Two-Dimensionality of Yeast Colony Expansion Accompanied by Pattern Formation

PLoS Computational Biology

Volumn 10, Issue 12, 2014, Pages

  Chen, Lin ^a   Noorbakhsh, Javad ^b   Adams, Rhys M ^a   Samaniego Evans, Joseph ^b   Agollah, Germaine ^a   Nevozhay, Dmitry ^a,c   Kuzdzal Fick, Jennie ^a   Mehta, Pankaj ^b   Balázsi, Gábor ^a,d,e  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b Boston University   (United States)

^c FAR EASTERN FEDERAL UNIVERSITY   (Russian Federation)

^d STONY BROOK UNIVERSITY   (United States)

^e St Francis Hospital The Heart Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAE; POLYSACCHARIDES; YEAST;

AGAR PLATES; COLONY EXPANSION; PATTERN FORMATION; PHYSICAL MODELLING; QUANTITATIVE METHOD; SHAPE PATTERNS; SUGAR CONCENTRATION; SURFACE PATTERN; TWO DIMENSIONALITY; YEAST COLONY;

GENES;

ARTICLE; BACTERIUM COLONY; CELL DEATH; CELL DENSITY; CELL GROWTH; CELL SIZE; CONTROLLED STUDY; FLO11 GENE; FUNGAL CELL; FUNGAL COLONIZATION; FUNGAL GENE; FUNGUS GROWTH; GENE FUNCTION; GROWTH INHIBITION; GROWTH RATE; MATHEMATICAL MODEL; NONHUMAN; SACCHAROMYCES CEREVISIAE; YEAST; CELL CULTURE TECHNIQUE; COMPUTER SIMULATION; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHYSIOLOGY; PROCEDURES;

FLO11 PROTEIN, S CEREVISIAE; GLUCOSE; MEMBRANE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

CELL CULTURE TECHNIQUES; COMPUTER SIMULATION; GLUCOSE; MEMBRANE GLYCOPROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84919622589     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003979     Document Type: Article

References (55)

1. Forgács G, Newman S (2005) Biological physics of the developing embryo. Cambridge, UK; New York: Cambridge University Press. vi, 337 p. p.
2. Richards MJ, Edwards JR, Culver DH, Gaynes RP, (2000) Nosocomial infections in combined medical-surgical intensive care units in the United States. Infect Control Hosp Epidemiol 21: 510–515.
3. Richards MJ, Edwards JR, Culver DH, Gaynes RP, (1999) Nosocomial infections in pediatric intensive care units in the United States. National Nosocomial Infections Surveillance System. Pediatrics 103: e39.
4. Richards MJ, Edwards JR, Culver DH, Gaynes RP, (1999) Nosocomial infections in medical intensive care units in the United States. National Nosocomial Infections Surveillance System. Crit Care Med 27: 887–892.
5. Kojic EM, Darouiche RO, (2004) Candida infections of medical devices. Clinical microbiology reviews 17: 255–267.
6. Costerton JW, Stewart PS, Greenberg EP, (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318–1322.
7. Kempes CP, Okegbe C, Mears-Clarke Z, Follows MJ, Dietrich LE, (2014) Morphological optimization for access to dual oxidants in biofilms. Proceedings of the National Academy of Sciences of the United States of America 111: 208–213.
8. Hall-Stoodley L, Costerton JW, Stoodley P, (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2: 95–108.
9. Picioreanu C, van Loosdrecht MC, Heijnen JJ, (1998) Mathematical modeling of biofilm structure with a hybrid differential-discrete cellular automaton approach. Biotechnol Bioeng 58: 101–116.
10. de Beer D, Stoodley P, Roe F, Lewandowski Z, (1994) Effects of biofilm structures on oxygen distribution and mass transport. Biotechnol Bioeng 43: 1131–1138.
11. Xavier JB, Foster KR, (2007) Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci U S A 104: 876–881.
12. Xavier JB, Martinez-Garcia E, Foster KR, (2009) Social evolution of spatial patterns in bacterial biofilms: when conflict drives disorder. Am Nat 174: 1–12.
13. Kim W, Racimo F, Schluter J, Levy SB, Foster KR, (2014) Importance of positioning for microbial evolution. Proc Natl Acad Sci U S A 111: E1639–1647.
14. Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, et al. (2001) Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J Bacteriol 183: 5385–5394.
15. Lambert G, Estevez-Salmeron L, Oh S, Liao D, Emerson BM, et al. (2011) An analogy between the evolution of drug resistance in bacterial communities and malignant tissues. Nat Rev Cancer 11: 375–382.
16. Ben-Jacob E, Coffey DS, Levine H, (2012) Bacterial survival strategies suggest rethinking cancer cooperativity. Trends Microbiol 20: 403–410.
17. Asally M, Kittisopikul M, Rue P, Du Y, Hu Z, et al. (2012) Localized cell death focuses mechanical forces during 3D patterning in a biofilm. Proceedings of the National Academy of Sciences of the United States of America 109: 18891–18896.
18. Reynolds TB, Fink GR, (2001) Bakers' yeast, a model for fungal biofilm formation. Science 291: 878–881.
19. Zara G, Goffrini P, Lodi T, Zara S, Mannazzu I, et al. (2012) FLO11 expression and lipid biosynthesis are required for air-liquid biofilm formation in a Saccharomyces cerevisiae flor strain. FEMS Yeast Res 12: 864–866.
20. Reynolds TB, Jansen A, Peng X, Fink GR, (2008) Mat formation in Saccharomyces cerevisiae requires nutrient and pH gradients. Eukaryotic cell 7: 122–130.
21. Octavio LM, Gedeon K, Maheshri N, (2009) Epigenetic and Conventional Regulation Is Distributed among Activators of FLO11 Allowing Tuning of Population-Level Heterogeneity in Its Expression. Plos Genetics 5.
22. Holmes DL, Lancaster AK, Lindquist S, Halfmann R, (2013) Heritable remodeling of yeast multicellularity by an environmentally responsive prion. Cell 153: 153–165.
23. Voordeckers K, De Maeyer D, van der Zande E, Vinces MD, Meert W, et al. (2012) Identification of a complex genetic network underlying Saccharomyces cerevisiae colony morphology. Mol Microbiol 86: 225–239.
24. Taylor MB, Ehrenreich IM, (2014) Genetic interactions involving five or more genes contribute to a complex trait in yeast. PLoS Genet 10: e1004324.
25. Bumgarner SL, Dowell RD, Grisafi P, Gifford DK, Fink GR, (2009) Toggle involving cis-interfering noncoding RNAs controls variegated gene expression in yeast. Proceedings of the National Academy of Sciences of the United States of America 106: 18321–18326.
26. Bumgarner SL, Neuert G, Voight BF, Symbor-Nagrabska A, Grisafi P, et al. (2012) Single-cell analysis reveals that noncoding RNAs contribute to clonal heterogeneity by modulating transcription factor recruitment. Molecular cell 45: 470–482.
27. Gagiano M, van Dyk D, Bauer FF, Lambrechts MG, Pretorius IS, (1999) Msn1p/Mss10p, Mss11p and Muc1p/Flo11p are part of a signal transduction pathway downstream of Mep2p regulating invasive growth and pseudohyphal differentiation in Saccharomyces cerevisiae. Molecular microbiology 31: 103–116.
28. Kim TS, Lee SB, Kang HS, (2004) Glucose repression of STA1 expression is mediated by the Nrg1 and Sfl1 repressors and the Srb8-11 complex. Molecular and cellular biology 24: 7695–7706.
29. Lo TL, Qu Y, Uwamahoro N, Quenault T, Beilharz TH, et al. (2012) The mRNA decay pathway regulates the expression of the Flo11 adhesin and biofilm formation in Saccharomyces cerevisiae. Genetics 191: 1387–1391.
30. Lo WS, Dranginis AM, (1998) The cell surface flocculin Flo11 is required for pseudohyphae formation and invasion by Saccharomyces cerevisiae. Molecular biology of the cell 9: 161–171.
31. Fujikawa H, Matsushita M, (1991) Bacterial Fractal Growth in the Concentration Field of Nutrient. Journal of the Physical Society of Japan 60: 88–94.
32. Gil de Prado E, Rivas EM, de Siloniz MI, Diezma B, Barreiro P, et al. (2014) Quantitative analysis of morphological changes in yeast colonies growing on solid medium: The eccentricity and Fourier indexes. Yeast
33. Matsushita M, Fujikawa H, (1990) Diffusion-Limited Growth in Bacterial Colony Formation. Physica A 168: 498–506.
34. Cooper AL, Dean AC, Hinshelwood C, (1968) Factors affecting the growth of bacterial colonies on agar plates. Proc R Soc Lond B Biol Sci 171: 175–199.
35. Palumbo SA, Johnson MG, Rieck VT, Witter LD, (1971) Growth measurements on surface colonies of bacteria. J Gen Microbiol 66: 137–143.
36. Su PT, Liao CT, Roan JR, Wang SH, Chiou A, et al. (2012) Bacterial colony from two-dimensional division to three-dimensional development. PLoS One 7: e48098.
37. Mimura M, Sakaguchi H, Matsushita M, (2000) Reaction-diffusion modelling of bacterial colony patterns. Physica A 282: 283–303.
38. 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.
39. Efimenko K, Rackaitis M, Manias E, Vaziri A, Mahadevan L, et al. (2005) Nested self-similar wrinkling patterns in skins. Nature materials 4: 293–297.
40. Vandeparre H, Damman P, (2008) Wrinkling of stimuloresponsive surfaces: Mechanical instability coupled to diffusion. Physical Review Letters 101.
41. Vachova L, Stovicek V, Hlavacek O, Chernyavskiy O, Stepanek L, et al. (2011) Flo11p, drug efflux pumps, and the extracellular matrix cooperate to form biofilm yeast colonies. The Journal of cell biology 194: 679–687.
42. Cerda E, Mahadevan L, (2003) Geometry and physics of wrinkling. Phys Rev Lett 90: 074302.
43. Korolev KS, Muller MJ, Karahan N, Murray AW, Hallatschek O, et al. (2012) Selective sweeps in growing microbial colonies. Physical biology 9: 026008.
44. Pontecorvo G, Gemmell AR, (1944) Colonies of Penicillium notatum and other moulds as models for the study of population genetics. Nature 154: 532–534.
45. Lindner P, (1893) Das Wachstum der Hefens auf festen Nährboden. Wochenschrift für Brauerei 10: 692.
46. Ben-Jacob E, Schochet O, Tenenbaum A, Cohen I, Czirok A, et al. (1994) Generic Modeling of Cooperative Growth-Patterns in Bacterial Colonies. Nature 368: 46–49.
47. Ben-Jacob E, Cohen I, Shochet O, Tenenbaum A, Vicsek T, et al. (1995) Cooperative Formation of Chiral Patterns during Growth of Bacterial Colonies. Physical Review Letters 75: 2899–2902.
48. Berk V, Fong JC, Dempsey GT, Develioglu ON, Zhuang X, et al. (2012) Molecular architecture and assembly principles of Vibrio cholerae biofilms. Science 337: 236–239.
49. Ben-Jacob E, Levine H, (2006) Self-engineering capabilities of bacteria. J R Soc Interface 3: 197–214.
50. Trejo M, Douarche C, Bailleux V, Poulard C, Mariot S, et al. (2013) Elasticity and wrinkled morphology of Bacillus subtilis pellicles. Proceedings of the National Academy of Sciences of the United States of America 110: 2011–2016.
51. Dietrich LE, Okegbe C, Price-Whelan A, Sakhtah H, Hunter RC, et al. (2013) Bacterial community morphogenesis is intimately linked to the intracellular redox state. Journal of bacteriology 195: 1371–1380.
52. Wilking JN, Zaburdaev V, De Volder M, Losick R, Brenner MP, et al. (2013) Liquid transport facilitated by channels in Bacillus subtilis biofilms. Proceedings of the National Academy of Sciences of the United States of America 110: 848–852.
53. Gietz RD, Schiestl RH, (2007) Large-scale high-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nature Protocols 2: 38–41.
54. Fu CC, Grimes A, Long M, Ferri CGL, Rich BD, et al. (2009) Tunable Nanowrinkles on Shape Memory Polymer Sheets. Advanced Materials 21: 4472.
55. Nayar VT, Weiland JD, Nelson CS, Hodge AM, (2012) Elastic and viscoelastic characterization of agar. J Mech Behav Biomed Mater 7: 60–68.