Hierarchical genomic analysis of carried and invasive serogroup A Neisseria meningitidis during the 2011 epidemic in Chad

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Abstract

Background

Serogroup A Neisseria meningitidis ( NmA) was the cause of the 2011 meningitis epidemics in Chad. This bacterium, often carried asymptomatically, is considered to be an “accidental pathogen”; however, the transition from carriage to disease phenotype remains poorly understood. This study examined the role genetic diversity might play in this transition by comparing genomes from geographically and temporally matched invasive and carried NmA isolates.

Results

All 23 NmA isolates belonged to the ST-5 clonal complex (cc5). Ribosomal MLST comparison with other publically available NmA:cc5 showed that isolates were closely related, although those from Chad formed two distinct branches and did not cluster with other NmA, based on their MLST profile, geographical and temporal location. Whole genome MLST (wgMLST) comparison identified 242 variable genes among all Chadian isolates and clustered them into three distinct phylogenetic groups (Clusters 1, 2, and 3): no systematic clustering by disease or carriage source was observed. There was a significant difference ( p = 0.0070) between the mean age of the individuals from which isolates from Cluster 1 and Cluster 2 were obtained, irrespective of whether the person was a case or a carrier.

Conclusions

Whole genome sequencing provided high-resolution characterization of the genetic diversity of these closely related NmA isolates. The invasive meningococcal isolates obtained during the epidemic were not homogeneous; rather, a variety of closely related but distinct clones were circulating in the human population with some clones preferentially colonizing specific age groups, reflecting a potential age-related niche adaptation. Systematic genetic differences were not identified between carriage and disease isolates consistent with invasive meningococcal disease being a multi-factorial event resulting from changes in host-pathogen interactions along with the bacterium.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-017-3789-0) contains supplementary material, which is available to authorized users.

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Most cited references 32

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Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms.

M. C. J. Maiden, J. Bygraves, E Feil … (1998)

Traditional and molecular typing schemes for the characterization of pathogenic microorganisms are poorly portable because they index variation that is difficult to compare among laboratories. To overcome these problems, we propose multilocus sequence typing (MLST), which exploits the unambiguous nature and electronic portability of nucleotide sequence data for the characterization of microorganisms. To evaluate MLST, we determined the sequences of approximately 470-bp fragments from 11 housekeeping genes in a reference set of 107 isolates of Neisseria meningitidis from invasive disease and healthy carriers. For each locus, alleles were assigned arbitrary numbers and dendrograms were constructed from the pairwise differences in multilocus allelic profiles by cluster analysis. The strain associations obtained were consistent with clonal groupings previously determined by multilocus enzyme electrophoresis. A subset of six gene fragments was chosen that retained the resolution and congruence achieved by using all 11 loci. Most isolates from hyper-virulent lineages of serogroups A, B, and C meningococci were identical for all loci or differed from the majority type at only a single locus. MLST using six loci therefore reliably identified the major meningococcal lineages associated with invasive disease. MLST can be applied to almost all bacterial species and other haploid organisms, including those that are difficult to cultivate. The overwhelming advantage of MLST over other molecular typing methods is that sequence data are truly portable between laboratories, permitting one expanding global database per species to be placed on a World-Wide Web site, thus enabling exchange of molecular typing data for global epidemiology via the Internet.

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Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain

Keith Jolley, Carly M. Bliss, Julia S. Bennett … (2012)

No single genealogical reconstruction or typing method currently encompasses all levels of bacterial diversity, from domain to strain. We propose ribosomal multilocus sequence typing (rMLST), an approach which indexes variation of the 53 genes encoding the bacterial ribosome protein subunits (rps genes), as a means of integrating microbial genealogy and typing. As with multilocus sequence typing (MLST), rMLST employs curated reference sequences to identify gene variants efficiently and rapidly. The rps loci are ideal targets for a universal characterization scheme as they are: (i) present in all bacteria; (ii) distributed around the chromosome; and (iii) encode proteins which are under stabilizing selection for functional conservation. Collectively, the rps loci exhibit variation that resolves bacteria into groups at all taxonomic and most typing levels, providing significantly more resolution than 16S small subunit rRNA gene phylogenies. A web-accessible expandable database, comprising whole-genome data from more than 1900 bacterial isolates, including 28 draft genomes assembled de novo from the European Bioinformatics Institute (EBI) sequence read archive, has been assembled. The rps gene variation catalogued in this database permits rapid and computationally non-intensive identification of the phylogenetic position of any bacterial sequence at the domain, phylum, class, order, family, genus, species and strain levels. The groupings generated with rMLST data are consistent with current nomenclature schemes and independent of the clustering algorithm used. This approach is applicable to the other domains of life, potentially providing a rational and universal approach to the classification of life that is based on one of its fundamental features, the translation mechanism.

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Description and Nomenclature of Neisseria meningitidis Capsule Locus

Odile B Harrison, Heike Claus, Ying Jiang … (2013)

Pathogenic Neisseria meningitidis isolates contain a polysaccharide capsule that is the main virulence determinant for this bacterium. Thirteen capsular polysaccharides have been described, and nuclear magnetic resonance spectroscopy has enabled determination of the structure of capsular polysaccharides responsible for serogroup specificity. Molecular mechanisms involved in N. meningitidis capsule biosynthesis have also been identified, and genes involved in this process and in cell surface translocation are clustered at a single chromosomal locus termed cps. The use of multiple names for some of the genes involved in capsule synthesis, combined with the need for rapid diagnosis of serogroups commonly associated with invasive meningococcal disease, prompted a requirement for a consistent approach to the nomenclature of capsule genes. In this report, a comprehensive description of all N. meningitidis serogroups is provided, along with a proposed nomenclature, which was presented at the 2012 XVIIIth International Pathogenic Neisseria Conference.

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Author and article information

Contributors

Kanny Diallo:

ORCID: http://orcid.org/0000-0002-0905-3980

+441 865271205 , kanny.diallo@zoo.ox.ac.uk

Kadija Gamougam: adoumhermann@hotmail.fr

Doumagoum M. Daugla: daugla1.doumagoum@gmail.com

Odile B. Harrison: odile.harrison@zoo.ox.ac.uk

James E. Bray: james.bray@zoo.ox.ac.uk

Dominique A. Caugant: Dominique.Caugant@fhi.no

Jay Lucidarme: Jay.Lucidarme@phe.gov.uk

Caroline L. Trotter: clt56@cam.ac.uk

Musa Hassan-King: mhassanking@hotmail.com

James M. Stuart: James.Stuart@lshtm.ac.uk

Olivier Manigart: Olivier.Manigart@lshtm.ac.uk

Brian M. Greenwood: Brian.Greenwood@lshtm.ac.uk

Martin C. J. Maiden: martin.maiden@zoo.ox.ac.uk

Journal

Journal ID (nlm-ta): BMC Genomics

Journal ID (iso-abbrev): BMC Genomics

Title: BMC Genomics

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2164

Publication date (Electronic): 22 May 2017

Publication date PMC-release: 22 May 2017

Publication date Collection: 2017

Volume: 18

Electronic Location Identifier: 398

Affiliations

[1 ]Centre pour les Vaccins en Développement, Bamako, Mali

[2 ]Centre de Support en Santé International, N’Djamena, Chad

[3 ]ISNI 0000 0004 1936 8948, GRID grid.4991.5, Department of Zoology, , University of Oxford, ; Peter Medawar Building for Pathogen Research, South Parks Road, OX1 3SY Oxford, UK

[4 ]ISNI 0000 0001 1541 4204, GRID grid.418193.6, , Norwegian Institute of Public Health, ; Oslo, Norway

[5 ]ISNI 0000 0001 2196 8713, GRID grid.9004.d, Vaccine Evaluation Unit, , Public Health England, ; Manchester, UK

[6 ]ISNI 0000000121885934, GRID grid.5335.0, Department of Veterinary Medicine, , University of Cambridge, ; Cambridge, UK

[7 ]ISNI 0000 0004 0425 469X, GRID grid.8991.9, , London School of Hygiene & Tropical Medicine, ; London, UK

Author information

Kanny Diallo http://orcid.org/0000-0002-0905-3980

Article

Publisher ID: 3789

DOI: 10.1186/s12864-017-3789-0

PMC ID: 5441073

PubMed ID: 28532434

SO-VID: a2ca6ff2-2ab8-461e-b0e2-56422bb90e80

License:

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 2 November 2016

Date accepted : 12 May 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;

Award ID: 103957/Z/14/Z

Award ID: 087622/Z/08/Z

Award Recipient : Kanny Diallo

Funded by: FundRef http://dx.doi.org/10.13039/100000865, Bill and Melinda Gates Foundation;

Award ID: 51251

Award Recipient : Brian M. Greenwood

Custom metadata

ScienceOpen disciplines: Genetics

Keywords: whole genome sequencing,meningitis epidemic,african meningitis belt,pharyngeal carriage,serogroup a neisseria meningitidis

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ScienceOpen disciplines: Genetics

Keywords: whole genome sequencing, meningitis epidemic, african meningitis belt, pharyngeal carriage, serogroup a neisseria meningitidis

Hierarchical genomic analysis of carried and invasive serogroup A Neisseria meningitidis during the 2011 epidemic in Chad

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Arabidopsis genomics

Most cited references 32

Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms.

Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain

Description and Nomenclature of Neisseria meningitidis Capsule Locus

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