Cell Distribution within Yeast Colonies and Colony Biofilms: How Structure Develops
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
19-11384S
Czech Science Foundation
LQ1604 NPU II
MEYS
RVO 61388971
Czech Academy of Sciences
BIOCEV CZ.1.05/1.1.00/02.0109
ERDF and MEYS
PubMed
32485964
PubMed Central
PMC7312624
DOI
10.3390/ijms21113873
PII: ijms21113873
Knihovny.cz E-zdroje
- Klíčová slova
- Flo11p adhesin, cell adhesion, cell organization, colonies and biofilms, laboratory and wild Saccharomyces cerevisiae strains, structure development, yeast multicellular structures,
- MeSH
- biofilmy * MeSH
- buněčné dělení MeSH
- membránové glykoproteiny genetika metabolismus MeSH
- mikrobiální interakce MeSH
- mutace MeSH
- Saccharomyces cerevisiae - proteiny genetika metabolismus MeSH
- Saccharomyces cerevisiae cytologie metabolismus fyziologie MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- FLO11 protein, S cerevisiae MeSH Prohlížeč
- membránové glykoproteiny MeSH
- Saccharomyces cerevisiae - proteiny MeSH
Multicellular structures formed by yeasts and other microbes are valuable models for investigating the processes of cell-cell interaction and pattern formation, as well as cell signaling and differentiation. These processes are essential for the organization and development of diverse microbial communities that are important in everyday life. Two major types of multicellular structures are formed by yeast Saccharomyces cerevisiae on semisolid agar. These are colonies formed by laboratory or domesticated strains and structured colony biofilms formed by wild strains. These structures differ in spatiotemporal organization and cellular differentiation. Using state-of-the-art microscopy and mutant analysis, we investigated the distribution of cells within colonies and colony biofilms and the involvement of specific processes therein. We show that prominent differences between colony and biofilm structure are determined during early stages of development and are associated with the different distribution of growing cells. Two distinct cell distribution patterns were identified-the zebra-type and the leopard-type, which are genetically determined. The role of Flo11p in cell adhesion and extracellular matrix production is essential for leopard-type distribution, because FLO11 deletion triggers the switch to zebra-type cell distribution. However, both types of cell organization are independent of cell budding polarity and cell separation as determined using respective mutants.
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Blankenship J.R., Mitchell A.P. How to build a biofilm: A fungal perspective. Curr. Opin. Microbiol. 2006;9:588–594. doi: 10.1016/j.mib.2006.10.003. PubMed DOI
Lohse M.B., Gulati M., Johnson A.D., Nobile C.J. Development and regulation of single- and multi-species Candida albicans biofilms. Nat. Rev. Microbiol. 2018;16:19–31. doi: 10.1038/nrmicro.2017.107. PubMed DOI PMC
Palkova Z., Vachova L. Yeast cell differentiation: Lessons from pathogenic and non-pathogenic yeasts. Semin. Cell Dev. Biol. 2016;57:110–119. PubMed
Pujol C., Daniels K.J., Soll D.R. A Comparison of switching and biofilm formation between MTL13 homozygous strains of Candida albicans and Candida dubliniensis. Eukaryot. Cell. 2015;14:1186–1202. doi: 10.1128/EC.00146-15. PubMed DOI PMC
Reynolds T.B. Going with the Flo: The role of Flo11-dependent and independent interactions in yeast Mat formation. J. Fungi. 2018;4:E132. PubMed PMC
Reynolds T.B., Fink G.R. Bakers’ yeast, a model for fungal biofilm formation. Science. 2001;291:878–881. doi: 10.1126/science.291.5505.878. PubMed DOI
Smukalla S., Caldara M., Pochet N., Beauvais A., Guadagnini S., Yan C., Vinces M.D., Jansen A., Prevost M.C., Latge J.P., et al. FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell. 2008;135:726–737. doi: 10.1016/j.cell.2008.09.037. PubMed DOI PMC
Vachova L., Palkova Z. How structured yeast multicellular communities live, age and die? FEMS Yeast Res. 2018;18:foy033. PubMed
Van Nguyen P., Plocek V., Vachova L., Palkova Z. Glucose, Cyc8p and Tup1p regulate biofilm formation and dispersal in wild Saccharomyces cerevisiae. NPJ Biofilms Microbiomes. 2020;6:7. doi: 10.1038/s41522-020-0118-1. PubMed DOI PMC
Zara S., Bakalinsky A.T., Zara G., Pirino G., Demontis M.A., Budroni M. FLO11-based model for air-liquid interfacial biofilm formation by Saccharomyces cerevisiae. Appl. Environ. Microbiol. 2005;71:2934–2939. PubMed PMC
Cap M., Stepanek L., Harant K., Vachova L., Palkova Z. Cell differentiation within a yeast colony: Metabolic and regulatory parallels with a tumor-affected organism. Mol. Cell. 2012;46:436–448. doi: 10.1016/j.molcel.2012.04.001. PubMed DOI
Vachova L., Hatakova L., Cap M., Pokorna M., Palkova Z. Rapidly developing yeast microcolonies differentiate in a similar way to aging giant colonies. Oxid Med. Cell Longev. 2013;2013:102485. doi: 10.1155/2013/102485. PubMed DOI PMC
Palkova Z., Forstova J. Yeast colonies synchronise their growth and development. J. Cell Sci. 2000;113:1923–1928. PubMed
Palkova Z., Janderova B., Gabriel J., Zikanova B., Pospisek M., Forstova J. Ammonia mediates communication between yeast colonies. Nature. 1997;390:532–536. doi: 10.1038/37398. PubMed DOI
Kuthan M., Devaux F., Janderova B., Slaninova I., Jacq C., Palkova Z. Domestication of wild Saccharomyces cerevisiae is accompanied by changes in gene expression and colony morphology. Mol. Microbiol. 2003;47:745–754. PubMed
Vachova L., Stovicek V., Hlavacek O., Chernyavskiy O., Stepanek L., Kubinova L., Palkova Z. Flo11p, drug efflux pumps, and the extracellular matrix cooperate to form biofilm yeast colonies. J. Cell Biol. 2011;194:679–687. PubMed PMC
Granek J.A., Magwene P.M. Environmental and genetic determinants of colony morphology in yeast. PLoS Genet. 2010;6:e1000823. doi: 10.1371/journal.pgen.1000823. PubMed DOI PMC
Stovicek V., Vachova L., Kuthan M., Palkova Z. General factors important for the formation of structured biofilm-like yeast colonies. Fungal. Genet. Biol. 2010;47:1012–1022. doi: 10.1016/j.fgb.2010.08.005. PubMed DOI
Nguyen P., Hlavacek O., Marsikova J., Vachova L., Palkova Z. Cyc8p and Tup1p transcription regulators antagonistically regulate Flo11p expression and complexity of yeast colony biofilms. PLoS Genet. 2018;14:e1007495. doi: 10.1371/journal.pgen.1007495. PubMed DOI PMC
Voordeckers K., De Maeyer D., van der Zande E., Vinces M.D., Meert W., Cloots L., Ryan O., Marchal K., Verstrepen K.J. Identification of a complex genetic network underlying Saccharomyces cerevisiae colony morphology. Mol. Microbiol. 2012;86:225–239. doi: 10.1111/j.1365-2958.2012.08192.x. PubMed DOI PMC
Cabib E., Roberts R., Bowers B. Synthesis of the yeast cell wall and its regulation. Ann. Rev. Biochem. 1982;51:763–793. doi: 10.1146/annurev.bi.51.070182.003555. PubMed DOI
Vachova L., Palkova Z. Physiological regulation of yeast cell death in multicellular colonies is triggered by ammonia. J. Cell Biol. 2005;169:711–717. doi: 10.1083/jcb.200410064. PubMed DOI PMC
Chant J., Herskowitz I. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell. 1991;65:1203–1212. PubMed
Chant J., Pringle J.R. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J. Cell Biol. 1995;129:751–765. doi: 10.1083/jcb.129.3.751. PubMed DOI PMC
Bidlingmaier S., Weiss E.L., Seidel C., Drubin D.G., Snyder M. The Cbk1p pathway is important for polarized cell growth and cell separation in Saccharomyces cerevisiae. Mol. Cell Biol. 2001;21:2449–2462. doi: 10.1128/MCB.21.7.2449-2462.2001. PubMed DOI PMC
Vopalenska I., Stovicek V., Janderova B., Vachova L., Palkova Z. Role of distinct dimorphic transitions in territory colonizing and formation of yeast colony architecture. Environ. Microbiol. 2010;12:264–277. doi: 10.1111/j.1462-2920.2009.02067.x. PubMed DOI
Stovicek V., Vachova L., Begany M., Wilkinson D., Palkova Z. Global changes in gene expression associated with phenotypic switching of wild yeast. BMC Genom. 2014;15:136. doi: 10.1186/1471-2164-15-136. PubMed DOI PMC
Vopalenska I., Hulkova M., Janderova B., Palkova Z. The morphology of Saccharomyces cerevisiae colonies is affected by cell adhesion and the budding pattern. Res. Microbiol. 2005;156:921–931. PubMed
Ratcliff W.C., Fankhauser J.D., Rogers D.W., Greig D., Travisano M. Origins of multicellular evolvability in snowflake yeast. Nat. Commun. 2015;6:6102. doi: 10.1038/ncomms7102. PubMed DOI PMC
Janke C., Magiera M.M., Rathfelder N., Taxis C., Reber S., Maekawa H., Moreno-Borchart A., Doenges G., Schwob E., Schiebel E., et al. A versatile toolbox for PCR-based tagging of yeast genes: New fluorescent proteins, more markers and promoter substitution cassettes. Yeast. 2004;21:947–962. PubMed
Podholová K., Plocek V., Rešetárová S., Kučerová H., Hlaváček O., Váchová L., Palková Z. Divergent branches of mitochondrial signaling regulate specific genes and the viability of specialized cell types of differentiated yeast colonies. Oncotarget. 2016;7:15299–15314. PubMed PMC
Guldener U., Heck S., Fielder T., Beinhauer J., Hegemann J.H. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 1996;24:2519–2524. doi: 10.1093/nar/24.13.2519. PubMed DOI PMC
Gietz R.D., Woods R.A. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Method Enzymol. 2002;350:87–96. PubMed
Vachova L., Chernyavskiy O., Strachotova D., Bianchini P., Burdikova Z., Fercikova I., Kubinova L., Palkova Z. Architecture of developing multicellular yeast colony: Spatio-temporal expression of Ato1p ammonium exporter. Environ. Microbiol. 2009;11:1866–1877. PubMed