Characterization of motility and piliation in pathogenic Neisseria Microbial biochemistry, physiology and metabolism

BMC Microbiology

Volumn 15, Issue 1, 2015, Pages

  Eriksson, Jens ^a   Eriksson, Olaspers Sara ^a   Maudsdotter, Lisa ^a   Palm, Oskar ^b   Engman, Jakob ^a   Sarkissian, Tim ^a   Aro, Helena ^a   Wallin, Mats ^b   Jonsson, Ann Beth ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

Neisseria; PilT; Twitching motility; Type IV pili

Indexed keywords

ARTICLE; BACTERIUM MUTANT; BACTERIUM PILUS; BASE PAIRING; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; IMAGING; NEISSERIA; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; PROMOTER REGION; TRANSMISSION ELECTRON MICROSCOPY; TWITCHING MOTILITY; VELOCITY; CONSERVED SEQUENCE; FIMBRIA; GENETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; SPECIES DIFFERENCE;

BACTERIA (MICROORGANISMS); NEISSERIA; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS;

FIMBRIA PROTEIN;

BASE SEQUENCE; CONSERVED SEQUENCE; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; MUTATION; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; PROMOTER REGIONS, GENETIC; SPECIES SPECIFICITY;

EID: 84938986788     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/s12866-015-0424-6     Document Type: Article

References (43)

1. Nudleman E, Kaiser D. Pulling together with type IV pili. J Mol Microbiol Biotechnol. 2004;7(1-2):52-62. doi:10.1159/000077869.
2. O'Toole GA, Kolter R. Flagellar and twitching motility are necessary for pseudomonas aeruginosa biofilm development. Mol Microbiol. 1998;30(2):295-304.
3. Lang E, Haugen K, Fleckenstein B, Homberset H, Frye SA, Ambur OH, et al. Identification of neisserial DNA binding components. Microbiology. 2009;155(Pt 3):852-62. doi:10.1099/mic.0.022640-0.
4. Howie HL, Glogauer M, So M. The N. gonorrhoeae type IV pilus stimulates mechanosensitive pathways and cytoprotection through a pilT-dependent mechanism. PLoS Biol. 2005;3(4):e100. doi:10.1371/journal.pbio.0030100.
5. Lappann M, Haagensen JA, Claus H, Vogel U, Molin S. Meningococcal biofilm formation: structure, development and phenotypes in a standardized continuous flow system. Mol Microbiol. 2006;62(5):1292-309.
6. Skerker JM, Berg HC. Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci U S A. 2001;98(12):6901-4. doi:10.1073/pnas.121171698.
7. Merz AJ, So M, Sheetz MP. Pilus retraction powers bacterial twitching motility. Nature. 2000;407(6800):98-102. doi:10.1038/35024105.
8. Potts WJ, Saunders JR. Nucleotide sequence of the structural gene for class I pilin from neisseria meningitidis: homologies with the pile locus of neisseria gonorrhoeae. Mol Microbiol. 1988;2(5):647-53.
9. Wormann ME, Horien CL, Bennett JS, Jolley KA, Maiden MC, Tang CM, 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. doi:10.1186/1471-2164-15-253.
10. Craig L, Volkmann N, Arvai AS, Pique ME, Yeager M, Egelman EH. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell. 2006;23(5):651-62.
11. Carbonnelle E, Helaine S, Nassif X, Pelicic V. A systematic genetic analysis in neisseria meningitidis defines the pil proteins required for assembly, functionality, stabilization and export of type IV pili. Mol Microbiol. 2006;61(6):1510-22.
12. Carbonnelle E, Helaine S, Prouvensier L, Nassif X, Pelicic V. Type IV pilus biogenesis in neisseria meningitidis: pilw is involved in a step occurring after pilus assembly, essential for fibre stability and function. Mol Microbiol. 2005;55(1):54-64. doi:10.1111/j.1365-2958.2004.04364.x.
13. Freitag NE, Seifert HS, Koomey M. Characterization of the pilf-pild pilus-assembly locus of neisseria gonorrhoeae. Mol Microbiol. 1995;16(3):575-86.
14. Brossay L, Paradis G, Fox R, Koomey M, Hebert J. Identification, localization, and distribution of the pilt protein in neisseria gonorrhoeae. Infect Immun. 1994;62(6):2302-8.
15. Linden M, Tuohimaa T, Jonsson AB, Wallin M. Force generation in small ensembles of brownian motors. Phys Rev E Stat Nonlin Soft Matter Phys. 2006;74(2 Pt 1):021908.
16. Misic AM, Satyshur KA, Forest KT. P. aeruginosa pilt structures with and without nucleotide reveal a dynamic type IV pilus retraction motor. J Mol Biol. 2010;400(5):1011-21. doi:10.1016/j.jmb.2010.05.066.
17. Satyshur KA, Worzalla GA, Meyer LS, Heiniger EK, Aukema KG, Misic AM, et al. Crystal structures of the pilus retraction motor Pilt suggest large domain movements and subunit cooperation drive motility. Structure. 2007;15(3):363-76. doi:10.1016/j.str.2007.01.018.
18. Shapiro L, McAdams HH, Losick R. Generating and exploiting polarity in bacteria. Science. 2002;298(5600):1942-6. doi:10.1126/science.1072163.
19. Chiang P, Habash M, Burrows LL. Disparate subcellular localization patterns of pseudomonas aeruginosa type IV pilus ATPases involved in twitching motility. J Bacteriol. 2005;187(3):829-39. doi:10.1128/JB.187.3.829-839.2005.
20. Bulyha I, Schmidt C, Lenz P, Jakovljevic V, Hone A, Maier B, et al. Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Mol Microbiol. 2009;74(3):691-706. doi:10.1111/j.1365-2958.2009.06891.x.
21. Kaiser D. Social gliding is correlated with the presence of pili in myxococcus xanthus. Proc Natl Acad Sci U S A. 1979;76(11):5952-6.
22. Marathe R, Meel C, Schmidt NC, Dewenter L, Kurre R, Greune L, et al. Bacterial twitching motility is coordinated by a two-dimensional tug-of-war with directional memory. Nat Commun. 2014;5:3759. doi:10.1038/ncomms4759.
23. Maier B, Potter L, So M, Long CD, Seifert HS, Sheetz MP. Single pilus motor forces exceed 100 pN. Proc Natl Acad Sci U S A. 2002;99(25):16012-7. doi:10.1073/pnas.242523299.
24. Maier B, Koomey M, Sheetz MP. A force-dependent switch reverses type IV pilus retraction. Proc Natl Acad Sci U S A. 2004;101(30):10961-6.
25. Clausen M, Jakovljevic V, Sogaard-Andersen L, Maier B. High-force generation is a conserved property of type IV pilus systems. J Bacteriol. 2009;191(14):4633-8. doi:10.1128/JB.00396-09.
26. Clausen M, Koomey M, Maier B. Dynamics of type IV pili is controlled by switching between multiple states. Biophys J. 2009;96(3):1169-77.
27. Kurre R, Maier B. Oxygen depletion triggers switching between discrete speed modes of gonococcal type IV pili. Biophys J. 2012;102(11):2556-63. doi:10.1016/j.bpj.2012.04.020.
28. Kurre R, Hone A, Clausen M, Meel C, Maier B. PilT2 enhances the speed of gonococcal type IV pilus retraction and of twitching motility. Mol Microbiol. 2012;86(4):857-65. doi:10.1111/mmi.12022.
29. Holz C, Opitz D, Greune L, Kurre R, Koomey M, Schmidt MA, et al. Multiple pilus motors cooperate for persistent bacterial movement in two dimensions. Phys Rev Lett. 2010;104(17):178104.
30. Jonsson AB, Ilver D, Falk P, Pepose J, Normark S. Sequence changes in the pilus subunit lead to tropism variation of neisseria gonorrhoeae to human tissue. Mol Microbiol. 1994;13(3):403-16.
31. Lin YH, Ryan CS, Davies JK. Neisserial Correia repeat-enclosed elements do not influence the transcription of pil genes in neisseria gonorrhoeae and neisseria meningitidis. J Bacteriol. 2011;193(20):5728-36. doi:10.1128/JB.05526-11.
32. Craig L, Volkmann N, Arvai AS, Pique ME, Yeager M, Egelman EH, et al. Type IV pilus structure by cryo-electron microscopy and crystallography: implications for pilus assembly and functions. Mol Cell. 2006;23(5):651-62. doi:10.1016/j.molcel.2006.07.004.
33. Marceau M, Beretti JL, Nassif X. High adhesiveness of encapsulated Neisseria meningitidis to epithelial cells is associated with the formation of bundles of pili. Mol Microbiol. 1995;17(5):855-63.
34. Long CD, Hayes SF, van Putten JP, Harvey HA, Apicella MA, Seifert HS. Modulation of gonococcal piliation by regulatable transcription of pile. J Bacteriol. 2001;183(5):1600-9. doi:10.1128/JB.183.5.1600-1609.2001.
35. Biais N, Ladoux B, Higashi D, So M, Sheetz M. Cooperative retraction of bundled type IV pili enables nanonewton force generation. PLoS Biol. 2008;6(4), e87. doi:10.1371/journal.pbio.0060087.
36. Davies BJ, de Vries N, Rijpkema SG, van Vliet AH, Penn CW. Transcriptional and mutational analysis of the Helicobacter pylori urease promoter. FEMS Microbiol Lett. 2002;213(1):27-32. doi: http://dx.doi.org/10.1111/j.1574-6968.2002.tb11281.x.
37. Wolfgang M, Lauer P, Park HS, Brossay L, Hebert J, Koomey M. PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated neisseria gonorrhoeae. Mol Microbiol. 1998;29(1):321-30.
38. Rahman M, Kallstrom H, Normark S, Jonsson AB. Pilc of pathogenic neisseria is associated with the bacterial cell surface. Mol Microbiol. 1997;25(1):11-25.
39. Virji M, Alexandrescu C, Ferguson DJ, Saunders JR, Moxon ER. Variations in the expression of pili: the effect on adherence of neisseria meningitidis to human epithelial and endothelial cells. Mol Microbiol. 1992;6(10):1271-9.
40. Jonsson AB, Pfeifer J, Normark S. Neisseria gonorrhoeae Pil expression provides a selective mechanism for structural diversity of pili. Proc Natl Acad Sci U S A. 1992;89(8):3204-8.
41. Jones A, Georg M, Maudsdotter L, Jonsson AB. Endotoxin, capsule, and bacterial attachment contribute to neisseria meningitidis resistance to the human antimicrobial peptide LL-37. J Bacteriol. 2009;191(12):3861-8. doi:10.1128/JB.01313-08.
42. Kuwae A, Sjolinder H, Eriksson J, Eriksson S, Chen Y, Jonsson AB. NafA negatively controls Neisseria meningitidis piliation. PLoS One. 2011;6(7), e21749. doi:10.1371/journal.pone.0021749.
43. Lee SW, Higashi DL, Snyder A, Merz AJ, Potter L, So M. PilT is required for PI(3,4,5)P3-mediated crosstalk between neisseria gonorrhoeae and epithelial cells. Cell Microbiol. 2005;7(9):1271-84. doi:10.1111/j.1462-5822.2005.00551.x.