Differential interaction forces govern bacterial sorting in early biofilms

eLife

Volumn 4, Issue September, 2015, Pages

  Oldewurtel, Enno R ^a   Kouzel, Nadzeya ^a   Dewenter, Lena ^a   Henseler, Katja ^a   Maier, Berenike ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRUCTURES; BACTERIUM PILUS; BIOFILM; CELL BODY; CELL INTERACTION; CELL SELECTION; CELL TRANSFORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA SEQUENCE; FLUORESCENCE MICROSCOPY; IMAGE ANALYSIS; MICROBIAL ADHESION; MORPHOTYPE; NEISSERIA GONORRHOEAE; NONHUMAN; PROTEIN PROCESSING; BACTERIUM ADHERENCE; CELL SURFACE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; ORGANISMAL INTERACTION; PHYSIOLOGY;

BACTERIAL ADHESION; BIOFILMS; CELL SURFACE EXTENSIONS; MICROBIAL INTERACTIONS; NEISSERIA GONORRHOEAE;

EID: 84945936739     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10811     Document Type: Article

References (41)

1. Aas FE, Vik A, Vedde J, Koomey M, Egge-Jacobsen W. 2007. Neisseria gonorrhoeae O-linked pilin glycosylation: functional analyses define both the biosynthetic pathway and glycan structure. Molecular Microbiology 65:607-624. doi: 10.1111/j.1365-2958.2007.05806.x.
2. Anderson MT, Dewenter L, Maier B, Seifert HS. 2014. Seminal plasma initiates a Neisseria gonorrhoeae transmission state. mBio 5:e01004-e01013. doi: 10.1128/mBio.01004-13.
3. Anyan ME, Amiri A, Harvey CW, Tierra G, Morales-Soto N, Driscoll CM, Alber MS, Shrout JD. 2014. Type IV pili interactions promote intercellular association and moderate swarming of Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences of USA 111:18013-18018. doi: 10.1073/pnas.1414661111.
4. Berry JL, Pelicic V. 2015. Exceptionally widespread nanomachines composed of type IV pilins: the prokaryotic Swiss Army knives. FEMS Microbiology Reviews 39:134-154. doi: 10.1093/femsre/fuu001.
5. Brodland GW, Chen HH. 2000. The mechanics of cell sorting and envelopment. Journal of Biomechanics 33(7): 845-851. doi: 10.1016/S0021-9290(00)00011-7.
6. Burton B, Dubnau D. 2010. Membrane-associated DNA transport machines. Cold Spring Harbor Perspectives in Biology 2:a000406. doi: 10.1101/cshperspect.a000406.
7. Cahoon LA, Seifert HS. 2009. An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science 325:764-767. doi: 10.1126/science.1175653.
8. 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, Dumé nil G. 2011. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 331:778-782. doi: 10.1126/science.1200729.
9. Clausen M, Koomey M, Maier B. 2009. Dynamics of type IV pili is controlled by switching between multiple states. Biophysical Journal 96:1169-1177. doi: 10.1016/j.bpj.2008.10.017.
10. Craig L, Pique ME, Tainer JA. 2004. Type IV pilus structure and bacterial pathogenicity. Nature Reviews Microbiology 2:363-378. doi: 10.1038/nrmicro885.
11. Criss AK, Kline KA, Seifert HS. 2005. The frequency and rate of pilin antigenic variation in Neisseria gonorrhoeae. Molecular Microbiology 58:510-519. doi: 10.1111/j.1365-2958.2005.04838.x.
12. Dewenter L, Volkmann TE, Maier B. 2015. Oxygen governs gonococcal microcolony stability by enhancing the interaction force between type IV pili. Integrative Biology 7:1161-1170. doi: 10.1039/c5ib00018a.
13. Fagotto F. 2014. The cellular basis of tissue separation. Development 141:3303-3318. doi: 10.1242/dev.090332.
14. Foty RA, Steinberg MS. 2004. Cadherin-mediated cell-cell adhesion and tissue segregation in relation to malignancy. The International Journal of Developmental Biology 48:397-409. doi: 10.1387/ijdb.041810rf.
15. Freitag NE, Seifert HS, Koomey M. 1995. Characterization of the pilF-pilD pilus-assembly locus of Neisseria gonorrhoeae. Molecular Microbiology 16:575-586. doi: 10.1111/j.1365-2958.1995.tb02420.x.
16. Gonzalez-Rodriguez D, Guevorkian K, Douezan S, Brochard-Wyart F. 2012. Soft matter models of developing tissues and tumors. Science 338:910-917. doi: 10.1126/science.1226418.
17. Graner F, Glazier JA. 1992. Simulation of biological cell sorting using a two-dimensional extended Potts model. Physical Review Letters 69:2013-2016. doi: 10.1103/PhysRevLett.69.2013.
18. Hallatschek O, Hersen P, Ramanathan S, Nelson DR. 2007. Genetic drift at expanding frontiers promotes gene segregation. Proceedings of the National Academy of Sciences of USA 104:19926-19930. doi: 10.1073/pnas.0710150104.
19. Harris AK. 1976. Is cell sorting caused by differences in work of intercellular-adhesion-critique of steinberg hypothesis. Journal of Theoretical Biology 61:267-285. doi: 10.1016/0022-5193(76)90019-9.
20. Hegge FT, Hitchen PG, Aas FE, Kristiansen H, Lovold C, Egge-Jacobsen W, Panico M, Leong WY, Bull V, Virji M, Morris HR, Dell A, Koomey M. 2004. Unique modifications with phosphocholine and phosphoethanolamine define alternate antigenic forms of Neisseria gonorrhoeae type IV pili. Proceedings of the National Academy of Sciences of USA 101:10798-10803. doi: 10.1073/pnas.0402397101.
21. Higashi DL, Zhang GH, Biais N, Myers LR, Weyand NJ, Elliott DA, So M. 2009. Influence of type IV pilus retraction on the architecture of the Neisseria gonorrhoeae-infected cell cortex. Nature Reviews Microbiology 155: 4084-4092. doi: 10.1099/mic.0.032656-0.
22. Holz C, Opitz D, Greune L, Kurre R, Koomey M, Schmidt MA, Maier B. 2010. Multiple pilus motors cooperate for persistent bacterial movement in two dimensions. Physical Review Letters 104:178104. doi: 10.1103/PhysRevLett. 104.178104.
23. Kashef J, Franz CM. 2015. Quantitative methods for analyzing cell-cell adhesion in development. Developmental Biology 401:165-174. doi: 10.1016/j.ydbio.2014.11.002.
24. Kirn TJ, Lafferty MJ, Sandoe CM, Taylor RK. 2000. Delineation of pilin domains required for bacterial association into microcolonies and intestinal colonization by Vibrio cholerae. Molecular Microbiology 35:896-910. doi: 10. 1046/j.1365-2958.2000.01764.x.
25. Klausen M, Aaes-Jorgensen A, Molin S, Tolker-Nielsen T. 2003. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Molecular Microbiology 50:61-68. doi: 10.1046/j.1365-2958.2003.03677.x.
26. Kouzel N, Oldewurtel E, Maier B. 2015. Gene transfer efficiency in gonococcal biofilms: role of biofilm age, and architecture, and pilin antigenic variation. Journal of Bacteriology 197:2422-2431. doi: 10.1128/JB. 00171-15.
27. Landsberg KP, Farhadifar R, Ranft J, Umetsu D, Widmann TJ, Bittig T, Said A, Jülicher F, Dahmann C. 2009. Increased cell bond tension governs cell sorting at the Drosophila anteroposterior compartment boundary. Current Biology 19:1950-1955. doi: 10.1016/j.cub.2009.10.021.
28. Long CD, Hayes SF, van Putten JP, Harvey HA, Apicella MA, Seifert HS. 2001. Modulation of gonococcal piliation by regulatable transcription of pilE. Journal of Bacteriology 183:1600-1609. doi: 10.1128/JB.183.5.1600-1609.2001.
29. Maier B. 2013. The bacterial type IV pilus system-a tunable molecular motor. Soft Matter 9:5667-5671. doi: 10. 1039/c3sm50546d.
30. Maier B, Potter L, So M, Long CD, Seifert HS, Sheetz MP. 2002. Single pilus motor forces exceed 100 pN. Proceedings of the National Academy of Sciences of USA 99:16012-16017. doi: 10.1073/pnas.242523299.
31. Maier B, Wong GC. 2015. How bacteria use type IV pilus machinery on surfaces. Trends in Microbiology. doi: 10. 1016/j.tim.2015.09.002.
32. Mao Y, Baum B. 2015. Tug of war-the influence of opposing physical forces on epithelial cell morphology. Developmental Biology 401:92-102. doi: 10.1016/j.ydbio.2014.12.030.
33. Marathe R, Meel C, Schmidt NC, Dewenter L, Kurre R, Greune L, Schmidt MA, Müller MJ, Lipowsky R, Maier B, Klumpp S. 2014. Bacterial twitching motility is coordinated by a two-dimensional tug-of-war with directional memory. Nature Communications 5:3759. doi: 10.1038/ncomms4759.
34. Marri PR, Paniscus M, Weyand NJ, Rendon 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. doi: 10.1371/journal.pone.0011835.
35. Mehr IJ, Seifert HS. 1997. Random shuttle mutagenesis: gonococcal mutants deficient in pilin antigenic variation. Molecular Microbiology 23:1121-1131. doi: 10.1046/j.1365-2958.1997.2971660.x.
36. Monds RD, O'Toole GA. 2009. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends in Microbiology 17:73-87. doi: 10.1016/j.tim.2008.11.001.
37. Rotman E, Seifert HS. 2014. The genetics of Neisseria species. Annual Review of Genetics 48:405-431. doi: 10. 1146/annurev-genet-120213-092007.
38. Steinberg MS. 1963. Reconstruction of tissues by dissociated cells. Some morphogenetic tissue movements and the sorting out of embryonic cells may have a common explanation. Science 141:401-408. doi: 10.1126/science. 141.3579.401.
39. Steinberg MS, Takeichi M. 1994. Experimental specification of cell sorting, tissue spreading, and specific spatial patterning by quantitative differences in cadherin expression. Proceedings of the National Academy of Sciences of USA 91:206-209. doi: 10.1073/pnas.91.1.206.
40. Wolfgang M, Lauer P, Park HS, Brossay L, Hebert J, Koomey M. 1998. PilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliated Neisseria gonorrhoeae. Molecular Microbiology 29:321-330. doi: 10.1046/j.1365-2958.1998.00935.x.
41. Wolfgang M, van Putten JP, Hayes SF, Dorward D, Koomey M. 2000. Components and dynamics of fiber formation define a ubiquitous biogenesis pathway for bacterial pili. The EMBO Journal 19:6408-6418. doi: 10.1093/emboj/ 19.23.6408.