Comparative analysis and supragenome modeling of twelve Moraxella catarrhalis clinical isolates

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Davie, Jeremiah J ^a   Earl, Josh ^c   de Vries, Stefan P W ^e   Ahmed, Azad ^c   Hu, Fen Z ^c,d   Bootsma, Hester J ^e   Stol, Kim ^e   Hermans, Peter W M ^e   Wadowsky, Robert M ^f,g,h   Ehrlich, Garth D ^c,d   Hays, John P ⁱ   Campagnari, Anthony A ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c ALLEGHENY SINGER RESEARCH INSTITUTE   (United States)

^d DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF PITTSBURGH   (United States)

^h CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

ⁱ ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

VIRULENCE FACTOR; BACTERIAL DNA;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIUM ISOLATE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONTROLLED STUDY; GENE CLUSTER; GENE IDENTIFICATION; GENOME ANALYSIS; HOMOLOGOUS RECOMBINATION; MATHEMATICAL MODEL; MORAXELLA CATARRHALIS; MULTILOCUS SEQUENCE TYPING; NONHUMAN; NUCLEOTIDE SEQUENCE; OTITIS MEDIA; SEQUENCE ANALYSIS; STREPTOCOCCUS PNEUMONIAE; SUPRAGENOME; BACTERIUM IDENTIFICATION; BIOLOGICAL MODEL; CODON; COMPARATIVE STUDY; DNA SEQUENCE; GENETICS; INTERSPERSED REPEAT; ISOLATION AND PURIFICATION; MULTIGENE FAMILY; SEQUENCE ALIGNMENT;

BACTERIA (MICROORGANISMS); MORAXELLA CATARRHALIS; NEGIBACTERIA; PROTEOBACTERIA;

BACTERIAL TYPING TECHNIQUES; CODON; DNA, BACTERIAL; GENOME, BACTERIAL; INTERSPERSED REPETITIVE SEQUENCES; MODELS, GENETIC; MORAXELLA (BRANHAMELLA) CATARRHALIS; MULTIGENE FAMILY; MULTILOCUS SEQUENCE TYPING; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; VIRULENCE FACTORS;

EID: 79251581292     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-70     Document Type: Article

References (73)

1. Hall-Stoodley L, Hu FZ, Gieseke A, Nistico L, Nguyen D, Hayes J, Forbes M, Greenberg DP, Dice B, Burrows A, Wackym PA, Stoodley P, Post JC, Ehrlich GD, Kerschner JE. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA 2006, 296:202-211. 10.1001/jama.296.2.202, 1885379, 16835426.
2. Nistico L, Gieseke A, Stoodley P, Hall-Stoodley L, Kerschner JE, Ehrlich GD. Fluorescence "in situ" hybridization for the detection of biofilm in the middle ear and upper respiratory tract mucosa. Methods Mol Biol 2009, 493:191-213. full_text, 18839349.
3. de Vries SPW, Bootsma HJ, Hays JP, Hermans PWM. Molecular aspects of Moraxella catarrhalis pathogenesis. Microbiol Mol Biol Rev 2009, 73:389-406. Table of Contents, 10.1128/MMBR.00007-09, 2738133, 19721084.
4. Luke NR, Jurcisek JA, Bakaletz LO, Campagnari AA. Contribution of Moraxella catarrhalis type IV pili to nasopharyngeal colonization and biofilm formation. Infect Immun 2007, 75:5559-5564. 10.1128/IAI.00946-07, 2168369, 17908808.
5. Leibovitz E, Broides A, Greenberg D, Newman N. Current management of pediatric acute otitis media. Expert Rev Anti Infect Ther 2010, 8:151-161. 10.1586/eri.09.112, 20109045.
6. Murphy TF, Parameswaran GI. Moraxella catarrhalis, a human respiratory tract pathogen. Clin Infect Dis 2009, 49:124-131. 10.1086/599375, 19480579.
7. Murphy TF. Vaccine development for Moraxella catarrhalis: rationale, approaches and challenges. Expert Rev Vaccines 2009, 8:655-658. 10.1586/erv.09.28, 19485745.
8. Post JC, Hiller NL, Nistico L, Stoodley P, Ehrlich GD. The role of biofilms in otolaryngologic infections: update 2007. Curr Opin Otolaryngol Head Neck Surg 2007, 15:347-351. 10.1097/MOO.0b013e3282b97327, 17823552.
9. Post JaE, GD Biofilms and their role in ear and respiratory infections. Otorhinolaryngology Head and Neck Surgery 2009, 839-845. PA. Hamiltion, Ontario: BC Decker Publisher, Snow JaW, 17, Post JaE, GD.
10. Sethi S, Murphy TF. Infection in the pathogenesis and course of chronic obstructive pulmonary disease. N Engl J Med 2008, 359:2355-2365. 10.1056/NEJMra0800353, 19038881.
11. Mannino DM, Buist AS. Global burden of COPD: risk factors, prevalence, and future trends. Lancet 2007, 370:765-773. 10.1016/S0140-6736(07)61380-4, 17765526.
12. Brixner DI. Improving acute otitis media outcomes through proper antibiotic use and adherence. Am J Manag Care 2005, 11:S202-210.
13. De Vries SPW, Van Hijum SAFT, Schueler W, Riesbeck K, Hays JP, Hermans PWM, Bootsma HJ. Genome Analysis of Moraxella catarrhalis Strain RH4, a Human Respiratory Tract Pathogen. Journal of Bacteriology 2010, 192:3574-3583. 10.1128/JB.00121-10, 2897349, 20453089.
14. Bootsma H, van der Heide H, van de Pas S, Schouls L, Mooi F. Analysis of Moraxella catarrhalis by DNA typing: evidence for a distinct subpopulation associated with virulence traits. J Infect Dis 2000, 181:1376-1387. 10.1086/315374, 10762569.
15. Verduin CM, Kools-Sijmons M, van der Plas J, Vlooswijk J, Tromp M, van Dijk H, Banks J, Verbrugh H, van Belkum A. Complement-resistant Moraxella catarrhalis forms a genetically distinct lineage within the species. FEMS Microbiol Lett 2000, 184:1-8. 10.1111/j.1574-6968.2000.tb08981.x, 10689157.
16. Wirth T, Morelli G, Kusecek B, van Belkum A, van der Schee C, Meyer A, Achtman M. The rise and spread of a new pathogen: seroresistant Moraxella catarrhalis. Genome Research 2007, 17:1647-1656. 10.1101/gr.6122607, 2045147, 17895425.
17. 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.
18. Christensen JJ, Ursing J, Bruun B. Genotypic and phenotypic relatedness of 80 strains of Branhamella catarrhalis of worldwide origin. FEMS Microbiol Lett 1994, 119:155-159. 10.1111/j.1574-6968.1994.tb06882.x, 8039655.
19. Unhanand M, Maciver I, Ramilo O, Arencibia-Mireles O, Argyle JC, McCracken GH, Hansen EJ. Pulmonary clearance of Moraxella catarrhalis in an animal model. J Infect Dis 1992, 165:644-650.
20. 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 Biology 2007, 8:R103. 10.1186/gb-2007-8-6-r103, 2394751, 17550610.
21. 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. Journal of Bacteriology 2007, 189:8186-8195. 10.1128/JB.00690-07, 2168654, 17675389.
22. Hall BG, Ehrlich GD, Hu FZ. Pan-genome analysis provides much higher strain typing resolution than multi-locus sequence typing. Microbiology 2010, 156:1060-1068. 10.1099/mic.0.035188-0, 20019077.
23. Hays JP, Eadie K, Verduin CM, Verbrugh H, van Belkum A. A novel plasmid (pEMCJH03) isolated from Moraxella catarrhalis possibly useful as a cloning and expression vector within this species. Plasmid 2005, 53:263-268. 10.1016/j.plasmid.2004.11.003, 15848230.
24. Liu L, Hansen EJ. Structural analysis of plasmid pLQ510 from Moraxella catarrhalis E22. Plasmid 1999, 42:150-153. 10.1006/plas.1999.1411, 10489333.
25. Catlin BW. Branhamella catarrhalis: an organism gaining respect as a pathogen. Clin Microbiol Rev 1990, 3:293-320. 358165, 2121328.
26. Attia AS, Sedillo JL, Hoopman TC, Liu W, Liu L, Brautigam CA, Hansen EJ. Identification of a bacteriocin and its cognate immunity factor expressed by Moraxella catarrhalis. BMC Microbiol 2009, 9:207. 10.1186/1471-2180-9-207, 2761928, 19781080.
27. Alvarez-Martinez CE, Christie PJ. Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 2009, 73:775-808. 10.1128/MMBR.00023-09, 2786583, 19946141.
28. Moszer I, Rocha EP, Danchin A. Codon usage and lateral gene transfer in Bacillus subtilis. Curr Opin Microbiol 1999, 2:524-528. 10.1016/S1369-5274(99)00011-9, 10508724.
29. Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Molecular Biology and Evolution 1985, 2:13-34.
30. Bennetzen JL, Hall BD. Codon selection in yeast. J Biol Chem 1982, 257:3026-3031.
31. Dong H, Nilsson L, Kurland CG. Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. J Mol Biol 1996, 260:649-663. 10.1006/jmbi.1996.0428, 8709146.
32. Wright F. The 'effective number of codons' used in a gene. Gene 1990, 87:23-29. 10.1016/0378-1119(90)90491-9, 2110097.
33. Fuglsang A. Estimating the "effective number of codons": the Wright way of determining codon homozygosity leads to superior estimates. Genetics 2006, 172:1301-1307. 10.1534/genetics.105.049643, 1456227, 16299393.
34. Karginov FV, Hannon GJ. The CRISPR System: Small RNA-Guided Defense in Bacteria and Archaea. Molecular Cell 2010, 37:7-19. 10.1016/j.molcel.2009.12.033, 2819186, 20129051.
35. Horvath P, Barrangou R. CRISPR/Cas, the immune system of bacteria and archaea. Science 2010, 327:167-170. 10.1126/science.1179555, 20056882.
36. Godde JS, Bickerton A. The repetitive DNA elements called CRISPRs and their associated genes: evidence of horizontal transfer among prokaryotes. J Mol Evol 2006, 62:718-729. 10.1007/s00239-005-0223-z, 16612537.
37. Kunin V, Sorek R, Hugenholtz P. Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol 2007, 8:R61. 10.1186/gb-2007-8-4-r61, 1896005, 17442114.
38. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS ONE 2010, 5:e11147. 10.1371/journal.pone.0011147, 2892488, 20593022.
39. Segura D, Mahadevan R, Juarez K, Lovley DR. Computational and experimental analysis of redundancy in the central metabolism of Geobacter sulfurreducens. PLoS Comput Biol 2008, 4:e36. 10.1371/journal.pcbi.0040036, 2233667, 18266464.
40. Corthesy-Theulaz IE, Bergonzelli GE, Henry H, Bachmann D, Schorderet DF, Blum AL, Ornston LN. Cloning and characterization of Helicobacter pylori succinyl CoA:acetoacetate CoA-transferase, a novel prokaryotic member of the CoA-transferase family. J Biol Chem 1997, 272:25659-25667. 10.1074/jbc.272.41.25659, 9325289.
41. Perez Vidakovics ML, Riesbeck K. Virulence mechanisms of Moraxella in the pathogenesis of infection. Curr Opin Infect Dis 2009, 22:279-285. 10.1097/QCO.0b013e3283298e4e, 19405217.
42. Aebi C, Maciver I, Latimer J, Cope L, Stevens M, Thomas S, McCracken G, Hansen E. A protective epitope of Moraxella catarrhalis is encoded by two different genes. Infect Immun 1997, 65:4367. 175628, 9353007.
43. Lafontaine ER, Cope LD, Aebi C, Latimer JL, McCracken GH, Hansen EJ. The UspA1 protein and a second type of UspA2 protein mediate adherence of Moraxella catarrhalis to human epithelial cells in vitro. Journal of Bacteriology 2000, 182:1364-1373. 10.1128/JB.182.5.1364-1373.2000, 94425, 10671460.
44. Balder R, Hassel J, Lipski S, Lafontaine ER. Moraxella catarrhalis Strain O35E Expresses Two Filamentous Hemagglutinin-Like Proteins That Mediate Adherence to Human Epithelial Cells. Infect Immun 2007, 75:2765-2775. 10.1128/IAI.00079-07, 1932885, 17371858.
45. Plamondon P, Luke NR, Campagnari AA. Identification of a novel two-partner secretion locus in Moraxella catarrhalis. Infect Immun 2007, 75:2929-2936. 10.1128/IAI.00396-07, 1932880, 17420235.
46. Nelson KE, Weinstock GM, Highlander SK, Worley KC, Creasy HH, Wortman JR, Rusch DB, Mitreva M, Sodergren E, Chinwalla AT, Feldgarden M, Gevers D, Haas BJ, Madupu R, Ward DV, Birren BW, Gibbs RA, Methe B, Petrosino JF, Strausberg RL, Sutton GG, White OR, Wilson RK, Durkin S, Giglio MG, Gujja S, Howarth C, Kodira CD, Kyrpides N, Mehta T, et al. A Catalog of Reference Genomes from the Human Microbiome. Science 2010, 328:994-999. 10.1126/science.1183605, 2940224, 20489017.
47. Danner DB, Deich RA, Sisco KL, Smith HO. An eleven-base-pair sequence determines the specificity of DNA uptake in Haemophilus transformation. Gene 1980, 11:311-318. 10.1016/0378-1119(80)90071-2, 6260577.
48. Maughan H, Wilson LA, Redfield RJ. Bacterial DNA Uptake Sequences Can Accumulate by Molecular Drive Alone. Genetics 2010, 186:613-627. 10.1534/genetics.110.119438, 20628039.
49. Prudhomme M, Attaiech L, Sanchez G, Martin B, Claverys J-P. Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science 2006, 313:89-92. 10.1126/science.1127912, 16825569.
50. Broides A, Dagan R, Greenberg D, Givon-Lavi N, Leibovitz E. Acute otitis media caused by Moraxella catarrhalis: epidemiologic and clinical characteristics. Clin Infect Dis 2009, 49:1641-1647. 10.1086/647933, 19886799.
51. Armbruster CE, Hong W, Pang B, Weimer KED, Juneau RA, Turner J, Swords WE. Indirect Pathogenicity of Haemophilus influenzae and Moraxella catarrhalis in Polymicrobial Otitis Media Occurs via Interspecies Quorum Signaling. mBio 2010, 1:e00102-00110-e00102-00119.
52. Wardle JK. Branhamella catarrhalis as an indirect pathogen. Drugs 1986, 31(Suppl 3):93-96. 10.2165/00003495-198600313-00020, 3732085.
53. Hol C, Van Dijke EE, Verduin CM, Verhoef J, van Dijk H. Experimental evidence for Moraxella-induced penicillin neutralization in pneumococcal pneumonia. J Infect Dis 1994, 170:1613-1616.
54. Budhani RK, Struthers JK. Interaction of Streptococcus pneumoniae and Moraxella catarrhalis: investigation of the indirect pathogenic role of beta-lactamase-producing moraxellae by use of a continuous-culture biofilm system. Antimicrobial Agents and Chemotherapy 1998, 42:2521-2526. 105877, 9756750.
55. Brook I. Direct and indirect pathogenicity of Branhamella catarrhalis. Drugs 1986, 31(Suppl 3):97-102. 10.2165/00003495-198600313-00021, 3488202.
56. Tan Thuan T, Mörgelin M, Forsgren A, Riesbeck K. Haemophilus influenzae survival during complement-mediated attacks Is promoted by Moraxella catarrhalis outer membrane vesicles. J Infect Dis 2007, 195:1661-1670. 10.1086/517611, 17471436.
57. Luke NR, Howlett AJ, Shao J, Campagnari AA. Expression of type IV pili by Moraxella catarrhalis is essential for natural competence and is affected by iron limitation. Infect Immun 2004, 72:6262-6270. 10.1128/IAI.72.11.6262-6270.2004, 523052, 15501752.
58. Beuzon CR, Chessa D, Casadesus J. IS200: an old and still bacterial transposon. Int Microbiol 2004, 7:3-12.
59. Ton-Hoang B, Guynet C, Ronning DR, Cointin-Marty B, Dyda F, Chandler M. Transposition of ISHp608, member of an unusual family of bacterial insertion sequences. EMBO J 2005, 24:3325-3338. 10.1038/sj.emboj.7600787, 1224677, 16163392.
60. Mahillon J, Chandler M. Insertion sequences. Microbiol Mol Biol Rev 1998, 62:725-774. 98933, 9729608.
61. Kroll JS, Loynds BM, Moxon ER. The Haemophilus influenzae capsulation gene cluster: a compound transposon. Mol Microbiol 1991, 5:1549-1560. 10.1111/j.1365-2958.1991.tb00802.x, 1664907.
62. Satola SW, Napier B, Farley MM. Association of IS1016 with the hia Adhesin Gene and Biotypes V and I in Invasive Nontypeable Haemophilus influenzae. Infect Immun 2008, 76:5221-5227. 10.1128/IAI.00672-08, 2573369, 18794287.
63. NCBI Prokaryotic Genomes Automatic Annotation Pipeline (PGAAP). , http://www.ncbi.nlm.nih.gov/genomes/static/Pipeline.html
64. Pearson WR, Lipman DJ. Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 1988, 85:2444-2448. 10.1073/pnas.85.8.2444, 280013, 3162770.
65. Felsenstein J. PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author 2005, Department of Genome Sciences, University of Washington, Seattle.
66. Moraxella catarrhalis MLST Database. , http://mlst.ucc.ie/mlst/dbs/Mcatarrhalis
67. PUBMLST Tree-Drawing Application. , http://pubmlst.org/perl/mlstanalyse/mlstanalyse.pl?site=pubmlst&page=treedraw&referer=pubmlst.org
68. McInerney JO. GCUA: general codon usage analysis. Bioinformatics 1998, 14:372-373. 10.1093/bioinformatics/14.4.372, 9632833.
69. CodonW v. 1.4. , http://sourceforge.net/projects/codonw/
70. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 2007, 35:W52-57. 10.1093/nar/gkm360, 1933234, 17537822.
71. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 2007, 35:W182-185. 10.1093/nar/gkm321, 1933193, 17526522.
72. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL. Improved microbial gene identification with GLIMMER. Nucleic Acids Res 1999, 27:4636-4641. 10.1093/nar/27.23.4636, 148753, 10556321.
73. Wang W, Reitzer L, Rasko DA, Pearson MM, Blick RJ, Laurence C, Hansen EJ. Metabolic analysis of Moraxella catarrhalis and the effect of selected in vitro growth conditions on global gene expression. Infect Immun 2007, 75:4959-4971. 10.1128/IAI.00073-07, 2044516, 17620351.