R, Gilsdorf JR. Risk factors for otitis media and carriage of multiple strains of Haemophilus influenzae and Streptococcus pneumonia. Emerg Infect Dis 2000, 6:622-630.
33. Musser JM, Barenkamp SJ, Granoff DM, Selander RK. Genetic relationships of serologically nontypeable and serotype b strains of Haemophilus influenza. Infect Immun 1986, 52:183-191.
34. Murphy TF, Lesse AJ, Kirkham C, Zhong H, Sethi S, Munson RS. A clonal group of nontypeable Haemophilus influenzae with two IgA proteases is adapted to infection in chronic obstructive pulmonary disease. PLoS One 2011, 6(10). E25923.
35. Fung WW, O'Dwyer CA, Sinha S, Brauer AL, Murphy TF, Kroll JS, Langford PR. Presence of copper-and zinc-containing superoxide dismutase in commensal H. influenzae isolates. J Clin Microbiol 2006, 44:4222-4226.
36. Shen K, Antalis P, Gladitz J, Sayeed S, Ahmed A, Yu S, Hayes J, Johnson S, Dice B, Dopico R, Keefe R, Janto B, Chong W, Goodwin J, Wadowsky RM, Erdos G, Post JC, Ehrlich GD, Hu FZ. Identification, distribution, and expression of novel genes in 10 clinical isolates of nontypeable Haemophilus influenza. Infect Immun 2005, 73:3479-3491.
37. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O. The RAST Server: rapid annotations using subsystems technology. BMC Genomics 2008, 9:75.
38. Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 1988, 1988(85):2444-2448.
39. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual, Volume 1 2001, 2344. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
40. Ausubel FM. Current protocols in molecular biology, Volume 1. (2.4.3) 1991, Hoboken, New Jersey: Wiley.
41. Paradis E, Claude J, Strimmer K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 2004, 20:289-290.
42. FigTree v1.3.1 available at http://tree.bio.ed.ac.uk/software/figtree/.
43. Lacross NC, Marrs CF, Patel M, Sandstedt SA, Gilsdorf JR. High genetic diversity of nontypeable Haemophilus influenzae isolates from two children attending a day care center. J Clin Microbiol 2008, 46:3817-3821.
44. Gerdes K, Rasmussen PB, Molin S. Unique type of plasmid maintenance function: postsegregational killing of plasmid-free cells. Proc Natl Acad Sci USA 1986, 83:3116-3120.
45. Wang WF, Cheng X, Molineux IJ. Isolation and Identification of fxsA, an Escherichia coli gene that can suppress F exclusion of bacteriophage T7. J Mol Biol 1999, 292:485-499.
46. Sandstedt SA, Zhang L, Patel M, Marrs CF, Gilsdorf JR. Comparison of laboratory-based and phylogenetic methods to distinguish between Haemophilus influenza and H. haemolyticus. J Microbioal Methods 2008, 75:369-371.
47. McCrea KW, Xie J, LaCross N, Patel M, Mukundan M, Murphy TF, Marrs CF, Gilsdorf JR. Relationships of non-typeable Haemophilus influenza with hemolytic and non-hemolytic Haemophilus haemolyticus. J Clin Microbiol 2008, 46:406-416.
48. Murphy TF, Brauer AL, Sethi S, Kilian M, Cai X, Lesse AJ. Haemophilus haemolyticus: a human respiratory tract commensal to be dintinguished from Haemophilus influenza. J Infect Dis 2007, 195:81-89.
49. Hiller NL, Eutsey RA, Powell E, Earl JP, Janto B, Martin DP, Dawid S, Ahmed A, Longwell MJ, Dahlgren ME, Ezzo S, Tettelin H, Daugherty SC, Mitchell TJ, Hillman TA, Buchinsky FJ, Tomasz A, de Lencastre H, Sá-Leão R, Post JC, Hu FZ, Ehrlich GD. Differences in genotype and virulence among four multidrug-resistant Streptococcus pneumoniae isolates belonging to the PMEN1 clone. PLoS One 2011, 6:e28850.
50. Hu FZ, Eutsey R, Ahmed A, Frazao N, Powell E, Hiller NH, Hillman T, Buchinsky FJ, Boissy R, Janto B, Kress-Bennett JM, Longwell M, Suzanne E, Post JC, Tomasz A, Ehrlich GD. In vivo capsular switch in Streptococcus pneumoniae. PLoS One 2012, 7(11):e47983.
51. Anderson R, Wang X, Briere EC, Katz LS, Cohn AC, Clark TA, Messonnier NE, Mayer LW. Haemophilus haemolyticus isolates causing clinical disease. J Clin Microbiol 2012, 50:2462-2465.
52. Wickert E, Machado MA, Lemos EG. Evaluation of the genetic diversity of Xylella fastidiosa strains from citrus and coffee hosts by single-nucleotide polymorphism markers. Phytopathology 2007, 97:1543-1549.
53. Mathee K, Narasimhan G, Valdes C, Qiu X, Matewish JM, Koehrsen M, Rokas A, Yandava CN, Engels R, Zeng E, Olavarietta R, Doud M, Smith RS, Montgomery P, White JR, Godfrey PA, Kodira C, Birren B, Galagan JE, Lory S. Dynamics of Pseudomonas aeruginosa genome evolution. Proc Natl Acad Sci U S A 2008, 105:3100-3105.
54. Mell JC, Shumilina S, Hall IM, Redfield RJ. Transformation of natural genetic variation into Haemophilus influenza genomes. PLoS Pathog 2011, 7(7):e1002151.
55. Nistico L, Earl J, Hiller NL, Ahmed A, Retchless A, Janto B, Costerton JW, Hu FZ, Ehrlich GD. Using the Core and Supra Genomes to Determine Diversity and Natural Proclivities among Bacterial Strains. Molecular Methods and Applications in Microbiology 2014, Norfolk, UK: Caister Academic Press, Skovhus TL, Caffrey S, Hubert C, In Press.