Emergence of a new epidemic neisseria meningitidis serogroup a clone in the African meningitis belt: High-resolution picture of genomic changes that mediate immune evasion

mBio

Volumn 5, Issue 5, 2014, Pages

  Lamelas, Araceli ^a,b   Harris, Simon R ^c   Röltgen, Katharina ^a,b   Dangy, Jean Pierre ^a,b   Hauser, Julia ^a,b   Kingsley, Robert A ^c   Connor, Thomas R ^c   Sie, Ali ^d   Hodgson, Abraham ^e   Dougan, Gordon ^c   Parkhill, Julian ^c   Bentley, Stephen D ^c,f   Pluschke, Gerd ^a,b  

^a SWISS TROPICAL AND PUBLIC HEALTH INSTITUTE   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d Center de Recherche en Sante de Nouna   (Burkina Faso)

^e NAVRONGO HEALTH RESEARCH CENTRE   (Ghana)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL ANTIGEN; MAF3 PROTEIN; MENINGOCOCCUS VACCINE; UNCLASSIFIED DRUG;

ANTIBODY RESPONSE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL MENINGITIS; BACTERIUM ISOLATE; BACTERIUM PILUS; COMPARATIVE GENOMIC HYBRIDIZATION; EPIDEMIC; EPIDEMIC MENINGITIS; GENE LOCUS; HERD IMMUNITY; HOMOLOGOUS RECOMBINATION; HOST PATHOGEN INTERACTION; HUMAN; IMMUNE EVASION; MOLECULAR CLONING; MULTILOCUS SEQUENCE TYPING; NEISSERIA MENINGITIDIS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYLOGEOGRAPHY; POINT MUTATION; POPULATION STRUCTURE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN SYNTHESIS; SEQUENCE ALIGNMENT; SEROTYPE; SINGLE NUCLEOTIDE POLYMORPHISM; AFRICA; BACTERIAL GENOME; CLASSIFICATION; DNA SEQUENCE; GENETICS; GENOTYPE; HORIZONTAL GENE TRANSFER; IMMUNOLOGY; ISOLATION AND PURIFICATION; MENINGITIS, MENINGOCOCCAL; SEQUENCE HOMOLOGY;

NEISSERIA MENINGITIDIS SEROGROUP A;

AFRICA; ANTIGENS, BACTERIAL; DISEASE OUTBREAKS; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; GENOTYPE; HOMOLOGOUS RECOMBINATION; HUMANS; IMMUNE EVASION; MENINGITIS, MENINGOCOCCAL; NEISSERIA MENINGITIDIS, SEROGROUP A; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY;

EID: 84908406609     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01974-14     Document Type: Article

References (55)

1. Greenwood B. 1999. Manson lecture. Meningococcal meningitis in Africa. Trans. R. Soc. Trop. Med. Hyg. 93:341-353. http://dx.doi.org/ 10.1016/S0035-9203(99)90106-2.
2. Teyssou R, Muros-Le Rouzic E. 2007. Meningitis epidemics in Africa: a brief overview. Vaccine 25(Suppl 1):A3-A7. http://dx.doi.org/10.1016/ j.vaccine.2007.04.032.
3. Achtman M. 1994. Clonal spread of serogroup A meningococci: a paradigm for the analysis of microevolution in bacteria. Mol. Microbiol. 11: 15-22. http://dx.doi.org/10.1111/j.1365-2958.1994.tb00285.x.
4. Caugant DA. 2008. Genetics and evolution of Neisseria meningitidis: importance for the epidemiology of meningococcal disease. Infect. Genet. Evol. 8:558-565. http://dx.doi.org/10.1016/j.meegid.2008.04.002.
5. Kristiansen PA, Diomandé F, Ba AK, Sanou I, Ouédraogo AS, Ouédraogo R, Sangaré L, Kandolo D, Aké F, Saga IM, Clark TA, Misegades L, Martin SW, Thomas JD, Tiendrebeogo SR, Hassan-King M, Djingarey MH, Messonnier NE, Préziosi MP, Laforce FM, Caugant DA. 2013. Impact of the serogroup A meningococcal conjugate vaccine, MenAfriVac, on carriage and herd immunity. Clin. Infect. Dis. 56: 354-363. http://dx.doi.org/10.1093/cid/cis892.
6. Ouangraoua S, Schlumberger M, Yaro S, Ouédraogo AS, Sanou S, Drabo A, Yaméogo TM, Ouedraogo R. 3 January 2014. Impact of a conjugated antimeningococcal A vaccine on notification of bacterial meningitis in West Burkina Faso (2009-2012). Bull. Soc. Pathol. Exot. http:// dx.doi.org/10.1007/s13149-014-0329-2. (In French.)
7. Daugla DM, Gami JP, Gamougam K, Naibei N, Mbainadji L, Narbé M, Toralta J, Kodbesse B, Ngadoua C, Coldiron ME, Fermon F, Page AL, Djingarey MH, Hugonnet S, Harrison OB, Rebbetts LS, Tekletsion Y, Watkins ER, Hill D, Caugant DA, Chandramohan D, Hassan-King M, Manigart O, Nascimento M, Woukeu A, Trotter C, Stuart JM, Maiden MC, Greenwood BM. 2014. Effect of a serogroup A meningococcal conjugate vaccine (PsA-TT) on serogroup A meningococcal meningitis and carriage in Chad: a community study [corrected]. Lancet 383:40-47. http://dx.doi.org/10.1016/S0140-6736(14)60303-2.
8. Leimkugel J, Forgor AA, Dangy JP, Pflüger V, Gagneux S, Hodgson A, Pluschke G. 2007. Genetic diversification of Neisseria meningitidis during waves of colonization and disease in the meningitis belt of sub-Saharan Africa. Vaccine 25(Suppl 1):A18 -A23. http://dx.doi.org/10.1016/ j.vaccine.2007.04.035.
9. Caugant DA, Maiden MC. 2009. Meningococcal carriage and disease- population biology and evolution. Vaccine 27(Suppl 2):B64 -B70. http:// dx.doi.org/10.1016/j.vaccine.2009.04.061.
10. Nicolas P, Décousset L, Riglet V, Castelli P, Stor R, Blanchet G. 2001. Clonal expansion of sequence type (ST-)5 and emergence of ST-7 in serogroup A meningococci, Africa. Emerg. Infect. Dis. 7:849-854. http:// dx.doi.org/10.3201/eid0705.010513.
11. Caugant DA, Nicolas P. 2007. Molecular surveillance of meningococcal meningitis in Africa. Vaccine 25(Suppl 1):A8 -A11. http://dx.doi.org/ 10.1016/j.vaccine.2007.04.033.
12. Kong Y, Ma JH, Warren K, Tsang RSW, Low DE, Jamieson FB, Alexander DC, Hao W. 2013. Homologous recombination drives both sequence diversity and gene content variation in Neisseria meningitidis. Genome Biol. Evol. 5:1611-1627. http://dx.doi.org/10.1093/gbe/evt116.
13. Perrin A, Bonacorsi S, Carbonnelle E, Talibi D, Dessen P, Nassif X, Tinsley C. 2002. Comparative genomics identifies the genetic islands that distinguish Neisseria meningitidis, the agent of cerebrospinal meningitis, from other Neisseria species. Infect. Immun. 70:7063-7072. http:// dx.doi.org/10.1128/IAI.70.12.7063-7072.2002.
14. Caugant DA, Kristiansen PA, Wang X, Mayer LW, Taha MK, Ouédraogo R, Kandolo D, Bougoudogo F, Sow S, Bonte L. 2012. Molecular characterization of invasive meningococcal isolates from countries in the African meningitis belt before introduction of a serogroup A conjugate vaccine. PLoS One 7:e46019. http://dx.doi.org/10.1371/ journal.pone.0046019.
15. Leimkugel J, Hodgson A, Forgor AA, Pflüger V, Dangy JP, Smith T, Achtman M, Gagneux S, Pluschke G. 2007. Clonal waves of Neisseria colonisation and disease in the African meningitis belt: eight-year longitudinal study in northern Ghana. PLoS Med. 4:e101. http://dx.doi.org/ 10.1371/journal.pmed.0040101.
16. Sié A, Pflüger V, Coulibaly B, Dangy JP, Kapaun A, Junghanss T, Pluschke G, Leimkugel J. 2008. ST2859 serogroup A meningococcal meningitis outbreak in Nouna Health District, Burkina Faso: a prospective study. Trop. Med. Int. Health 13:861-868. http://dx.doi.org/10.1111/ j.1365-3156.2008.02056.x.
17. Schoen C, Weber-Lehmann J, Blom J, Joseph B, Goesmann A, Strittmatter A, Frosch M. 2011. Whole-genome sequence of the transformable Neisseria meningitidis serogroup A strain WUE2594. J. Bacteriol. 193: 2064-2065. http://dx.doi.org/10.1128/JB.00084-11.
18. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J, van der Linden M, McGee L, von Gottberg A, Song JH, Ko KS, Pichon B, Baker S, Parry CM, Lambertsen LM, Shahinas D, Pillai DR, Mitchell TJ, Dougan G, Tomasz A, Klugman KP, Parkhill J, Hanage WP, Bentley SD. 2011. Rapid pneumococcal evolution in response to clinical interventions. Science 331:430-434. http://dx.doi.org/10.1126/science.1198545.
19. Harris SR, Feil EJ, Holden MT, Quail MA, Nickerson EK, Chantratita N, Gardete S, Tavares A, Day N, Lindsay JA, Edgeworth JD, de Lencastre H, Parkhill J, Peacock SJ, Bentley SD. 2010. Evolution of MRSA during hospital transmission and intercontinental spread. Science 327: 469-474. http://dx.doi.org/10.1126/science.1182395.
20. Okoro CK, Kingsley RA, Connor TR, Harris SR, Parry CM, Al- Mashhadani MN, Kariuki S, Msefula CL, Gordon MA, de Pinna E, Wain J, Heyderman RS, Obaro S, Alonso PL, Mandomando I, MacLennan CA, Tapia MD, Levine MM, Tennant SM, Parkhill J, Dougan G. 2012. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat. Genet. 44:1215-1221. http://dx.doi.org/10.1038/ng.2423.
21. Morelli G, Song Y, Mazzoni CJ, Eppinger M, Roumagnac P, Wagner DM, Feldkamp M, Kusecek B, Vogler AJ, Li Y, Cui Y, Thomson NR, Jombart T, Leblois R, Lichtner P, Rahalison L, Petersen JM, Balloux F, Keim P, Wirth T, Ravel J, Yang R, Carniel E, Achtman M. 2010. Yersinia pestis genome sequencing identifies patterns of global phylogenetic diversity. Nat. Genet. 42:1140-1143. http://dx.doi.org/10.1038/ng.705.
22. Castillo-Ramírez S, Harris SR, Holden MT, He M, Parkhill J, Bentley SD, Feil EJ. 2011. The impact of recombination on dN/dS within recently emerged bacterial clones. PLoS Pathog. 7:e1002129. http://dx.doi.org/ 10.1371/journal.ppat.1002129.
23. Parkhill J, Achtman M, James KD, Bentley SD, Churcher C, Klee SR, Morelli G, Basham D, Brown D, Chillingworth T, Davies RM, Davis P, Devlin K, Feltwell T, Hamlin N, Holroyd S, Jagels K, Leather S, Moule S, Mungall K, Quail MA, Rajandream MA, Rutherford KM, Simmonds M, Skelton J, Whitehead S, Spratt BG, Barrell BG. 2000. Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491. Nature 404:502-506. http://dx.doi.org/10.1038/35006655.
24. Hey J. 2004. What's so hot about recombination hotspots? PLoS Biol. 2:e190. http://dx.doi.org/10.1371/journal.pbio.0020190.
25. Børud B, Aas FE, Vik A, Winther-Larsen HC, Egge-Jacobsen W, Koomey M. 2010. Genetic, structural, and antigenic analyses of glycan diversity in the O-linked protein glycosylation systems of human Neisseria species. J. Bacteriol. 192:2816-2829. http://dx.doi.org/10.1128/JB.00101 -10.
26. Chattopadhyay S, Weissman SJ, Minin VN, Russo TA, Dykhuizen DE, Sokurenko EV. 2009. High frequency of hotspot mutations in core genes of Escherichia coli due to short-term positive selection. Proc. Natl. Acad. Sci. U. S. A. 106:12412-12417. http://dx.doi.org/10.1073/ pnas.0906217106.
27. Harrison OB, Claus H, Jiang Y, Bennett JS, Bratcher HB, Jolley KA, Corton C, Care R, Poolman JT, Zollinger WD, Frasch CE, Stephens DS, Feavers I, Frosch M, Parkhill J, Vogel U, Quail MA, Bentley SD, Maiden MC. 2013. Description and nomenclature of Neisseria meningitidis capsule locus. Emerg. Infect. Dis. 19:566 -573. http://dx.doi.org/10.3201/ eid1904.111799.
28. Zhu P, van der Ende A, Falush D, Brieske N, Morelli G, Linz B, Popovic T, Schuurman IG, Adegbola RA, Zurth K, Gagneux S, Platonov AE, Riou JY, Caugant DA, Nicolas P, Achtman M. 2001. Fit genotypes and escape variants of subgroup III Neisseria meningitidis during three pandemics of epidemic meningitis. Proc. Natl. Acad. Sci. U. S. A. 98: 5234-5239. http://dx.doi.org/10.1073/pnas.061386098.
29. Maiden MC. 2008. Population genomics: diversity and virulence in the Neisseria. Curr. Opin. Microbiol. 11:467-471. http://dx.doi.org/10.1016/ j.mib.2008.09.002.
30. Børud B, Viburiene R, Hartley MD, Paulsen BS, Egge-Jacobsen W, Imperiali B, Koomey M. 2011. Genetic and molecular analyses reveal an evolutionary trajectory for glycan synthesis in a bacterial protein glycosylation system. Proc. Natl. Acad. Sci. U. S. A. 108:9643-9648. http:// dx.doi.org/10.1073/pnas.1103321108.
31. Marceau M, Nassif X. 1999. Role of glycosylation at Ser63 in production of soluble pilin in pathogenic Neisseria. J. Bacteriol. 181:656-661.
32. Kahler CM. 2011. Sticky and sweet: the role of post-translational modifications on neisserial pili. Front. Microbiol. 2:87. http://dx.doi.org/ 10.3389/fmicb.2011.00087.
33. Chamot-Rooke J, Mikaty G, Malosse C, Soyer M, Dumont A, Gault J, Imhaus AF, Martin P, Trellet M, Clary G, Chafey P, Camoin L, Nilges M, Nassif X, Duménil G. 2011. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 331: 778-782. http://dx.doi.org/10.1126/science.1200729.
34. Anonsen JH, Vik Å, Egge-Jacobsen W, Koomey M. 2012. An extended spectrum of target proteins and modification sites in the general O-linked protein glycosylation system in Neisseria gonorrhoeae. J. Proteome Res. 11:5781-5793. http://dx.doi.org/10.1021/pr300584x.
35. Wolfgang M, Park HS, Hayes SF, van Putten JP, Koomey M. 1998. Suppression of an absolute defect in type IV pilus biogenesis by loss-offunction mutations in pilT, a twitching motility gene in Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. U. S. A. 95:14973-14978. http://dx.doi.org/ 10.1073/pnas.95.25.14973.
36. Aas FE, Wolfgang M, Frye S, Dunham S, Løvold C, Koomey M. 2002. Competence for natural transformation in Neisseria gonorrhoeae: components of DNA binding and uptake linked to type IV pilus expression. Mol. Microbiol. 46:749 -760. http://dx.doi.org/10.1046/j.1365 -2958.2002.03193.x.
37. Eriksson J, Eriksson OS, Jonsson AB. 2012. Loss of meningococcal PilU delays microcolony formation and attenuates virulence in vivo. Infect. Immun. 80:2538-2547. http://dx.doi.org/10.1128/IAI.06354-11.
38. Echenique-Rivera H, Muzzi A, Del Tordello E, Seib KL, Francois P, Rappuoli R, Pizza M, Serruto D. 2011. Transcriptome analysis of Neisseria meningitidis in human whole blood and mutagenesis studies identify virulence factors involved in blood survival. PLoS Pathog. 7:e1002027. http://dx.doi.org/10.1371/journal.ppat.1002027.
39. Willis LM, Whitfield C. 2013. Structure, biosynthesis, and function of bacterial capsular polysaccharides synthesized by ABC transporterdependent pathways. Carbohydr. Res. 378:35- 44. http://dx.doi.org/ 10.1016/j.carres.2013.05.007.
40. Stephens DS, McGee ZA. 1983. Association of virulence of Neisseria meningitidis with transparent colony type and low-molecular-weight outer membrane proteins. J. Infect. Dis. 147:282-292. http://dx.doi.org/ 10.1093/infdis/147.2.282.
41. Virji M, Makepeace K, Ferguson DJ, Achtman M, Sarkari J, Moxon ER. 1992. Expression of the Opc protein correlates with invasion of epithelial and endothelial cells by Neisseria meningitidis. Mol. Microbiol. 6:2785-2795. http://dx.doi.org/10.1111/j.1365-2958.1992.tb01458.x.
42. Gudlavalleti SK, Datta AK, Tzeng YL, Noble C, Carlson RW, Stephens DS. 2004. The Neisseria meningitidis serogroup A capsular polysaccharide O-3 and O-4 acetyltransferase. J. Biol. Chem. 279:42765-42773. http:// dx.doi.org/10.1074/jbc.M313552200.
43. Lappann M, Vogel U. 2010. Biofilm formation by the human pathogen Neisseria meningitidis. Med. Microbiol. Immunol. 199:173-183. http:// dx.doi.org/10.1007/s00430-010-0149-y.
44. Katz LS, Sharma NV, Harcourt BH, Thomas JD, Wang X, Mayer LW, Jordan IK. 2011. Using single-nucleotide polymorphisms to discriminate disease-associated from carried genomes of Neisseria meningitidis. J. Bacteriol. 193:3633-3641. http://dx.doi.org/10.1128/JB.01198-10.
45. Marri PR, Paniscus M, Weyand NJ, Rendón MA, Calton CM, Hernández DR, Higashi DL, Sodergren E, Weinstock GM, Rounsley SD, So M. 2010. Genome sequencing reveals widespread virulence gene exchange among human Neisseria species. PLoS One 5:e11835. http://dx.doi.org/ 10.1371/journal.pone.0011835.
46. Seifert HS, Ajioka RS, Paruchuri D, Heffron F, So M. 1990. Shuttle mutagenesis of Neisseria gonorrhoeae: pilin null mutations lower DNA transformation competence. J. Bacteriol. 172:40-46.
47. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078 -2079. http://dx.doi.org/10.1093/bioinformatics/ btp352.
48. Holt KE, Parkhill J, Mazzoni CJ, Roumagnac P, Weill FX, Goodhead I, Rance R, Baker S, Maskell DJ, Wain J, Dolecek C, Achtman M, Dougan G. 2008. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat. Genet. 40:987-993. http://dx.doi.org/10.1038/ng.195.
49. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13:555-556.
50. Zerbino DR, Birney E. 2008. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 18:821- 829. http:// dx.doi.org/10.1101/gr.074492.107.
51. Assefa S, Keane TM, Otto TD, Newbold C, Berriman M. 2009. ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 25:1968 -1969. http://dx.doi.org/10.1093/bioinformatics/ btp347.
52. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. 2005. ACT: the Artemis comparison tool. Bioinformatics 21: 3422-3423. http://dx.doi.org/10.1093/bioinformatics/bti553.
53. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. http://dx.doi.org/10.1093/bioinformatics/btl446.
54. Fall S, Mercier A, Bertolla F, Calteau A, Gueguen L, Perrière G, Vogel TM, Simonet P. 2007. Horizontal gene transfer regulation in bacteria as a "spandrel" of DNA repair mechanisms. PLoS One 2:e1055. http:// dx.doi.org/10.1371/journal.pone.0001055.
55. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7:214. http://dx.doi.org/10.1186/ 1471-2148-7-214.