IDEAS home Printed from https://ideas.repec.org/a/plo/pcbi00/1003979.html
   My bibliography  Save this article

Two-Dimensionality of Yeast Colony Expansion Accompanied by Pattern Formation

Author

Listed:
  • Lin Chen
  • Javad Noorbakhsh
  • Rhys M Adams
  • Joseph Samaniego-Evans
  • Germaine Agollah
  • Dmitry Nevozhay
  • Jennie Kuzdzal-Fick
  • Pankaj Mehta
  • Gábor Balázsi

Abstract

Yeasts can form multicellular patterns as they expand on agar plates, a phenotype that requires a functional copy of the FLO11 gene. Although the biochemical and molecular requirements for such patterns have been examined, the mechanisms underlying their formation are not entirely clear. Here we develop quantitative methods to accurately characterize the size, shape, and surface patterns of yeast colonies for various combinations of agar and sugar concentrations. We combine these measurements with mathematical and physical models and find that FLO11 gene constrains cells to grow near the agar surface, causing the formation of larger and more irregular colonies that undergo hierarchical wrinkling. Head-to-head competition assays on agar plates indicate that two-dimensional constraint on the expansion of FLO11 wild type (FLO11) cells confers a fitness advantage over FLO11 knockout (flo11Δ) cells on the agar surface.Author Summary: Microbial biofilms are commonly found in nature and are highly relevant to public health. Biofilms can impose high risks to drinking water distribution by stable adherence to the interior of water pipes, and to food industry by contamination of food processing systems. Biofilm adherence to indwelling medical devices causes high rates of clinical infections that are difficult to eliminate as biofilm microbes resist treatment with antibiotics and biocides. These microbial abilities are related to the spatial composition and overall morphology of the biofilm. While the mechanisms underlying biofilm structure and morphology have been examined for bacteria, much less is known about eukaryotic biofilms. Here we find that the size, shape and patterning of budding yeast colonies can arise from constraining colony expansion to the surface of agar plates. Through computational analysis and mathematical modeling, we find that rapid colony expansion, colony shape irregularity and hierarchical wrinkling of the yeast colony surface can result from two-dimensionality of expansion imposed by the adhesin FLO11. Finally, we find that two-dimensional expansion conveys competitive advantage during head-to-head competition with the mutant cells lacking FLO11.

Suggested Citation

  • Lin Chen & Javad Noorbakhsh & Rhys M Adams & Joseph Samaniego-Evans & Germaine Agollah & Dmitry Nevozhay & Jennie Kuzdzal-Fick & Pankaj Mehta & Gábor Balázsi, 2014. "Two-Dimensionality of Yeast Colony Expansion Accompanied by Pattern Formation," PLOS Computational Biology, Public Library of Science, vol. 10(12), pages 1-14, December.
  • Handle: RePEc:plo:pcbi00:1003979
    DOI: 10.1371/journal.pcbi.1003979
    as

    Download full text from publisher

    File URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1003979
    Download Restriction: no

    File URL: https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1003979&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pcbi.1003979?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Mimura, Masayasu & Sakaguchi, Hideo & Matsushita, Mitsugu, 2000. "Reaction–diffusion modelling of bacterial colony patterns," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 282(1), pages 283-303.
    2. Golding, Ido & Kozlovsky, Yonathan & Cohen, Inon & Ben-Jacob, Eshel, 1998. "Studies of bacterial branching growth using reaction–diffusion models for colonial development," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 260(3), pages 510-554.
    3. Matsushita, Mitsugu & Fujikawa, Hiroshi, 1990. "Diffusion-limited growth in bacterial colony formation," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 168(1), pages 498-506.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Leyva, J. Francisco & Málaga, Carlos & Plaza, Ramón G., 2013. "The effects of nutrient chemotaxis on bacterial aggregation patterns with non-linear degenerate cross diffusion," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 392(22), pages 5644-5662.
    2. Mansour, M.B.A., 2007. "Traveling wave solutions of a reaction–diffusion model for bacterial growth," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 383(2), pages 466-472.
    3. Samvel Sarukhanian & Anna Maslovskaya & Christina Kuttler, 2023. "Three-Dimensional Cellular Automaton for Modeling of Self-Similar Evolution in Biofilm-Forming Bacterial Populations," Mathematics, MDPI, vol. 11(15), pages 1-18, July.
    4. Banitz, Thomas & Fetzer, Ingo & Johst, Karin & Wick, Lukas Y. & Harms, Hauke & Frank, Karin, 2011. "Assessing biodegradation benefits from dispersal networks," Ecological Modelling, Elsevier, vol. 222(14), pages 2552-2560.
    5. Ben-Jacob, Eshel & Cohen, Inon & Golding, Ido & Gutnick, David L. & Tcherpakov, Marianna & Helbing, Dirk & Ron, Ilan G., 2000. "Bacterial cooperative organization under antibiotic stress," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 282(1), pages 247-282.
    6. Csahók, Zoltán & Czirók, András, 1997. "Hydrodynamics of bacterial motion," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 243(3), pages 304-318.
    7. Chapwanya, Michael & Dumani, Phindile, 2023. "Stationary and oscillatory patterns in microbial population under environmental stress," Mathematics and Computers in Simulation (MATCOM), Elsevier, vol. 210(C), pages 370-383.
    8. Ben-Jacob, Eshel, 1998. "Bacterial wisdom, Gödel's theorem and creative genomic webs," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 248(1), pages 57-76.
    9. Gafiychuk, V.V. & Datsko, B.Yo., 2006. "Pattern formation in a fractional reaction–diffusion system," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 365(2), pages 300-306.
    10. Badoual, M. & Derbez, P. & Aubert, M. & Grammaticos, B., 2009. "Simulating the migration and growth patterns of Bacillus subtilis," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 388(4), pages 549-559.
    11. Golding, Ido & Kozlovsky, Yonathan & Cohen, Inon & Ben-Jacob, Eshel, 1998. "Studies of bacterial branching growth using reaction–diffusion models for colonial development," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 260(3), pages 510-554.
    12. Muzzio, Nicolás E. & Horowitz, Claudio M. & Azzaroni, Omar & Moya, Sergio E. & Pasquale, Miguel A., 2021. "Tilted mammalian cell colony propagation dynamics on patterned substrates," Chaos, Solitons & Fractals, Elsevier, vol. 146(C).
    13. Ron, Ilan G. & Golding, Ido & Lifsitz-Mercer, Beatrice & Ben-Jacob, Eshel, 2003. "Bursts of sectors in expanding bacterial colonies as a possible model for tumor growth and metastases," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 320(C), pages 485-496.
    14. Ruzicka, Marek C. & Fridrich, Mirek & Burkhard, Martin, 1995. "A bacterial colony is not self-similar," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 216(4), pages 382-385.
    15. Ben-Jacob, Eshel & Tenenbaum, Adam & Shochet, Ofer & Avidan, Orna, 1994. "Holotransformations of bacterial colonies and genome cybernetics," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 202(1), pages 1-47.
    16. Tatek, Yergou B. & Slater, Gary W., 2006. "A simulation model of biofilms with autonomous cells: I. Analysis of a two-dimensional version," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 362(2), pages 382-402.
    17. Ben-Jacob, Eshel & Cohen, Inon & Czirók, András & Vicsek, Tamás & Gutnick, David L., 1997. "Chemomodulation of cellular movement, collective formation of vortices by swarming bacteria, and colonial development," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 238(1), pages 181-197.
    18. Salcedo-Sanz, S. & Cuadra, L., 2019. "Hybrid L-systems–Diffusion Limited Aggregation schemes," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 514(C), pages 592-605.
    19. Kaoru Sugimura & Kohei Shimono & Tadashi Uemura & Atsushi Mochizuki, 2007. "Self-organizing Mechanism for Development of Space-filling Neuronal Dendrites," PLOS Computational Biology, Public Library of Science, vol. 3(11), pages 1-12, November.
    20. Frey, Erwin, 2010. "Evolutionary game theory: Theoretical concepts and applications to microbial communities," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 389(20), pages 4265-4298.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pcbi00:1003979. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: ploscompbiol (email available below). General contact details of provider: https://journals.plos.org/ploscompbiol/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.