1887

Abstract

Candidatus Ornithobacterium hominis’ represents a new member of the Flavobacteriaceae detected in 16S rRNA gene surveys of people from South-East Asia, Africa and Australia. It frequently colonizes the infant nasopharynx at high proportional abundance, and we demonstrate its presence in 42 % of nasopharyngeal swabs from 12-month-old children in the Maela refugee camp in Thailand. The species, a Gram-negative bacillus, has not yet been cultured, but the cells can be identified in mixed samples by fluorescent hybridization. Here, we report seven genomes assembled from metagenomic data, two to improved draft standard. The genomes are approximately 1.9 Mb, sharing 62 % average amino acid identity with the only other member of the genus, the bird pathogen Ornithobacterium rhinotracheale . The draft genomes encode multiple antibiotic-resistance genes, competition factors, Flavobacterium johnsoniae -like gliding motility genes and a homologue of the Pasteurella multocida mitogenic toxin. Intra- and inter-host genome comparison suggests that colonization with this bacterium is both persistent and strain exclusive.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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2019-02-05
2024-04-18
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References

  1. Salter SJ, Turner C, Watthanaworawit W, De Goffau MC, Wagner J et al. A longitudinal study of the infant nasopharyngeal microbiota: the effects of age, illness and antibiotic use in a cohort of South East Asian children. PLoS Negl Trop Dis 2017; 11:e0005975 [View Article][PubMed]
    [Google Scholar]
  2. Kwambana BA, Mohammed NI, Jeffries D, Barer M, Adegbola RA et al. Differential effects of frozen storage on the molecular detection of bacterial taxa that inhabit the nasopharynx. BMC Clin Pathol 2011; 11:2 [View Article][PubMed]
    [Google Scholar]
  3. Kwambana-Adams B, Hanson B, Worwui A, Agbla S, Foster-Nyarko E et al. Rapid replacement by non-vaccine pneumococcal serotypes may mitigate the impact of the pneumococcal conjugate vaccine on nasopharyngeal bacterial ecology. Sci Rep 2017; 7:8127 [View Article][PubMed]
    [Google Scholar]
  4. Feazel LM, Santorico SA, Robertson CE, Bashraheil M, Scott JA et al. Effects of vaccination with 10-valent pneumococcal non-typeable Haemophilus influenza protein D conjugate vaccine (PHiD-CV) on the nasopharyngeal microbiome of Kenyan toddlers. PLoS One 2015; 10:e0128064 [View Article][PubMed]
    [Google Scholar]
  5. Marsh RL, Kaestli M, Chang AB, Binks MJ, Pope CE et al. The microbiota in bronchoalveolar lavage from young children with chronic lung disease includes taxa present in both the oropharynx and nasopharynx. Microbiome 2016; 4:37 [View Article][PubMed]
    [Google Scholar]
  6. Eren AM, Morrison HG, Lescault PJ, Reveillaud J, Vineis JH et al. Minimum entropy decomposition: unsupervised oligotyping for sensitive partitioning of high-throughput marker gene sequences. Isme J 2015; 9:968–979 [View Article][PubMed]
    [Google Scholar]
  7. Turner P, Turner C, Jankhot A, Helen N, Lee SJ et al. A longitudinal study of Streptococcus pneumoniae carriage in a cohort of infants and their mothers on the Thailand-Myanmar border. PLoS One 2012; 7:e38271 [View Article][PubMed]
    [Google Scholar]
  8. Turner C, Turner P, Carrara V, Burgoine K, Tha Ler Htoo S et al. High rates of pneumonia in children under two years of age in a South East Asian refugee population. PLoS One 2013; 8:e54026 [View Article][PubMed]
    [Google Scholar]
  9. WHO Cough or Difficulty Breathing. Pocket Book of Hospital Care for Children: Guidelines for the Management of Common Illnesses with Limited Resources, 2nd edn.. Geneva:: World Health Organization; 2013
    [Google Scholar]
  10. Scott P, Walker A. Whole genome amplification of single bacterial cells. In McGenity TJ, Timmis KN, Fernandez BN. (editors) Hydrocarbon and Lipid Microbiology Protocols: Single-Cell and Single-Molecule Methods Berlin, Heidelberg: Springer Nature; 2016 pp. 29–41
    [Google Scholar]
  11. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 2014; 15:R46 [View Article][PubMed]
    [Google Scholar]
  12. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
    [Google Scholar]
  13. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article]
    [Google Scholar]
  14. Bonfield JK, Whitwham A. Gap5-editing the billion fragment sequence assembly. Bioinformatics 2010; 26:1699–1703 [View Article][PubMed]
    [Google Scholar]
  15. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  16. Pruitt KD, Tatusova T, Brown GR, Maglott DR. NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res 2012; 40:D130–D135 [View Article][PubMed]
    [Google Scholar]
  17. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 2016:e1900v1901
    [Google Scholar]
  18. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article][PubMed]
    [Google Scholar]
  19. Qin QL, Xie BB, Zhang XY, Chen XL, Zhou BC et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196:2210–2215 [View Article][PubMed]
    [Google Scholar]
  20. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article][PubMed]
    [Google Scholar]
  21. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  22. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 2012; 40:D109–D114 [View Article][PubMed]
    [Google Scholar]
  23. Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 2016; 428:726–731 [View Article][PubMed]
    [Google Scholar]
  24. Pourhoseingholi MA, Vahedi M, Rahimzadeh M. Sample size calculation in medical studies. Gastroenterol Hepatol Bed Bench 2013; 6:14–17[PubMed]
    [Google Scholar]
  25. Shi J, Blundell TL, Mizuguchi K. FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol 2001; 310:243–257 [View Article][PubMed]
    [Google Scholar]
  26. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN et al. The Protein Data Bank. Nucleic Acids Res 2000; 28:235–242 [View Article][PubMed]
    [Google Scholar]
  27. Kitadokoro K, Kamitani S, Miyazawa M, Hanajima-Ozawa M, Fukui A et al. Crystal structures reveal a thiol protease-like catalytic triad in the C-terminal region of Pasteurella multocida toxin. Proc Natl Acad Sci USA 2007; 104:5139–5144 [View Article][PubMed]
    [Google Scholar]
  28. Webb B, Sali A. Comparative protein structure modeling using MODELLER. Curr Protoc Bioinformatics 2016; 54:5.6.1–5.6.37
    [Google Scholar]
  29. Zehr ES, Bayles DO, Boatwright WD, Tabatabai LB, Register KB. Complete genome sequence of Ornithobacterium rhinotracheale strain ORT-UMN 88. Stand Genomic Sci 2014; 9:16 [View Article][PubMed]
    [Google Scholar]
  30. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article][PubMed]
    [Google Scholar]
  31. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom 2016; 2:e000056 [View Article][PubMed]
    [Google Scholar]
  32. Nakane D, Sato K, Wada H, Mcbride MJ, Nakayama K. Helical flow of surface protein required for bacterial gliding motility. Proc Natl Acad Sci USA 2013; 110:11145–11150 [View Article][PubMed]
    [Google Scholar]
  33. Lasica AM, Ksiazek M, Madej M, Potempa J. The type IX secretion system (T9SS): highlights and recent insights into its structure and function. Front Cell Infect Microbiol 2017; 7:215 [View Article][PubMed]
    [Google Scholar]
  34. Johnston JJ, Shrivastava A, Mcbride MJ. Untangling Flavobacterium johnsoniae gliding motility and protein secretion. J Bacteriol 2018; 200:e00362-17 [View Article][PubMed]
    [Google Scholar]
  35. Barbier P, Lunazzi A, Fujiwara-Nagata E, Avendaño-Herrera R, Bernardet JF et al. From the Flavobacterium genus to the phylum Bacteroidetes: genomic analysis of dnd gene clusters. FEMS Microbiol Lett 2013; 348:26–35 [View Article][PubMed]
    [Google Scholar]
  36. Tribble GD, Parker AC, Smith CJ. The Bacteroides mobilizable transposon Tn4555 integrates by a site-specific recombination mechanism similar to that of the gram-positive bacterial element Tn916. J Bacteriol 1997; 179:2731–2739 [View Article][PubMed]
    [Google Scholar]
  37. Jackson AP, Thomas GH, Parkhill J, Thomson NR. Evolutionary diversification of an ancient gene family (rhs) through C-terminal displacement. BMC Genomics 2009; 10:584 [View Article][PubMed]
    [Google Scholar]
  38. Koskiniemi S, Lamoureux JG, Nikolakakis KC, T'kint de Roodenbeke C, Kaplan MD et al. Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci USA 2013; 110:7032–7037 [View Article][PubMed]
    [Google Scholar]
  39. Cuthbertson L, Rogers GB, Walker AW, Oliver A, Hoffman LR et al. Implications of multiple freeze-thawing on respiratory samples for culture-independent analyses. J Cyst Fibros 2015; 14:464–467 [View Article][PubMed]
    [Google Scholar]
  40. Pérez Morales TG, Ho TD, Liu WT, Dorrestein PC, Ellermeier CD. Production of the cannibalism toxin SDP is a multistep process that requires SdpA and SdpB. J Bacteriol 2013; 195:3244–3251 [View Article][PubMed]
    [Google Scholar]
  41. Lerouge I, Vanderleyden J. O-antigen structural variation: mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol Rev 2002; 26:17–47 [View Article][PubMed]
    [Google Scholar]
  42. Thieme S, Mühldorfer K, Lüschow D, Hafez HM. Molecular characterization of the recently emerged poultry pathogen Ornithobacterium rhinotracheale by multilocus sequence typing. PLoS One 2016; 11:e0148158 [View Article][PubMed]
    [Google Scholar]
  43. Nan B, Zusman DR. Novel mechanisms power bacterial gliding motility. Mol Microbiol 2016; 101:186–193 [View Article][PubMed]
    [Google Scholar]
  44. Mcbride MJ, Zhu Y. Gliding motility and Por secretion system genes are widespread among members of the phylum Bacteroidetes. J Bacteriol 2013; 195:270–278 [View Article][PubMed]
    [Google Scholar]
  45. Chakraborty S, Kloos B, Harre U, Schett G, Kubatzky KF. Pasteurella multocida toxin triggers RANKL-independent osteoclastogenesis. Front Immunol 2017; 8:185 [View Article][PubMed]
    [Google Scholar]
  46. Klein NC, Cunha BA. Pasteurella multocida pneumonia. Semin Respir Infect 1997; 12:54–56[PubMed]
    [Google Scholar]
  47. Pijoan C, Lastra A, Ramirez C, Leman AD. Isolation of toxigenic strains of Pasteurella multocida from lungs of pneumonic swine. J Am Vet Med Assoc 1984; 185:522–523[PubMed]
    [Google Scholar]
  48. Wilson BA, Ho M. Pasteurella multocida toxin interaction with host cells: entry and cellular effects. Curr Top Microbiol Immunol 2012; 361:93–111 [View Article][PubMed]
    [Google Scholar]
  49. Weise M, Vettel C, Spiger K, Gilsbach R, Hein L et al. A systemic Pasteurella multocida toxin aggravates cardiac hypertrophy and fibrosis in mice. Cell Microbiol 2015; 17:1320–1331 [View Article][PubMed]
    [Google Scholar]
  50. Cheville NF, Rimler RB. A protein toxin from Pasteurella multocida type D causes acute and chronic hepatic toxicity in rats. Vet Pathol 1989; 26:148–157 [View Article][PubMed]
    [Google Scholar]
  51. Hoskins IC, Thomas LH, Lax AJ. Nasal infection with Pasteurella multocida causes proliferation of bladder epithelium in gnotobiotic pigs. Vet Rec 1997; 140:22 [View Article][PubMed]
    [Google Scholar]
  52. Orth JH, Aktories K. Molecular biology of Pasteurella multocida toxin. Curr Top Microbiol Immunol 2012; 361:73–92 [View Article][PubMed]
    [Google Scholar]
  53. Orth JH, Preuss I, Fester I, Schlosser A, Wilson BA et al. Pasteurella multocida toxin activation of heterotrimeric G proteins by deamidation. Proc Natl Acad Sci USA 2009; 106:7179–7184 [View Article][PubMed]
    [Google Scholar]
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