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Abstract

The genus Neisseria comprises a diverse group of commensal bacteria, which typically colonize the mucosal surfaces of humans and other animals. Neisseria meningitidis, the meningococcus, is notable for its potential to cause invasive meningococcal disease (IMD) in humans; however, IMD is comparatively rare, and meningococci normally colonize the nasopharynx asymptomatically. Possession of a polysaccharide capsule has been shown to be a prerequisite for disease in almost all IMD cases, and was previously considered unique to N. meningitidis, and potentially acquired by horizontal genetic transfer (HGT). Nevertheless, the capsule must also have some role in asymptomatic colonization and/or transmission, consistent with the existence of six non-disease-associated meningococcal capsule serogroups. In this study, full complements of putative capsule genes were identified in non-pathogenic Neisseria species, including Neisseria subflava and Neisseria elongata. These species contained genes for capsule transport and translocation homologous to those of N. meningitidis, as well as novel putative capsule synthesis genes. Phylogenetic analyses were consistent with the proposal that these genes were acquired by the meningococcus through HGT. In contrast with previous evolutionary models, however, the most parsimonious explanation of these data was that capsule transport genes had been lost in the common ancestor of the meningococcus, gonococcus, and their close relatives, and then reacquired by some meningococci. The most likely donor of the meningococcal transport genes was another Neisseria species.

  • 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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2018-08-03
2024-03-28
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References

  1. Liu G, Tang CM, Exley RM. Non-pathogenic Neisseria: members of an abundant, multi-habitat, diverse genus. Microbiology 2015; 161:1297–1312 [View Article][PubMed]
    [Google Scholar]
  2. Rosenstein NE, Perkins BA, Stephens DS, Popovic T, Hughes JM et al. Meningococcal disease. N Engl J Med 2001; 344:1378–1388 [View Article][PubMed]
    [Google Scholar]
  3. Schoen C, Blom J, Claus H, Schramm-Glück A, Brandt P et al. Whole-genome comparison of disease and carriage strains provides insights into virulence evolution in Neisseria meningitidis. Proc Natl Acad Sci USA 2008; 105:3473–3478 [View Article][PubMed]
    [Google Scholar]
  4. Roberts IS. The biochemistry and genetics of capsular polysaccharide production in bacteria. Annu Rev Microbiol 1996; 50:285–315 [View Article][PubMed]
    [Google Scholar]
  5. Ulanova M, Tsang RSW. Haemophilus influenzae serotype a as a cause of serious invasive infections. Lancet Infect Dis 2014; 14:70–82 [View Article][PubMed]
    [Google Scholar]
  6. Podschun R, Ullmann U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev 1998; 11:589–603[PubMed]
    [Google Scholar]
  7. Halperin SA, Bettinger JA, Greenwood B, Harrison LH, Jelfs J et al. The changing and dynamic epidemiology of meningococcal disease. Vaccine 2012; 30:B26–B36 [View Article][PubMed]
    [Google Scholar]
  8. Kahler CM, Martin LE, Shih GC, Rahman MM, Carlson RW et al. The (alpha2–>8)-linked polysialic acid capsule and lipooligosaccharide structure both contribute to the ability of serogroup B Neisseria meningitidis to resist the bactericidal activity of normal human serum. Infect Immun 1998; 66:5939–5947[PubMed]
    [Google Scholar]
  9. Unkmeir A, Kämmerer U, Stade A, Hübner C, Haller S et al. Lipooligosaccharide and polysaccharide capsule: virulence factors of Neisseria meningitidis that determine meningococcal interaction with human dendritic cells. Infect Immun 2002; 70:2454–2462 [View Article][PubMed]
    [Google Scholar]
  10. Cowen JP. Morphological study of marine bacterial capsules: implications for marine aggregates. Mar Biol 1992; 114:85–95
    [Google Scholar]
  11. Liu CH, Lee SM, Vanlare JM, Kasper DL, Mazmanian SK. Regulation of surface architecture by symbiotic bacteria mediates host colonization. Proc Natl Acad Sci USA 2008; 105:3951–3956 [View Article][PubMed]
    [Google Scholar]
  12. Weber MV, Claus H, Maiden MC, Frosch M, Vogel U. Genetic mechanisms for loss of encapsulation in polysialyltransferase-gene-positive meningococci isolated from healthy carriers. Int J Med Microbiol 2006; 296:475–484 [View Article][PubMed]
    [Google Scholar]
  13. Loh E, Kugelberg E, Tracy A, Zhang Q, Gollan B et al. Temperature triggers immune evasion by Neisseria meningitidis. Nature 2013; 502:237–240 [View Article][PubMed]
    [Google Scholar]
  14. Willis LM, Stupak J, Richards MR, Lowary TL, Li J et al. Conserved glycolipid termini in capsular polysaccharides synthesized by ATP-binding cassette transporter-dependent pathways in Gram-negative pathogens. Proc Natl Acad Sci USA 2013; 110:7868–7873 [View Article][PubMed]
    [Google Scholar]
  15. Harrison OB, Claus H, Jiang Y, Bennett JS, Bratcher HB et al. Description and nomenclature of Neisseria meningitidis capsule locus. Emerg Infect Dis 2013; 19:566–573 [View Article][PubMed]
    [Google Scholar]
  16. Willis LM, Whitfield C. Structure, biosynthesis, and function of bacterial capsular polysaccharides synthesized by ABC transporter-dependent pathways. Carbohydr Res 2013; 378:35–44 [View Article][PubMed]
    [Google Scholar]
  17. Hammerschmidt S, Birkholz C, Zähringer U, Robertson BD, van Putten J et al. Contribution of genes from the capsule gene complex (cps) to lipooligosaccharide biosynthesis and serum resistance in Neisseria meningitidis. Mol Microbiol 1994; 11:885–896 [View Article][PubMed]
    [Google Scholar]
  18. Petering H, Hammerschmidt S, Frosch M, van Putten JP, Ison CA et al. Genes associated with meningococcal capsule complex are also found in Neisseria gonorrhoeae. J Bacteriol 1996; 178:3342–3345 [View Article][PubMed]
    [Google Scholar]
  19. Claus H, Maiden MC, Maag R, Frosch M, Vogel U. Many carried meningococci lack the genes required for capsule synthesis and transport. Microbiology 2002; 148:1813–1819 [View Article][PubMed]
    [Google Scholar]
  20. Snyder LA, Saunders NJ. The majority of genes in the pathogenic Neisseria species are present in non-pathogenic Neisseria lactamica, including those designated as 'virulence genes'. BMC Genomics 2006; 7:128 [View Article][PubMed]
    [Google Scholar]
  21. Marri PR, Paniscus M, Weyand NJ, Rendón MA, Calton CM et al. Genome sequencing reveals widespread virulence gene exchange among human Neisseria species. PLoS One 2010; 5:e11835 [View Article][PubMed]
    [Google Scholar]
  22. Bartley SN, Mowlaboccus S, Mullally CA, Stubbs KA, Vrielink A et al. Acquisition of the capsule locus by horizontal gene transfer in Neisseria meningitidis is often accompanied by the loss of UDP-GalNAc synthesis. Sci Rep 2017; 7:44442 [View Article][PubMed]
    [Google Scholar]
  23. Jolley KA, Maiden MC. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010; 11:595 [View Article][PubMed]
    [Google Scholar]
  24. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C et al. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 2012; 158:1005–1015 [View Article][PubMed]
    [Google Scholar]
  25. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P et al. Artemis: sequence visualization and annotation. Bioinformatics 2000; 16:944–945 [View Article][PubMed]
    [Google Scholar]
  26. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article][PubMed]
    [Google Scholar]
  27. Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J et al. The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 2016; 44:D279–D285 [View Article][PubMed]
    [Google Scholar]
  28. Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res 2014; 42:D490–D495 [View Article][PubMed]
    [Google Scholar]
  29. Park BH, Karpinets TV, Syed MH, Leuze MR, Uberbacher EC. CAZymes analysis toolkit (CAT): web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology 2010; 20:1574–1584 [View Article][PubMed]
    [Google Scholar]
  30. Guy L, Kultima JR, Andersson SG. genoPlotR: comparative gene and genome visualization in R. Bioinformatics 2010; 26:2334–2335 [View Article][PubMed]
    [Google Scholar]
  31. 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]
  32. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG et al. ACT: the artemis comparison tool. Bioinformatics 2005; 21:3422–3423 [View Article][PubMed]
    [Google Scholar]
  33. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002; 30:3059–3066 [View Article][PubMed]
    [Google Scholar]
  34. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article][PubMed]
    [Google Scholar]
  35. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9:772 [View Article][PubMed]
    [Google Scholar]
  36. Didelot X, Wilson DJ. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput Biol 2015; 11:e1004041 [View Article][PubMed]
    [Google Scholar]
  37. Huerta-Cepas J, Serra F, Bork P. ETE 3: reconstruction, analysis, and visualization of phylogenomic data. Mol Biol Evol 2016; 33:1635–1638 [View Article][PubMed]
    [Google Scholar]
  38. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article][PubMed]
    [Google Scholar]
  39. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article][PubMed]
    [Google Scholar]
  40. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011; 27:1164–1165 [View Article][PubMed]
    [Google Scholar]
  41. Skov Sørensen UB, Yao K, Yang Y, Tettelin H, Kilian M. Capsular polysaccharide expression in commensal Streptococcus species: genetic and antigenic similarities to Streptococcus pneumoniae. MBio 2016; 7:e01844-16 [View Article][PubMed]
    [Google Scholar]
  42. Hill C. Virulence or niche factors: what's in a name?. J Bacteriol 2012; 194:5725–5727 [View Article][PubMed]
    [Google Scholar]
  43. Claus H, Stummeyer K, Batzilla J, Mühlenhoff M, Vogel U. Amino acid 310 determines the donor substrate specificity of serogroup W-135 and Y capsule polymerases of Neisseria meningitidis. Mol Microbiol 2009; 71:960–971 [View Article][PubMed]
    [Google Scholar]
  44. Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 2006; 75:39–68 [View Article][PubMed]
    [Google Scholar]
  45. Donati C, Zolfo M, Albanese D, Tin Truong D, Asnicar F et al. Uncovering oral Neisseria tropism and persistence using metagenomic sequencing. Nat Microbiol 2016; 1:16070 [View Article][PubMed]
    [Google Scholar]
  46. Lerat E, Daubin V, Ochman H, Moran NA. Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 2005; 3:e130 [View Article][PubMed]
    [Google Scholar]
  47. Van Passel MW, Marri PR, Ochman H. The emergence and fate of horizontally acquired genes in Escherichia coli. PLoS Comput Biol 2008; 4:e1000059 [View Article][PubMed]
    [Google Scholar]
  48. Wörmann ME, Horien CL, Bennett JS, Jolley KA, Maiden MCJ et al. Sequence, distribution and chromosomal context of class I and class II pilin genes of Neisseria meningitidis identified in whole genome sequences. BMC Genomics 2014; 15:253 [View Article][PubMed]
    [Google Scholar]
  49. Nielsen SM, de Gier C, Dimopoulou C, Gupta V, Hansen LH et al. The capsule biosynthesis locus of Haemophilus influenzae shows conspicuous similarity to the corresponding locus in Haemophilus sputorum and may have been recruited from this species by horizontal gene transfer. Microbiology 2015; 161:1182–1188 [View Article][PubMed]
    [Google Scholar]
  50. Frosch M, Edwards U, Bousset K, Krausse B, Weisgerber C. Evidence for a common molecular origin of the capsule gene loci in gram-negative bacteria expressing group II capsular polysaccharides. Mol Microbiol 1991; 5:1251–1263 [View Article][PubMed]
    [Google Scholar]
  51. Lâm TT, Claus H, Frosch M, Vogel U. Sequence analysis of serotype-specific synthesis regions II of Haemophilus influenzae serotypes c and d: evidence for common ancestry of capsule synthesis in Pasteurellaceae and Neisseria meningitidis. Res Microbiol 2011; 162:483–487 [View Article][PubMed]
    [Google Scholar]
  52. Wen Z, Zhang JR. Bacterial capsules. In Tang YW, Sussman M, Liu D, Poxton I, Schwartzman J et al. (editors) Molecular Medical Microbiology, 2nd ed. Cambridge, MA: Elsevier; 2015 pp. 33–53
    [Google Scholar]
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