Transcriptomic buffering of cryptic genetic variation contributes to meningococcal virulence

Ampattu BJ, Hagmann L, Liang C, Dittrich M, Schlüter A, Blom J, Krol E, Goesmann A, Becker A, Dandekar T, Mueller T, et al. (2017)
BMC Genomics 18(1): 282.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Ampattu, Biju Joseph; Hagmann, Laura; Liang, Chunguang; Dittrich, Marcus; Schlüter, AndreasUniBi ; Blom, Jochen; Krol, Elizaveta; Goesmann, Alexander; Becker, Anke; Dandekar, Thomas; Mueller, Tobias; Schoen, Christoph
Abstract / Bemerkung
Background: Commensal bacteria like Neisseria meningitidis sometimes cause serious disease. However, genomic comparison of hyperinvasive and apathogenic lineages did not reveal unambiguous hints towards indispensable virulence factors. Here, in a systems biological approach we compared gene expression of the invasive strain MC58 and the carriage strain alpha 522 under different ex vivo conditions mimicking commensal and virulence compartments to assess the strain-specific impact of gene regulation on meningococcal virulence. Results: Despite indistinguishable ex vivo phenotypes, both strains differed in the expression of over 500 genes under infection mimicking conditions. These differences comprised in particular metabolic and information processing genes as well as genes known to be involved in host-damage such as the nitrite reductase and numerous LOS biosynthesis genes. A model based analysis of the transcriptomic differences in human blood suggested ensuing metabolic flux differences in energy, glutamine and cysteine metabolic pathways along with differences in the activation of the stringent response in both strains. In support of the computational findings, experimental analyses revealed differences in cysteine and glutamine auxotrophy in both strains as well as a strain and condition dependent essentiality of the (p) ppGpp synthetase gene relA and of a short non-coding AT-rich repeat element in its promoter region. Conclusions: Our data suggest that meningococcal virulence is linked to transcriptional buffering of cryptic genetic variation in metabolic genes including global stress responses. They further highlight the role of regulatory elements for bacterial virulence and the limitations of model strain approaches when studying such genetically diverse species as N. meningitidis.
Neisseria meningitidis; Virulence; Regulatory evolution; Systems; biology; Metabolism; Cryptic genetic variation; Stringent response; MITE; RelA
BMC Genomics
Page URI


Ampattu BJ, Hagmann L, Liang C, et al. Transcriptomic buffering of cryptic genetic variation contributes to meningococcal virulence. BMC Genomics. 2017;18(1): 282.
Ampattu, B. J., Hagmann, L., Liang, C., Dittrich, M., Schlüter, A., Blom, J., Krol, E., et al. (2017). Transcriptomic buffering of cryptic genetic variation contributes to meningococcal virulence. BMC Genomics, 18(1), 282. doi:10.1186/s12864-017-3616-7
Ampattu, Biju Joseph, Hagmann, Laura, Liang, Chunguang, Dittrich, Marcus, Schlüter, Andreas, Blom, Jochen, Krol, Elizaveta, et al. 2017. “Transcriptomic buffering of cryptic genetic variation contributes to meningococcal virulence”. BMC Genomics 18 (1): 282.
Ampattu, B. J., Hagmann, L., Liang, C., Dittrich, M., Schlüter, A., Blom, J., Krol, E., Goesmann, A., Becker, A., Dandekar, T., et al. (2017). Transcriptomic buffering of cryptic genetic variation contributes to meningococcal virulence. BMC Genomics 18:282.
Ampattu, B.J., et al., 2017. Transcriptomic buffering of cryptic genetic variation contributes to meningococcal virulence. BMC Genomics, 18(1): 282.
B.J. Ampattu, et al., “Transcriptomic buffering of cryptic genetic variation contributes to meningococcal virulence”, BMC Genomics, vol. 18, 2017, : 282.
Ampattu, B.J., Hagmann, L., Liang, C., Dittrich, M., Schlüter, A., Blom, J., Krol, E., Goesmann, A., Becker, A., Dandekar, T., Mueller, T., Schoen, C.: Transcriptomic buffering of cryptic genetic variation contributes to meningococcal virulence. BMC Genomics. 18, : 282 (2017).
Ampattu, Biju Joseph, Hagmann, Laura, Liang, Chunguang, Dittrich, Marcus, Schlüter, Andreas, Blom, Jochen, Krol, Elizaveta, Goesmann, Alexander, Becker, Anke, Dandekar, Thomas, Mueller, Tobias, and Schoen, Christoph. “Transcriptomic buffering of cryptic genetic variation contributes to meningococcal virulence”. BMC Genomics 18.1 (2017): 282.

4 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Neisseria genomics: current status and future perspectives.
Harrison OB, Schoen C, Retchless AC, Wang X, Jolley KA, Bray JE, Maiden MCJ., Pathog Dis 75(6), 2017
PMID: 28591853

125 References

Daten bereitgestellt von Europe PubMed Central.


DA, Vaccine 27(Suppl 2), 2009

WW, Arch Intern Med 23(4), 1919
Epidemic meningitis, meningococcaemia, and Neisseria meningitidis.
Stephens DS, Greenwood B, Brandtzaeg P., Lancet 369(9580), 2007
PMID: 17604802
Bacterial pathogenomics.
Pallen MJ, Wren BW., Nature 449(7164), 2007
PMID: 17943120

S, Rev Infect Dis 10(Suppl 2), 1988

C, Vaccine 27(Suppl 2), 2009
Genome sequencing reveals widespread virulence gene exchange among human Neisseria species.
Marri PR, Paniscus M, Weyand NJ, Rendon MA, Calton CM, Hernandez DR, Higashi DL, Sodergren E, Weinstock GM, Rounsley SD, So M., PLoS ONE 5(7), 2010
PMID: 20676376
Role of selection in the emergence of lineages and the evolution of virulence in Neisseria meningitidis.
Buckee CO, Jolley KA, Recker M, Penman B, Kriz P, Gupta S, Maiden MC., Proc. Natl. Acad. Sci. U.S.A. 105(39), 2008
PMID: 18815379
Metabolism and virulence in Neisseria meningitidis.
Schoen C, Kischkies L, Elias J, Ampattu BJ., Front Cell Infect Microbiol 4(), 2014
PMID: 25191646
Evolution of transcriptional regulatory circuits in bacteria.
Perez JC, Groisman EA., Cell 138(2), 2009
PMID: 19632175
Bacterial regulatory networks are extremely flexible in evolution.
Lozada-Chavez I, Janga SC, Collado-Vides J., Nucleic Acids Res. 34(12), 2006
PMID: 16840530
Evolutionary dynamics of prokaryotic transcriptional regulatory networks.
Madan Babu M, Teichmann SA, Aravind L., J. Mol. Biol. 358(2), 2006
PMID: 16530225
Genomic analysis of a key innovation in an experimental Escherichia coli population.
Blount ZD, Barrick JE, Davidson CJ, Lenski RE., Nature 489(7417), 2012
PMID: 22992527
Transfer of noncoding DNA drives regulatory rewiring in bacteria.
Oren Y, Smith MB, Johns NI, Kaplan Zeevi M, Biran D, Ron EZ, Corander J, Wang HH, Alm EJ, Pupko T., Proc. Natl. Acad. Sci. U.S.A. 111(45), 2014
PMID: 25313052
A single regulatory gene is sufficient to alter bacterial host range.
Mandel MJ, Wollenberg MS, Stabb EV, Visick KL, Ruby EG., Nature 458(7235), 2009
PMID: 19182778
A specific genetic background is required for acquisition and expression of virulence factors in Escherichia coli.
Escobar-Paramo P, Clermont O, Blanc-Potard AB, Bui H, Le Bouguenec C, Denamur E., Mol. Biol. Evol. 21(6), 2004
PMID: 15014151
Indirect and suboptimal control of gene expression is widespread in bacteria.
Price MN, Deutschbauer AM, Skerker JM, Wetmore KM, Ruths T, Mar JS, Kuehl JV, Shao W, Arkin AP., Mol. Syst. Biol. 9(), 2013
PMID: 23591776
Transcriptome analysis of Neisseria meningitidis in human whole blood and mutagenesis studies identify virulence factors involved in blood survival.
Echenique-Rivera H, Muzzi A, Del Tordello E, Seib KL, Francois P, Rappuoli R, Pizza M, Serruto D., PLoS Pathog. 7(5), 2011
PMID: 21589640
Available carbon source influences the resistance of Neisseria meningitidis against complement.
Exley RM, Shaw J, Mowe E, Sun YH, West NP, Williamson M, Botto M, Smith H, Tang CM., J. Exp. Med. 201(10), 2005
PMID: 15897277
A novel phase variation mechanism in the meningococcus driven by a ligand-responsive repressor and differential spacing of distal promoter elements.
Metruccio MM, Pigozzi E, Roncarati D, Berlanda Scorza F, Norais N, Hill SA, Scarlato V, Delany I., PLoS Pathog. 5(12), 2009
PMID: 20041170
Systems genetics approaches to understand complex traits.
Civelek M, Lusis AJ., Nat. Rev. Genet. 15(1), 2013
PMID: 24296534
Genetics of global gene expression.
Rockman MV, Kruglyak L., Nat. Rev. Genet. 7(11), 2006
PMID: 17047685
Neisseria meningitidis is structured in clades associated with restriction modification systems that modulate homologous recombination.
Budroni S, Siena E, Dunning Hotopp JC, Seib KL, Serruto D, Nofroni C, Comanducci M, Riley DR, Daugherty SC, Angiuoli SV, Covacci A, Pizza M, Rappuoli R, Moxon ER, Tettelin H, Medini D., Proc. Natl. Acad. Sci. U.S.A. 108(11), 2011
PMID: 21368196
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, Muller T, Vogel U, Schoen C., PLoS ONE 6(4), 2011
PMID: 21541312
Characterization of a novel Neisseria meningitidis Fur and iron-regulated operon required for protection from oxidative stress: utility of DNA microarray in the assignment of the biological role of hypothetical genes.
Grifantini R, Frigimelica E, Delany I, Bartolini E, Giovinazzi S, Balloni S, Agarwal S, Galli G, Genco C, Grandi G., Mol. Microbiol. 54(4), 2004
PMID: 15522080
Identification of iron-activated and -repressed Fur-dependent genes by transcriptome analysis of Neisseria meningitidis group B.
Grifantini R, Sebastian S, Frigimelica E, Draghi M, Bartolini E, Muzzi A, Rappuoli R, Grandi G, Genco CA., Proc. Natl. Acad. Sci. U.S.A. 100(16), 2003
PMID: 12883001
Analysis of the heat shock response of Neisseria meningitidis with cDNA- and oligonucleotide-based DNA microarrays.
Guckenberger M, Kurz S, Aepinus C, Theiss S, Haller S, Leimbach T, Panzner U, Weber J, Paul H, Unkmeir A, Frosch M, Dietrich G., J. Bacteriol. 184(9), 2002
PMID: 11948171
Role of FNR and FNR-regulated, sugar fermentation genes in Neisseria meningitidis infection.
Bartolini E, Frigimelica E, Giovinazzi S, Galli G, Shaik Y, Genco C, Welsch JA, Granoff DM, Grandi G, Grifantini R., Mol. Microbiol. 60(4), 2006
PMID: 16677307
MisR/MisS two-component regulon in Neisseria meningitidis.
Tzeng YL, Kahler CM, Zhang X, Stephens DS., Infect. Immun. 76(2), 2007
PMID: 18056476
Cryptic genetic variation: evolution's hidden substrate.
Paaby AB, Rockman MV., Nat. Rev. Genet. 15(4), 2014
PMID: 24614309
Expanded microbial genome coverage and improved protein family annotation in the COG database.
Galperin MY, Makarova KS, Wolf YI, Koonin EV., Nucleic Acids Res. 43(Database issue), 2014
PMID: 25428365
A bacterial siren song: intimate interactions between Neisseria and neutrophils.
Criss AK, Seifert HS., Nat. Rev. Microbiol. 10(3), 2012
PMID: 22290508

C, 2006
A functional two-partner secretion system contributes to adhesion of Neisseria meningitidis to epithelial cells.
Schmitt C, Turner D, Boesl M, Abele M, Frosch M, Kurzai O., J. Bacteriol. 189(22), 2007
PMID: 17873034
Neisseria meningitidis NadA is a new invasin which promotes bacterial adhesion to and penetration into human epithelial cells.
Capecchi B, Adu-Bobie J, Di Marcello F, Ciucchi L, Masignani V, Taddei A, Rappuoli R, Pizza M, Arico B., Mol. Microbiol. 55(3), 2005
PMID: 15660996
Biochemical composition of human saliva in relation to other mucosal fluids.
Schenkels LC, Veerman EC, Nieuw Amerongen AV., Crit. Rev. Oral Biol. Med. 6(2), 1995
PMID: 7548622
Underestimation of meningococci in tonsillar tissue by nasopharyngeal swabbing.
Sim RJ, Harrison MM, Moxon ER, Tang CM., Lancet 356(9242), 2000
PMID: 11089827
Biofilm formation by Neisseria meningitidis.
Yi K, Rasmussen AW, Gudlavalleti SK, Stephens DS, Stojiljkovic I., Infect. Immun. 72(10), 2004
PMID: 15385518

M, Cold Spring Harbor Perspect Med 3(4), 2013

BC, Shock (Augusta, Ga) 44(5), 2015
Nitric oxide metabolism in Neisseria meningitidis.
Anjum MF, Stevanin TM, Read RC, Moir JW., J. Bacteriol. 184(11), 2002
PMID: 12003939
Neisseria meningitidis induces platelet inhibition and increases vascular endothelial permeability via nitric oxide regulated pathways.
Kobsar A, Siauw C, Gambaryan S, Hebling S, Speer C, Schubert-Unkmeir A, Eigenthaler M., Thromb. Haemost. 106(6), 2011
PMID: 22072136

TM, Microbes Infection/Institut Pasteur 9(8), 2007
Identifying functional modules in protein-protein interaction networks: an integrated exact approach.
Dittrich MT, Klau GW, Rosenwald A, Dandekar T, Muller T., Bioinformatics 24(13), 2008
PMID: 18586718
STRING v9.1: protein-protein interaction networks, with increased coverage and integration.
Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von Mering C, Jensen LJ., Nucleic Acids Res. 41(Database issue), 2012
PMID: 23203871
Integrated network reconstruction, visualization and analysis using YANAsquare.
Schwarz R, Liang C, Kaleta C, Kuhnel M, Hoffmann E, Kuznetsov S, Hecker M, Griffiths G, Schuster S, Dandekar T., BMC Bioinformatics 8(), 2007
PMID: 17725829
Staphylococcus aureus physiological growth limitations: insights from flux calculations built on proteomics and external metabolite data.
Liang C, Liebeke M, Schwarz R, Zuhlke D, Fuchs S, Menschner L, Engelmann S, Wolz C, Jaglitz S, Bernhardt J, Hecker M, Lalk M, Dandekar T., Proteomics 11(10), 2011
PMID: 21472852

C, 1981
NeMeSys: a biological resource for narrowing the gap between sequence and function in the human pathogen Neisseria meningitidis.
Rusniok C, Vallenet D, Floquet S, Ewles H, Mouze-Soulama C, Brown D, Lajus A, Buchrieser C, Medigue C, Glaser P, Pelicic V., Genome Biol. 10(10), 2009
PMID: 19818133
Nitrogen assimilation in Escherichia coli: putting molecular data into a systems perspective.
van Heeswijk WC, Westerhoff HV, Boogerd FC., Microbiol. Mol. Biol. Rev. 77(4), 2013
PMID: 24296575
The minimal mobile element.
Saunders NJ, Snyder LA., Microbiology (Reading, Engl.) 148(Pt 12), 2002
PMID: 12480877
The repertoire of minimal mobile elements in the Neisseria species and evidence that these are involved in horizontal gene transfer in other bacteria.
Snyder LA, McGowan S, Rogers M, Duro E, O'Farrell E, Saunders NJ., Mol. Biol. Evol. 24(12), 2007
PMID: 17921485

N, FEBS Lett 522(1–3), 2002
A two-component system is required for colonization of host cells by meningococcus.
Jamet A, Rousseau C, Monfort JB, Frapy E, Nassif X, Martin P., Microbiology (Reading, Engl.) 155(Pt 7), 2009
PMID: 19389768
Infection with an avirulent phoP mutant of Neisseria meningitidis confers broad cross-reactive immunity.
Newcombe J, Eales-Reynolds LJ, Wootton L, Gorringe AR, Funnell SG, Taylor SC, McFadden JJ., Infect. Immun. 72(1), 2004
PMID: 14688113
Effect of Neisseria meningitidis fur mutations on global control of gene transcription.
Delany I, Grifantini R, Bartolini E, Rappuoli R, Scarlato V., J. Bacteriol. 188(7), 2006
PMID: 16547035
Ecf, an alternative sigma factor from Neisseria gonorrhoeae, controls expression of msrAB, which encodes methionine sulfoxide reductase.
Gunesekere IC, Kahler CM, Ryan CS, Snyder LA, Saunders NJ, Rood JI, Davies JK., J. Bacteriol. 188(10), 2006
PMID: 16672599
Deep sequencing whole transcriptome exploration of the σE regulon in Neisseria meningitidis.
Huis in 't Veld RA, Willemsen AM, van Kampen AH, Bradley EJ, Baas F, Pannekoek Y, van der Ende A., PLoS ONE 6(12), 2011
PMID: 22194974
Base pairing small RNAs and their roles in global regulatory networks.
Beisel CL, Storz G., FEMS Microbiol. Rev. 34(5), 2010
PMID: 20662934
The RNA chaperone Hfq is involved in stress response and virulence in Neisseria meningitidis and is a pleiotropic regulator of protein expression.
Fantappie L, Metruccio MM, Seib KL, Oriente F, Cartocci E, Ferlicca F, Giuliani MM, Scarlato V, Delany I., Infect. Immun. 77(5), 2009
PMID: 19223479
Transcriptional landscape and essential genes of Neisseria gonorrhoeae.
Remmele CW, Xian Y, Albrecht M, Faulstich M, Fraunholz M, Heinrichs E, Dittrich MT, Muller T, Reinhardt R, Rudel T., Nucleic Acids Res. 42(16), 2014
PMID: 25143534
ppGpp conjures bacterial virulence.
Dalebroux ZD, Svensson SL, Gaynor EC, Swanson MS., Microbiol. Mol. Biol. Rev. 74(2), 2010
PMID: 20508246
The magic spot: a ppGpp binding site on E. coli RNA polymerase responsible for regulation of transcription initiation.
Ross W, Vrentas CE, Sanchez-Vazquez P, Gaal T, Gourse RL., Mol. Cell 50(3), 2013
PMID: 23623682
Impact of small repeat sequences on bacterial genome evolution.
Delihas N., Genome Biol Evol 3(), 2011
PMID: 21803768
Microbial quest for food in vivo: 'nutritional virulence' as an emerging paradigm.
Abu Kwaik Y, Bumann D., Cell. Microbiol. 15(6), 2013
PMID: 23490329
Revisiting the host as a growth medium.
Brown SA, Palmer KL, Whiteley M., Nat. Rev. Microbiol. 6(9), 2008
PMID: 18679171
Recognition of meningococcal molecular patterns by innate immune receptors.
Schmitt C, Villwock A, Kurzai O., Int. J. Med. Microbiol. 299(1), 2008
PMID: 18706860
Defenses against oxidative stress in Neisseria gonorrhoeae: a system tailored for a challenging environment.
Seib KL, Wu HJ, Kidd SP, Apicella MA, Jennings MP, McEwan AG., Microbiol. Mol. Biol. Rev. 70(2), 2006
PMID: 16760307
Modeling Neisseria meningitidis metabolism: from genome to metabolic fluxes.
Baart GJ, Zomer B, de Haan A, van der Pol LA, Beuvery EC, Tramper J, Martens DE., Genome Biol. 8(7), 2007
PMID: 17617894
Glutamate utilization promotes meningococcal survival in vivo through avoidance of the neutrophil oxidative burst.
Tala A, Monaco C, Nagorska K, Exley RM, Corbett A, Zychlinsky A, Alifano P, Tang CM., Mol. Microbiol. 81(5), 2011
PMID: 21777301
Identification of a meningococcal L-glutamate ABC transporter operon essential for growth in low-sodium environments.
Monaco C, Tala A, Spinosa MR, Progida C, De Nitto E, Gaballo A, Bruni CB, Bucci C, Alifano P., Infect. Immun. 74(3), 2006
PMID: 16495545
The damage-response framework of microbial pathogenesis.
Casadevall A, Pirofski LA., Nat. Rev. Microbiol. 1(1), 2003
PMID: 15040176
A genome-scale computational study of the interplay between transcriptional regulation and metabolism.
Shlomi T, Eisenberg Y, Sharan R, Ruppin E., Mol. Syst. Biol. 3(), 2007
PMID: 17437026
Somewhat in control--the role of transcription in regulating microbial metabolic fluxes.
Kochanowski K, Sauer U, Chubukov V., Curr. Opin. Biotechnol. 24(6), 2013
PMID: 23571096
Analysis of the regulated transcriptome of Neisseria meningitidis in human blood using a tiling array.
Del Tordello E, Bottini S, Muzzi A, Serruto D., J. Bacteriol. 194(22), 2012
PMID: 22984255
The effect of immune selection on the structure of the meningococcal opa protein repertoire.
Callaghan MJ, Buckee CO, Jolley KA, Kriz P, Maiden MC, Gupta S., PLoS Pathog. 4(3), 2008
PMID: 18369470
NadA diversity and carriage in Neisseria meningitidis.
Comanducci M, Bambini S, Caugant DA, Mora M, Brunelli B, Capecchi B, Ciucchi L, Rappuoli R, Pizza M., Infect. Immun. 72(7), 2004
PMID: 15213166
Carried meningococci in the Czech Republic: a diverse recombining population.
Jolley KA, Kalmusova J, Feil EJ, Gupta S, Musilek M, Kriz P, Maiden MC., J. Clin. Microbiol. 38(12), 2000
PMID: 11101585
Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms.
Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA, Feavers IM, Achtman M, Spratt BG., Proc. Natl. Acad. Sci. U.S.A. 95(6), 1998
PMID: 9501229
The human oral microbiome.
Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, Lakshmanan A, Wade WG., J. Bacteriol. 192(19), 2010
PMID: 20656903
Comparison and calibration of transcriptome data from RNA-Seq and tiling arrays.
Agarwal A, Koppstein D, Rozowsky J, Sboner A, Habegger L, Hillier LW, Sasidharan R, Reinke V, Waterston RH, Gerstein M., BMC Genomics 11(), 2010
PMID: 20565764
Relacin, a novel antibacterial agent targeting the Stringent Response.
Wexselblatt E, Oppenheimer-Shaanan Y, Kaspy I, London N, Schueler-Furman O, Yavin E, Glaser G, Katzhendler J, Ben-Yehuda S., PLoS Pathog. 8(9), 2012
PMID: 23028324
Genetic analysis of meningococci carried by children and young adults.
Claus H, Maiden MC, Wilson DJ, McCarthy ND, Jolley KA, Urwin R, Hessler F, Frosch M, Vogel U., J. Infect. Dis. 191(8), 2005
PMID: 15776372
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
Meningococcal biofilm formation: structure, development and phenotypes in a standardized continuous flow system.
Lappann M, Haagensen JA, Claus H, Vogel U, Molin S., Mol. Microbiol. 62(5), 2006
PMID: 17121595
Carbohydrate composition of meningococcal lipopolysaccharide modulates the interaction of Neisseria meningitidis with human dendritic cells.
Kurzai O, Schmitt C, Claus H, Vogel U, Frosch M, Kolb-Maurer A., Cell. Microbiol. 7(9), 2005
PMID: 16098219
Complement factor C3 deposition and serum resistance in isogenic capsule and lipooligosaccharide sialic acid mutants of serogroup B Neisseria meningitidis.
Vogel U, Weinberger A, Frank R, Muller A, Kohl J, Atkinson JP, Frosch M., Infect. Immun. 65(10), 1997
PMID: 9317002
Reordering contigs of draft genomes using the Mauve aligner.
Rissman AI, Mau B, Biehl BS, Darling AE, Glasner JD, Perna NT., Bioinformatics 25(16), 2009
PMID: 19515959
GenDB--an open source genome annotation system for prokaryote genomes.
Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J, Kalinowski J, Linke B, Rupp O, Giegerich R, Puhler A., Nucleic Acids Res. 31(8), 2003
PMID: 12682369
Mauve: multiple alignment of conserved genomic sequence with rearrangements.
Darling AC, Mau B, Blattner FR, Perna NT., Genome Res. 14(7), 2004
PMID: 15231754
ACT: the Artemis Comparison Tool.
Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J., Bioinformatics 21(16), 2005
PMID: 15976072
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ., Nucleic Acids Res. 25(17), 1997
PMID: 9254694
CDD: NCBI's conserved domain database.
Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH., Nucleic Acids Res. 43(Database issue), 2014
PMID: 25414356
PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes.
Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, Dao P, Sahinalp SC, Ester M, Foster LJ, Brinkman FS., Bioinformatics 26(13), 2010
PMID: 20472543

TL, Nucleic Acids Res 37(Web Server issu), 2009
EMBOSS: the European Molecular Biology Open Software Suite.
Rice P, Longden I, Bleasby A., Trends Genet. 16(6), 2000
PMID: 10827456
Complete DNA sequence of a serogroup A strain of Neisseria meningitidis Z2491.
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., Nature 404(6777), 2000
PMID: 10761919
Evaluation of one- and two-color gene expression arrays for microbial comparative genome hybridization analyses in routine applications.
Schwarz R, Joseph B, Gerlach G, Schramm-Gluck A, Engelhard K, Frosch M, Muller T, Schoen C., J. Clin. Microbiol. 48(9), 2010
PMID: 20592156


GK, 2005
BioNet: an R-Package for the functional analysis of biological networks.
Beisser D, Klau GW, Dandekar T, Muller T, Dittrich MT., Bioinformatics 26(8), 2010
PMID: 20189939
Comparative genome biology of a serogroup B carriage and disease strain supports a polygenic nature of meningococcal virulence.
Joseph B, Schneiker-Bekel S, Schramm-Gluck A, Blom J, Claus H, Linke B, Schwarz RF, Becker A, Goesmann A, Frosch M, Schoen C., J. Bacteriol. 192(20), 2010
PMID: 20709895

H, Science (New York, NY) 287(5459), 2000
Invasive meningococcal disease: a disease of the endothelial cells.
Coureuil M, Bourdoulous S, Marullo S, Nassif X., Trends Mol Med 20(10), 2014
PMID: 25178566

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

PMID: 28388876
PubMed | Europe PMC

Suchen in

Google Scholar