1887

Abstract

is a common cause of respiratory tract infection, particularly otitis media in children, whilst it is also associated with the onset of exacerbation in chronic obstructive pulmonary disease in adults. Despite the need for an efficacious vaccine against , no candidates have progressed to clinical trial. This study, therefore, aimed to characterize the diversity of isolated from the upper respiratory tract of healthy children and adults, to gain a better understanding of the epidemiology of and the distribution of genes associated with virulence factors, to aid vaccine efforts. Isolates were sequenced and the presence of target genes reported. Contrary to prevailing data, this study found that lipooligosaccharide (LOS) B serotypes are not exclusively associated with 16S type 1. In addition, a particularly low prevalence of LOS B and high prevalence of LOS C serotypes was observed. isolates showed low prevalence of antimicrobial resistance and a high gene prevalence for a number of the target genes investigated: (also known as ), , , , , (also known as ), , , , , , , , and , , , , , mod, , , and .

Funding
This study was supported by the:
  • Bupa Foundation
    • Principle Award Recipient: StuartC. Clarke
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-05-26
2024-04-28
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References

  1. Aebi C. Moraxella catarrhalis – pathogen or commensal?. Adv Exp Med Biol 2011; 697:107–116 [View Article]
    [Google Scholar]
  2. Frosch PKW. Die Mikrokokken 1896
    [Google Scholar]
  3. Catlin BW. Branhamella catarrhalis: an organism gaining respect as a pathogen. Clin Microbiol Rev 1990; 3:293–320 [View Article] [PubMed]
    [Google Scholar]
  4. Feder HM, Garibaldi RA. The significance of nongonococcal, nonmeningococcal Neisseria isolates from blood cultures. Rev Infect Dis 1984; 6:181–188 [View Article] [PubMed]
    [Google Scholar]
  5. McLeod DT, Ahmad F, Power JT, Calder MA, Seaton A. Bronchopulmonary infection due to Branhamella catarrhalis. Br Med J (Clin Res Ed) 1983; 287:1446–1447 [View Article] [PubMed]
    [Google Scholar]
  6. Johnson MA, Drew WL, Roberts M. Branhamella (Neisseria) catarrhalis – a lower respiratory tract pathogen?. J Clin Microbiol 1981; 13:1066–1069 [View Article] [PubMed]
    [Google Scholar]
  7. Onofrio JM, Shulkin AN, Heidbrink PJ, Toews GB, Pierce AK. Pulmonary clearance and phagocytic cell response to normal pharyngeal flora. Am Rev Respir Dis 1981; 123:222–225 [View Article] [PubMed]
    [Google Scholar]
  8. Hager H, Verghese A, Alvarez S, Berk SL. Branhamella catarrhalis respiratory infections. Rev Infect Dis 1987; 9:1140–1149 [View Article] [PubMed]
    [Google Scholar]
  9. McNeely DJ, Kitchens CS, Kluge RM. Fatal Neisseria (Branhamella) catarrhalis pneumonia in an immunodeficient host. Am Rev Respir Dis 1976; 114:399–402 [View Article] [PubMed]
    [Google Scholar]
  10. Bosch AATM, Biesbroek G, Trzcinski K, Sanders EAM, Bogaert D. Viral and bacterial interactions in the upper respiratory tract. PLoS Pathog 2013; 9:e1003057 [View Article] [PubMed]
    [Google Scholar]
  11. Murphy TF, Bakaletz LO, Smeesters PR. Microbial interactions in the respiratory tract. Pediatr Infect Dis J 2009; 28:S121–S126 [View Article] [PubMed]
    [Google Scholar]
  12. Ngo CC, Massa HM, Thornton RB, Cripps AW. Predominant bacteria detected from the middle ear fluid of children experiencing otitis media: a systematic review. PLoS One 2016; 11:e0150949 [View Article] [PubMed]
    [Google Scholar]
  13. Monasta L, Ronfani L, Marchetti F, Montico M, Vecchi Brumatti L et al. Burden of disease caused by otitis media: systematic review and global estimates. PLoS One 2012; 7:e36226 [View Article] [PubMed]
    [Google Scholar]
  14. Faden H, Duffy L, Boeve M. Otitis media: back to basics. Pediatr Infect Dis J 1998; 17:1105–1112 [View Article] [PubMed]
    [Google Scholar]
  15. Murphy TF, Parameswaran GI. Moraxella catarrhalis, a human respiratory tract pathogen. Clin Infect Dis 2009; 49:124–131 [View Article]
    [Google Scholar]
  16. Wilkinson TMA, Aris E, Bourne S, Clarke SC, Peeters M et al. A prospective, observational cohort study of the seasonal dynamics of airway pathogens in the aetiology of exacerbations in COPD. Thorax 2017; 72:919–927 [View Article] [PubMed]
    [Google Scholar]
  17. World Health Organization The Top 10 Causes of Death 2018 ( http://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-of-death) Geneva: World Health Organization; 2018
    [Google Scholar]
  18. Wirth T, Morelli G, Kusecek B, van Belkum A, van der Schee C et al. The rise and spread of a new pathogen: seroresistant Moraxella catarrhalis. Genome Res 2007; 17:1647–1656 [View Article] [PubMed]
    [Google Scholar]
  19. Earl JP, de Vries SPW, Ahmed A, Powell E, Schultz MP et al. Comparative genomic analyses of the Moraxella catarrhalis serosensitive and seroresistant lineages demonstrate their independent evolution. Genome Biol Evol 2016; 8:955–974 [View Article] [PubMed]
    [Google Scholar]
  20. Schaller A, Troller R, Molina D, Gallati S, Aebi C et al. Rapid typing of Moraxella catarrhalis subpopulations based on outer membrane proteins using mass spectrometry. Proteomics 2006; 6:172–180 [View Article] [PubMed]
    [Google Scholar]
  21. Bootsma HJ, van der Heide HG, van de Pas S, Schouls LM, Mooi FR. Analysis of Moraxella catarrhalis by DNA typing: evidence for a distinct subpopulation associated with virulence traits. J Infect Dis 2000; 181:1376–1387 [View Article] [PubMed]
    [Google Scholar]
  22. Verhaegh SJC, Streefland A, Dewnarain JK, Farrell DJ, van Belkum A et al. Age-related genotypic and phenotypic differences in Moraxella catarrhalis isolates from children and adults presenting with respiratory disease in 2001–2002. Microbiology 2008; 154:1178–1184 [View Article] [PubMed]
    [Google Scholar]
  23. Fomsgaard JS, Fomsgaard A, Høiby N, Bruun B, Galanos C. Comparative immunochemistry of lipopolysaccharides from Branhamella catarrhalis strains. Infect Immun 1991; 59:3346–3349 [View Article] [PubMed]
    [Google Scholar]
  24. de Vries SPW, Bootsma HJ, Hays JP, Hermans PWM. Molecular aspects of Moraxella catarrhalis pathogenesis. Microbiol Mol Biol Rev 2009; 73:389–406 [View Article] [PubMed]
    [Google Scholar]
  25. Perez AC, Murphy TF. A Moraxella catarrhalis vaccine to protect against otitis media and exacerbations of COPD: an update on current progress and challenges. Hum Vaccin Immunother 2017; 13:2322–2331 [View Article] [PubMed]
    [Google Scholar]
  26. Perez AC, Murphy TF. Potential impact of a Moraxella catarrhalis vaccine in COPD. Vaccine 2019; 37:5551–5558 [View Article] [PubMed]
    [Google Scholar]
  27. Verhaegh SJC, Snippe ML, Levy F, Verbrugh HA, Jaddoe VWV et al. Colonization of healthy children by Moraxella catarrhalis is characterized by genotype heterogeneity, virulence gene diversity and co-colonization with Haemophilus influenzae. Microbiology 2011; 157:169–178 [View Article] [PubMed]
    [Google Scholar]
  28. Blakeway LV, Tan A, Peak IRA, Seib KL. Virulence determinants of Moraxella catarrhalis: distribution and considerations for vaccine development. Microbiology 2017; 163:1371–1384 [View Article] [PubMed]
    [Google Scholar]
  29. Möllenkvist A, Nordström T, Halldén C, Christensen JJ, Forsgren A et al. The Moraxella catarrhalis immunoglobulin D-binding protein MID has conserved sequences and is regulated by a mechanism corresponding to phase variation. J Bacteriol 2003; 185:2285–2295 [View Article] [PubMed]
    [Google Scholar]
  30. Coughtrie AL, Whittaker RN, Begum N, Anderson R, Tuck A et al. Evaluation of swabbing methods for estimating the prevalence of bacterial carriage in the upper respiratory tract: a cross sectional study. BMJ Open 2014; 4:e005341 [View Article] [PubMed]
    [Google Scholar]
  31. Coughtrie AL, Morris DE, Anderson R, Begum N, Cleary DW et al. Ecology and diversity in upper respiratory tract microbial population structures from a cross-sectional community swabbing study. J Med Microbiol 2018; 67:1096–1108 [View Article] [PubMed]
    [Google Scholar]
  32. Public Health England Identification of Moraxella species and Morphologically Similar Organisms London: Standards Unit, Microbiology Services, PHE; 2015
    [Google Scholar]
  33. van den Bergh MR, Bogaert D, Dun L, Vons J, Chu MLJN et al. Alternative sampling methods for detecting bacterial pathogens in children with upper respiratory tract infections. J Clin Microbiol 2012; 50:4134–4137 [View Article] [PubMed]
    [Google Scholar]
  34. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article] [PubMed]
    [Google Scholar]
  35. Nurk S, Bankevich A, Antipov D, Gurevich A, Korobeynikov A et al. Assembling genomes and mini-metagenomes from highly chimeric reads. In Deng M, Jiang R, Sun F, Zhang X. eds Research in Computational Molecular Biology Berlin, Heidelberg: Springer; 2013
    [Google Scholar]
  36. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  37. Edwards KJ, Schwingel JM, Datta AK, Campagnari AA. Multiplex PCR assay that identifies the major lipooligosaccharide serotype expressed by Moraxella catarrhalis clinical isolates. J Clin Microbiol 2005; 43:6139–6143 [View Article] [PubMed]
    [Google Scholar]
  38. Inouye M, Dashnow H, Raven L-A, Schultz MB, Pope BJ et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 2014; 6:90 [View Article] [PubMed]
    [Google Scholar]
  39. Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 2014; 15:524 [View Article] [PubMed]
    [Google Scholar]
  40. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:W242–W245 [View Article] [PubMed]
    [Google Scholar]
  41. Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG et al. Anvio: an advanced analysis and visualization platform foromics data. PeerJ 2015; 3:e1319 [View Article] [PubMed]
    [Google Scholar]
  42. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 2012; 67:2640–2644 [View Article] [PubMed]
    [Google Scholar]
  43. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:539 [View Article] [PubMed]
    [Google Scholar]
  44. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754–1760 [View Article] [PubMed]
    [Google Scholar]
  45. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [View Article] [PubMed]
    [Google Scholar]
  46. Vaneechoutte M, Verschraegen G, Claeys G, Van Den Abeele AM. Serological typing of Branhamella catarrhalis strains on the basis of lipopolysaccharide antigens. J Clin Microbiol 1990; 28:182–187 [View Article] [PubMed]
    [Google Scholar]
  47. Mitov IG, Gergova RT, Ouzounova-Raykova VV. Distribution of genes encoding virulence factors ompB2, ompCD, ompE, β-lactamase and serotype in pathogenic and colonizing strains of Moraxella catarrhalis. Arch Med Res 2010; 41:530–535 [View Article] [PubMed]
    [Google Scholar]
  48. Nunvar J, Huckova T, Licha I. Identification and characterization of repetitive extragenic palindromes (REP)-associated tyrosine transposases: implications for REP evolution and dynamics in bacterial genomes. BMC Genomics 2010; 11:44 [View Article] [PubMed]
    [Google Scholar]
  49. Galperin MY, Jedrzejas MJ. Conserved core structure and active site residues in alkaline phosphatase superfamily enzymes. Proteins 2001; 45:318–324 [View Article] [PubMed]
    [Google Scholar]
  50. Harsági N, Keglevich G. The hydrolysis of phosphinates and phosphonates: a review. Molecules 2021; 26:2840 [View Article] [PubMed]
    [Google Scholar]
  51. Zaheer R, Morton R, Proudfoot M, Yakunin A, Finan TM. Genetic and biochemical properties of an alkaline phosphatase PhoX family protein found in many bacteria. Environ Microbiol 2009; 11:1572–1587 [View Article] [PubMed]
    [Google Scholar]
  52. Icho T, Raetz CR. Multiple genes for membrane-bound phosphatases in Escherichia coli and their action on phospholipid precursors. J Bacteriol 1983; 153:722–730 [View Article] [PubMed]
    [Google Scholar]
  53. Schneider E, Hunke S. ATP-binding-cassette (ABC) transport systems: functional and structural aspects of the ATP-hydrolyzing subunits/domains. FEMS Microbiol Rev 1998; 22:1–20 [View Article] [PubMed]
    [Google Scholar]
  54. Williams RJ. Restriction endonucleases: classification, properties, and applications. Mol Biotechnol 2003; 23:225–243 [View Article] [PubMed]
    [Google Scholar]
  55. Waite-Rees PA, Keating CJ, Moran LS, Slatko BE, Hornstra LJ et al. Characterization and expression of the Escherichia coli Mrr restriction system. J Bacteriol 1991; 173:5207–5219 [View Article] [PubMed]
    [Google Scholar]
  56. Aertsen A, Michiels CW. Mrr instigates the SOS response after high pressure stress in Escherichia coli. Mol Microbiol 2005; 58:1381–1391 [View Article] [PubMed]
    [Google Scholar]
  57. Briolat V, Reysset G. Identification of the Clostridium perfringens genes involved in the adaptive response to oxidative stress. J Bacteriol 2002; 184:2333–2343 [View Article] [PubMed]
    [Google Scholar]
  58. Fujisawa H, Nagata S, Misono H. Characterization of short-chain dehydrogenase/reductase homologues of Escherichia coli (YdfG) and Saccharomyces cerevisiae (YMR226C). Biochim Biophys Acta 2003; 1645:89–94 [View Article] [PubMed]
    [Google Scholar]
  59. Hu Y, Hu Q, Wei R, Li R, Zhao D et al. The XRE family transcriptional regulator SrtR in Streptococcus suis is involved in oxidant tolerance and virulence. Front Cell Infect Microbiol 2018; 8:452 [View Article] [PubMed]
    [Google Scholar]
  60. Ruan B, Söll D. The bacterial YbaK protein is a Cys-tRNAPro and Cys-tRNA Cys deacylase. J Biol Chem 2005; 280:25887–25891 [View Article] [PubMed]
    [Google Scholar]
  61. Kumar S, Das M, Hadad CM, Musier-Forsyth K. Aminoacyl-tRNA substrate and enzyme backbone atoms contribute to translational quality control by YbaK. J Phys Chem B 2013; 117:4521–4527 [View Article] [PubMed]
    [Google Scholar]
  62. Liger D, Quevillon-Cheruel S, Sorel I, Bremang M, Blondeau K et al. Crystal structure of YHI9, the yeast member of the phenazine biosynthesis PhzF enzyme superfamily. Proteins 2005; 60:778–786 [View Article] [PubMed]
    [Google Scholar]
  63. López-Garrido J, Casadesús J. The DamX protein of Escherichia coli and Salmonella enterica. Gut Microbes 2010; 1:285–288 [View Article] [PubMed]
    [Google Scholar]
  64. Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M et al. ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother 2014; 58:212–220 [View Article] [PubMed]
    [Google Scholar]
  65. Bootsma HJ, van Dijk H, Verhoef J, Fleer A, Mooi FR. Molecular characterization of the BRO beta-lactamase of Moraxella (Branhamella) catarrhalis. Antimicrob Agents Chemother 1996; 40:966–972 [View Article] [PubMed]
    [Google Scholar]
  66. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 2020; 75:3491–3500 [View Article] [PubMed]
    [Google Scholar]
  67. McGregor K, Chang BJ, Mee BJ, Riley TV. Moraxella catarrhalis: clinical significance, antimicrobial susceptibility and BRO beta-lactamases. Eur J Clin Microbiol Infect Dis 1998; 17:219–234 [View Article] [PubMed]
    [Google Scholar]
  68. Ejlertsen T, Skov R. The beta-lactamases of Moraxella (Branhamella) catarrhalis isolated from Danish children. APMIS 1996; 104:557–562 [View Article] [PubMed]
    [Google Scholar]
  69. Wallace RJ Jr, Steingrube VA, Nash DR, Hollis DG, Flanagan C et al. BRO beta-lactamases of Branhamella catarrhalis and Moraxella subgenus Moraxella, including evidence for chromosomal beta-lactamase transfer by conjugation in B. catarrhalis, M. nonliquefaciens, and M. lacunata. Antimicrob Agents Chemother 1989; 33:1845–1854 [View Article] [PubMed]
    [Google Scholar]
  70. Shi W, Wen D, Chen C, Yuan L, Gao W et al. β-Lactamase production and antibiotic susceptibility pattern of Moraxella catarrhalis isolates collected from two county hospitals in China. BMC Microbiol 2018; 18:77 [View Article] [PubMed]
    [Google Scholar]
  71. Easton DM, Smith A, Gallego SG, Foxwell AR, Cripps AW et al. Characterization of a novel porin protein from Moraxella catarrhalis and identification of an immunodominant surface loop. J Bacteriol 2005; 187:6528–6535 [View Article] [PubMed]
    [Google Scholar]
  72. 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 [View Article] [PubMed]
    [Google Scholar]
  73. Milne I, Stephen G, Bayer M, Cock PJA, Pritchard L et al. Using tablet for visual exploration of second-generation sequencing data. Brief Bioinform 2013; 14:193–202 [View Article] [PubMed]
    [Google Scholar]
  74. 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 [View Article] [PubMed]
    [Google Scholar]
  75. Plamondon P, Luke NR, Campagnari AA. Identification of a novel two-partner secretion locus in Moraxella catarrhalis. Infect Immun 2007; 75:2929–2936 [View Article] [PubMed]
    [Google Scholar]
  76. Myers LE, Yang YP, Du RP, Wang Q, Harkness RE et al. The transferrin binding protein B of Moraxella catarrhalis elicits bactericidal antibodies and is a potential vaccine antigen. Infect Immun 1998; 66:4183–4192 [View Article] [PubMed]
    [Google Scholar]
  77. Du RP, Wang Q, Yang YP, Schryvers AB, Chong P et al. Cloning and expression of the Moraxella catarrhalis lactoferrin receptor genes. Infect Immun 1998; 66:3656–3665 [View Article] [PubMed]
    [Google Scholar]
  78. Ruckdeschel EA, Kirkham C, Lesse AJ, Hu Z, Murphy TF. Mining the Moraxella catarrhalis genome: identification of potential vaccine antigens expressed during human infection. Infect Immun 2008; 76:1599–1607 [View Article] [PubMed]
    [Google Scholar]
  79. Blakeway LV, Power PM, Jen FE-C, Worboys SR, Boitano M et al. ModM DNA methyltransferase methylome analysis reveals a potential role for Moraxella catarrhalis phasevarions in otitis media. FASEB J 2014; 28:5197–5207 [View Article] [PubMed]
    [Google Scholar]
  80. Luke-Marshall NR, Sauberan SL, Campagnari AA. Comparative analyses of the Moraxella catarrhalis type-IV pilus structural subunit PilA. Gene 2011; 477:19–23 [View Article] [PubMed]
    [Google Scholar]
  81. Buskirk SW, Lafontaine ER. Moraxella catarrhalis expresses a cardiolipin synthase that impacts adherence to human epithelial cells. J Bacteriol 2014; 196:107–120 [View Article] [PubMed]
    [Google Scholar]
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