Motility Enhancement through Surface Modification Is Sufficient for Cyanobacterial Community Organization during Phototaxis

PLoS Computational Biology

Volumn 9, Issue 9, 2013, Pages

  Ursell, Tristan ^a   Chau, Rosanna Man Wah ^a,b   Wisen, Susanne ^b   Bhaya, Devaki ^b   Huang, Kerwyn Casey ^a,c  

^a Stanford University   (United States)

^b STANFORD UNIVERSITY   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY;

CELL-CELL COMMUNICATIONS; COMMUNITY ORGANIZATIONS; CYANOBACTERIUM SYNECHOCYSTIS; EMERGENT BEHAVIOURS; INDIVIDUAL CELLS; SINGLE CELLS; SPATIAL ORGANIZATION; SURFACE-BASED; SURFACE-MODIFICATION; SYNECHOCYSTIS SP;

SURFACE TREATMENT;

ARTICLE; BACTERIAL GROWTH; BIOMASS; CELL FUNCTION; CELL INTERACTION; CELLULAR SECRETION; DEGRADATION; LIGHT; MICROBIAL COMMUNITY; MICROBIAL MORPHOLOGY; NONHUMAN; PHOTOTAXIS; QUANTITATIVE ANALYSIS; SYNECHOCYSTIS; TIME-LAPSE VIDEO MICROSCOPY;

CYANOBACTERIA; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

BIOPHYSICS; SURFACE PROPERTIES; SYNECHOCYSTIS;

EID: 84884694120     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003205     Document Type: Article

References (62)

1. Kamruzzaman M, Udden SM, Cameron DE, Calderwood SB, Nair GB, et al. (2010) Quorum-regulated biofilms enhance the development of conditionally viable, environmental Vibrio cholerae. Proc Natl Acad Sci U S A 107: 1588-1593.
2. Ryan RP, Dow JM, (2008) Diffusible signals and interspecies communication in bacteria. Microbiology 154: 1845-1858.
3. Stoodley P, Sauer K, Davies DG, Costerton JW, (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56: 187-209.
4. Ley RE, Harris JK, Wilcox J, Spear JR, Miller SR, et al. (2006) Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl Environ Microbiol 72: 3685-3695.
5. Bhaya D, Grossman AR, Steunou AS, Khuri N, Cohan FM, et al. (2007) Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses. ISME J 1: 703-713.
6. Klatt CG, Wood JM, Rusch DB, Bateson MM, Hamamura N, et al. (2011) Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential. ISME J 5: 1262-1278.
7. Allen EE, Banfield JF, (2005) Community genomics in microbial ecology and evolution. Nat Rev Microbiol 3: 489-498.
8. Denef VJ, Mueller RS, Banfield JF, (2010) AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J 4: 599-610.
9. Nemergut DR, Costello EK, Hamady M, Lozupone C, Jiang L, et al. (2011) Global patterns in the biogeography of bacterial taxa. Environ Microbiol 13: 135-144.
10. Werner JJ, Knights D, Garcia ML, Scalfone NB, Smith S, et al. (2011) Bacterial community structures are unique and resilient in full-scale bioenergy systems. Proc Natl Acad Sci U S A 108: 4158-4163.
11. Gieseke A, Purkhold U, Wagner M, Amann R, Schramm A, (2001) Community structure and activity dynamics of nitrifying bacteria in a phosphate-removing biofilm. Appl Environ Microbiol 67: 1351-1362.
12. Hansen SK, Rainey PB, Haagensen JA, Molin S, (2007) Evolution of species interactions in a biofilm community. Nature 445: 533-536.
13. Sutherland IW, (2001) The biofilm matrix-an immobilized but dynamic microbial environment. Trends Microbiol 9: 222-227.
14. Paerl HW, Pinckney JL, (1996) A Mini-review of Microbial Consortia: Their Roles in Aquatic Production and Biogeochemical Cycling. Microb Ecol 31: 225-247.
15. Ward DM, Ferris MJ, Nold SC, Bateson MM, (1998) A natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiol Mol Biol Rev 62: 1353-1370.
16. Seminara A, Angelini TE, Wilking JN, Vlamakis H, Ebrahim S, et al. (2012) Osmotic spreading of Bacillus subtilis biofilms driven by an extracellular matrix. Proc Natl Acad Sci U S A 109: 1116-1121.
17. Caldara M, Friedlander RS, Kavanaugh NL, Aizenberg J, Foster KR, et al. (2012) Mucin biopolymers prevent bacterial aggregation by retaining cells in the free-swimming state. Curr Biol 22: 2325-2330.
18. Mitri S, Xavier JB, Foster KR, (2011) Social evolution in multispecies biofilms. Proc Natl Acad Sci U S A 108 Suppl 2: 10839-10846.
19. Mignot T, Kirby JR, (2008) Genetic circuitry controlling motility behaviors of Myxococcus xanthus. Bioessays 30: 733-743.
20. Zhang Y, Ducret A, Shaevitz J, Mignot T, (2012) From individual cell motility to collective behaviors: insights from a prokaryote, Myxococcus xanthus. FEMS Microbiol Rev 36: 149-164.
21. West SA, Griffin AS, Gardner A, Diggle SP, (2006) Social evolution theory for microorganisms. Nat Rev Microbiol 4: 597-607.
22. Hibbing ME, Fuqua C, Parsek MR, Peterson SB, (2010) Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8: 15-25.
23. Rougeaux H, Guezennec M, Che LM, Payri C, Deslandes E, et al. (2001) Microbial communities and exopolysaccharides from Polynesian mats. Mar Biotechnol (NY) 3: 181-187.
24. Bergel A, Feron D, Flemming HC, (2010) From fundamentals to microbial power plants: electrochemically active biofilms. Bioelectrochemistry 78: 1.
25. Wierzchos J, Berlanga M, Ascaso C, Guerrero R, (2006) Micromorphological characterization and lithification of microbial mats from the Ebro Delta (Spain). Int Microbiol 9: 289-295.
26. Epstein AK, Pokroy B, Seminara A, Aizenberg J, (2011) Bacterial biofilm shows persistent resistance to liquid wetting and gas penetration. Proc Natl Acad Sci U S A 108: 995-1000.
27. Roeselers G, Loosdrecht MC, Muyzer G, (2008) Phototrophic biofilms and their potential applications. J Appl Phycol 20: 227-235.
28. Bhaya D, (2004) Light matters: phototaxis and signal transduction in unicellular cyanobacteria. Mol Microbiol 53: 745-754.
29. Brahamsha B, Bhaya D (2013) Motility in Unicellular and Filamentous Cyanobacteria. In: Flores E, editor. Cell Biology of Cyanobacteria.
30. Galante A, Wisen S, Bhaya D, Levy D, (2012) Modeling local interactions during the motion of cyanobacteria. J Theor Biol 309: 147-158.
31. Levy D, Requeijo T, (2008) Stochastic models for phototaxis. Bull Math Biol 70: 1684-1706.
32. Fiedler B, Borner T, Wilde A, (2005) Phototaxis in the cyanobacterium Synechocystis sp. PCC 6803: role of different photoreceptors. Photochem Photobiol 81: 1481-1488.
33. Grossman AR, Bhaya D, He Q, (2001) Tracking the light environment by cyanobacteria and the dynamic nature of light harvesting. J Biol Chem 276: 11449-11452.
34. Jekely G, (2009) Evolution of phototaxis. Philos Trans R Soc Lond B Biol Sci 364: 2795-2808.
35. Bhaya D, Bianco NR, Bryant D, Grossman A, (2000) Type IV pilus biogenesis and motility in the cyanobacterium Synechocystis sp. PCC6803. Mol Microbiol 37: 941-951.
36. Bhaya D, Watanabe N, Ogawa T, Grossman AR, (1999) The role of an alternative sigma factor in motility and pilus formation in the cyanobacterium Synechocystis sp. strain PCC6803. Proc Natl Acad Sci U S A 96: 3188-3193.
37. Gibiansky ML, Conrad JC, Jin F, Gordon VD, Motto DA, et al. (2010) Bacteria use type IV pili to walk upright and detach from surfaces. Science 330: 197.
38. Skerker JM, Berg HC, (2001) Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci U S A 98: 6901-6904.
39. Ng WO, Grossman AR, Bhaya D, (2003) Multiple light inputs control phototaxis in Synechocystis sp. strain PCC6803. J Bacteriol 185: 1599-1607.
40. Choi JS, Chung YH, Moon YJ, Kim C, Watanabe M, et al. (1999) Photomovement of the gliding cyanobacterium Synechocystis sp. PCC 6803. Photochem Photobiol 70: 95-102.
41. Bhaya D, Nakasugi K, Fazeli F, Burriesci MS, (2006) Phototaxis and impaired motility in adenylyl cyclase and cyclase receptor protein mutants of Synechocystis sp. strain PCC 6803. J Bacteriol 188: 7306-7310.
42. Burriesci M, Bhaya D, (2008) Tracking phototactic responses and modeling motility of Synechocystis sp. strain PCC6803. J Photochem Photobiol B 91: 77-86.
43. Chen BG, Turner L, Berg HC, (2007) The wetting agent required for swarming in Salmonella enterica serovar typhimurium is not a surfactant. J Bacteriol 189: 8750-8753.
44. Berleman JE, Vicente JJ, Davis AE, Jiang SY, Seo YE, et al. (2011) FrzS regulates social motility in Myxococcus xanthus by controlling exopolysaccharide production. PLoS One 6: e23920.
45. Bhaya D, Levy D, Requeijo T (2008) Group Dynamics of Phototaxis: Interacting Stochastic Many-Particle Systems and Their Continuum Limit. In: Benzoni-Gavage S, Serre D, editors. Hyperbolic Problems: Theory, Numerics, Applications: Springer Berlin Heidelberg. pp. 145-159.
46. Hu W, Yang Z, Lux R, Zhao M, Wang J, et al. (2012) Direct visualization of the interaction between pilin and exopolysaccharides of Myxococcus xanthus with eGFP-fused PilA protein. FEMS Microbiol Lett 326: 23-30.
47. Nan B, Zusman DR, (2011) Uncovering the mystery of gliding motility in the myxobacteria. Annu Rev Genet 45: 21-39.
48. Wu Y, Kaiser AD, Jiang Y, Alber MS, (2009) Periodic reversal of direction allows Myxobacteria to swarm. Proc Natl Acad Sci U S A 106: 1222-1227.
49. Harvey CW, Morcos F, Sweet CR, Kaiser D, Chatterjee S, et al. (2011) Study of elastic collisions of Myxococcus xanthus in swarms. Phys Biol 8: 026016.
50. Miller MB, Bassler BL, (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55: 165-199.
51. Chen YE, Tropini C, Jonas K, Tsokos CG, Huang KC, et al. (2011) Spatial gradient of protein phosphorylation underlies replicative asymmetry in a bacterium. Proc Natl Acad Sci U S A 108: 1052-1057.
52. Huang KC, Meir Y, Wingreen NS, (2003) Dynamic structures in Escherichia coli: spontaneous formation of MinE rings and MinD polar zones. Proc Natl Acad Sci U S A 100: 12724-12728.
53. Marée AFM, Panfilov AV, Hogeweg P, (1999) Phototaxis during the slug stage of Dictyostelium discoideum: a model study. Proceedings of the Royal Society of London Series B: Biological Sciences 266: 1351-1360.
54. Painter KJ, Sherratt JA, (2003) Modelling the movement of interacting cell populations. J Theor Biol 225: 327-339.
55. Markus M, Nagy-Ungvarai Z, Hess B, (1992) Phototaxis of spiral waves. Science 257: 225-227.
56. Golding I, Kozlovsky Y, Cohen I, Ben-Jacob E, (1998) Studies of bacterial branching growth using reaction-diffusion models for colonial development. Physica A: Statistical Mechanics and its Applications 260: 510-554.
57. Kozlovsky Y, Cohen I, Golding I, Ben-Jacob E, (1999) Lubricating bacteria model for branching growth of bacterial colonies. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 59: 7025-7035.
58. Fatehi H, Meyer-Hermann M, Figge MT, (2010) Modelling cellular aggregation induced by chemotaxis and phototaxis. Mathematical Medicine and Biology 27: 373-384.
59. Bhaya D, Takahashi A, Grossman AR, (2001) Light regulation of type IV pilus-dependent motility by chemosensor-like elements in Synechocystis PCC6803. Proc Natl Acad Sci U S A 98: 7540-7545.
60. Diz-Munoz A, Krieg M, Bergert M, Ibarlucea-Benitez I, Muller DJ, et al. (2010) Control of directed cell migration in vivo by membrane-to-cortex attachment. PLoS Biol 8: e1000544.
61. Joyce JA, Pollard JW, (2009) Microenvironmental regulation of metastasis. Nat Rev Cancer 9: 239-252.
62. Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G, (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol Rev 35: 171-205.