Virulence Evolution of the Human Pathogen Neisseria meningitidis by Recombination in the Core and Accessory Genome

Joseph B, Schwarz RF, Linke B, Blom J, Becker A, Claus H, Goesmann A, Frosch M, Mueller T, Vogel U, Schoen C (2011)
PLoS ONE 6(4).

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Abstract
Background: Neisseria meningitidis is a naturally transformable, facultative pathogen colonizing the human nasopharynx. Here, we analyze on a genome-wide level the impact of recombination on gene-complement diversity and virulence evolution in N. meningitidis. We combined comparative genome hybridization using microarrays (mCGH) and multilocus sequence typing (MLST) of 29 meningococcal isolates with computational comparison of a subset of seven meningococcal genome sequences. Principal Findings: We found that lateral gene transfer of minimal mobile elements as well as prophages are major forces shaping meningococcal population structure. Extensive gene content comparison revealed novel associations of virulence with genetic elements besides the recently discovered meningococcal disease associated (MDA) island. In particular, we identified an association of virulence with a recently described canonical genomic island termed IHT-E and a differential distribution of genes encoding RTX toxin-and two-partner secretion systems among hyperinvasive and non-hyperinvasive lineages. By computationally screening also the core genome for signs of recombination, we provided evidence that about 40% of the meningococcal core genes are affected by recombination primarily within metabolic genes as well as genes involved in DNA replication and repair. By comparison with the results of previous mCGH studies, our data indicated that genetic structuring as revealed by mCGH is stable over time and highly similar for isolates from different geographic origins. Conclusions: Recombination comprising lateral transfer of entire genes as well as homologous intragenic recombination has a profound impact on meningococcal population structure and genome composition. Our data support the hypothesis that meningococcal virulence is polygenic in nature and that differences in metabolism might contribute to virulence.
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Joseph B, Schwarz RF, Linke B, et al. Virulence Evolution of the Human Pathogen Neisseria meningitidis by Recombination in the Core and Accessory Genome. PLoS ONE. 2011;6(4).
Joseph, B., Schwarz, R. F., Linke, B., Blom, J., Becker, A., Claus, H., Goesmann, A., et al. (2011). Virulence Evolution of the Human Pathogen Neisseria meningitidis by Recombination in the Core and Accessory Genome. PLoS ONE, 6(4).
Joseph, B., Schwarz, R. F., Linke, B., Blom, J., Becker, A., Claus, H., Goesmann, A., Frosch, M., Mueller, T., Vogel, U., et al. (2011). Virulence Evolution of the Human Pathogen Neisseria meningitidis by Recombination in the Core and Accessory Genome. PLoS ONE 6.
Joseph, B., et al., 2011. Virulence Evolution of the Human Pathogen Neisseria meningitidis by Recombination in the Core and Accessory Genome. PLoS ONE, 6(4).
B. Joseph, et al., “Virulence Evolution of the Human Pathogen Neisseria meningitidis by Recombination in the Core and Accessory Genome”, PLoS ONE, vol. 6, 2011.
Joseph, B., Schwarz, R.F., Linke, B., Blom, J., Becker, A., Claus, H., Goesmann, A., Frosch, M., Mueller, T., Vogel, U., Schoen, C.: Virulence Evolution of the Human Pathogen Neisseria meningitidis by Recombination in the Core and Accessory Genome. PLoS ONE. 6, (2011).
Joseph, Biju, Schwarz, Roland F., Linke, Burkhard, Blom, Jochen, Becker, Anke, Claus, Heike, Goesmann, Alexander, Frosch, Matthias, Mueller, Tobias, Vogel, Ulrich, and Schoen, Christoph. “Virulence Evolution of the Human Pathogen Neisseria meningitidis by Recombination in the Core and Accessory Genome”. PLoS ONE 6.4 (2011).
This data publication is cited in the following publications:
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25 Citations in Europe PMC

Data provided by Europe PubMed Central.

How the Knowledge of Interactions between Meningococcus and the Human Immune System Has Been Used to Prepare Effective Neisseria meningitidis Vaccines.
Gasparini R, Panatto D, Bragazzi NL, Lai PL, Bechini A, Levi M, Durando P, Amicizia D., J Immunol Res 2015(), 2015
PMID: 26351643
How clonal are Neisseria species? The epidemic clonality model revisited.
Tibayrenc M, Ayala FJ., Proc. Natl. Acad. Sci. U.S.A. 112(29), 2015
PMID: 26195766
Genomic Analysis of the Evolution and Global Spread of Hyper-invasive Meningococcal Lineage 5.
Harrison OB, Bray JE, Maiden MC, Caugant DA., EBioMedicine 2(3), 2015
PMID: 25984558
Metabolism and virulence in Neisseria meningitidis.
Schoen C, Kischkies L, Elias J, Ampattu BJ., Front Cell Infect Microbiol 4(), 2014
PMID: 25191646
Defining the estimated core genome of bacterial populations using a Bayesian decision model.
van Tonder AJ, Mistry S, Bray JE, Hill DM, Cody AJ, Farmer CL, Klugman KP, von Gottberg A, Bentley SD, Parkhill J, Jolley KA, Maiden MC, Brueggemann AB., PLoS Comput. Biol. 10(8), 2014
PMID: 25144616
Genome comparison of three serovar 5 pathogenic strains of Haemophilus parasuis: insights into an evolving swine pathogen.
Bello-Orti B, Aragon V, Pina-Pedrero S, Bensaid A., Microbiology (Reading, Engl.) 160(Pt 9), 2014
PMID: 24951673
Differential activation of acid sphingomyelinase and ceramide release determines invasiveness of Neisseria meningitidis into brain endothelial cells.
Simonis A, Hebling S, Gulbins E, Schneider-Schaulies S, Schubert-Unkmeir A., PLoS Pathog. 10(6), 2014
PMID: 24945304
Campylobacter ureolyticus: a portrait of the pathogen.
O'Donovan D, Corcoran GD, Lucey B, Sleator RD., Virulence 5(4), 2014
PMID: 24717836
Novel configurations of type I and II CRISPR-Cas systems in Corynebacterium diphtheriae.
Sangal V, Fineran PC, Hoskisson PA., Microbiology (Reading, Engl.) 159(Pt 10), 2013
PMID: 23904149
Homologous recombination drives both sequence diversity and gene content variation in Neisseria meningitidis.
Kong Y, Ma JH, Warren K, Tsang RS, Low DE, Jamieson FB, Alexander DC, Hao W., Genome Biol Evol 5(9), 2013
PMID: 23902748
Description of an unusual Neisseria meningitidis isolate containing and expressing Neisseria gonorrhoeae-Specific 16S rRNA gene sequences.
Walcher M, Skvoretz R, Montgomery-Fullerton M, Jonas V, Brentano S., J. Clin. Microbiol. 51(10), 2013
PMID: 23863567
Constraints on genome dynamics revealed from gene distribution among the Ralstonia solanacearum species.
Lefeuvre P, Cellier G, Remenant B, Chiroleu F, Prior P., PLoS ONE 8(5), 2013
PMID: 23723974
Processing-independent CRISPR RNAs limit natural transformation in Neisseria meningitidis.
Zhang Y, Heidrich N, Ampattu BJ, Gunderson CW, Seifert HS, Schoen C, Vogel J, Sontheimer EJ., Mol. Cell 50(4), 2013
PMID: 23706818
ODoSE: a webserver for genome-wide calculation of adaptive divergence in prokaryotes.
Vos M, te Beek TA, van Driel MA, Huynen MA, Eyre-Walker A, van Passel MW., PLoS ONE 8(5), 2013
PMID: 23671597
Controlling serogroup B invasive meningococcal disease: the Canadian perspective.
Bettinger JA, Deeks SL, Halperin SA, Tsang R, Scheifele DW., Expert Rev Vaccines 12(5), 2013
PMID: 23659299
Attachment and invasion of Neisseria meningitidis to host cells is related to surface hydrophobicity, bacterial cell size and capsule.
Bartley SN, Tzeng YL, Heel K, Lee CW, Mowlaboccus S, Seemann T, Lu W, Lin YH, Ryan CS, Peacock C, Stephens DS, Davies JK, Kahler CM., PLoS ONE 8(2), 2013
PMID: 23405216
Opc expression, LPS immunotype switch and pilin conversion contribute to serum resistance of unencapsulated meningococci.
Hubert K, Pawlik MC, Claus H, Jarva H, Meri S, Vogel U., PLoS ONE 7(9), 2012
PMID: 23028802
Evolutionary and genomic insights into meningococcal biology.
Bratcher HB, Bennett JS, Maiden MC., Future Microbiol 7(7), 2012
PMID: 22827308
Genome characterisation of the genus Francisella reveals insight into similar evolutionary paths in pathogens of mammals and fish.
Sjodin A, Svensson K, Ohrman C, Ahlinder J, Lindgren P, Duodu S, Johansson A, Colquhoun DJ, Larsson P, Forsman M., BMC Genomics 13(), 2012
PMID: 22727144
Whole genome sequencing to investigate the emergence of clonal complex 23 Neisseria meningitidis serogroup Y disease in the United States.
Krauland MG, Dunning Hotopp JC, Riley DR, Daugherty SC, Marsh JW, Messonnier NE, Mayer LW, Tettelin H, Harrison LH., PLoS ONE 7(4), 2012
PMID: 22558202
Evolution of variation in presence and absence of genes in bacterial pathways.
Francis AR, Tanaka MM., BMC Evol. Biol. 12(), 2012
PMID: 22520826

84 References

Data provided by Europe PubMed Central.

A genomic perspective on protein families.
Tatusov RL, Koonin EV, Lipman DJ., Science 278(5338), 1997
PMID: 9381173
RevTrans: Multiple alignment of coding DNA from aligned amino acid sequences.
Wernersson R, Pedersen AG., Nucleic Acids Res. 31(13), 2003
PMID: 12824361
Clonal and variable properties of Neisseria meningitidis isolated from cases and carriers during and after an epidemic in The Gambia, West Africa.
Crowe BA, Wall RA, Kusecek B, Neumann B, Olyhoek T, Abdillahi H, Hassan-King M, Greenwood BM, Poolman JT, Achtman M., J. Infect. Dis. 159(4), 1989
PMID: 2494268
Point mutation in meningococcal por A gene associated with increased endemic disease.
McGuinness BT, Clarke IN, Lambden PR, Barlow AK, Poolman JT, Jones DM, Heckels JE., Lancet 337(8740), 1991
PMID: 1705642

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