Flo11p, drug efflux pumps, and the extracellular matrix cooperate to form biofilm yeast colonies
Language English Country United States Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
Grant support
Howard Hughes Medical Institute - United States
PubMed
21875945
PubMed Central
PMC3171128
DOI
10.1083/jcb.201103129
PII: jcb.201103129
Knihovny.cz E-resources
- MeSH
- ATP-Binding Cassette Transporters genetics metabolism MeSH
- Biofilms growth & development MeSH
- Models, Biological MeSH
- Gene Deletion MeSH
- DNA-Binding Proteins genetics metabolism MeSH
- Extracellular Matrix physiology MeSH
- Galactokinase genetics metabolism MeSH
- Galactose metabolism MeSH
- Hydroxymethylglutaryl CoA Reductases genetics metabolism MeSH
- Copper metabolism MeSH
- Membrane Glycoproteins genetics metabolism MeSH
- Metallothionein genetics metabolism MeSH
- Oxazines metabolism MeSH
- Permeability MeSH
- Profilins genetics MeSH
- Cell Cycle Proteins genetics MeSH
- Multidrug Resistance-Associated Proteins genetics metabolism MeSH
- Recombinant Fusion Proteins genetics metabolism MeSH
- Saccharomyces cerevisiae Proteins genetics metabolism MeSH
- Saccharomyces cerevisiae cytology growth & development metabolism MeSH
- Transcription Factors genetics metabolism MeSH
- Green Fluorescent Proteins genetics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- ATP-Binding Cassette Transporters MeSH
- CDC3 protein, S cerevisiae MeSH Browser
- CUP1-1 protein, S cerevisiae MeSH Browser
- DNA-Binding Proteins MeSH
- enhanced green fluorescent protein MeSH Browser
- FLO11 protein, S cerevisiae MeSH Browser
- GAL1 protein, S cerevisiae MeSH Browser
- Galactokinase MeSH
- Galactose MeSH
- Hydroxymethylglutaryl CoA Reductases MeSH
- Copper MeSH
- Membrane Glycoproteins MeSH
- Metallothionein MeSH
- nile red MeSH Browser
- Oxazines MeSH
- PDR1 protein, S cerevisiae MeSH Browser
- PDR5 protein, S cerevisiae MeSH Browser
- Profilins MeSH
- Cell Cycle Proteins MeSH
- Multidrug Resistance-Associated Proteins MeSH
- Recombinant Fusion Proteins MeSH
- Saccharomyces cerevisiae Proteins MeSH
- SNQ2 protein, S cerevisiae MeSH Browser
- Transcription Factors MeSH
- Green Fluorescent Proteins MeSH
Much like other microorganisms, wild yeasts preferentially form surface-associated communities, such as biofilms and colonies, that are well protected against hostile environments and, when growing as pathogens, against the host immune system. However, the molecular mechanisms underlying the spatiotemporal development and environmental resistance of biofilms and colonies remain largely unknown. In this paper, we show that a biofilm yeast colony is a finely tuned, complex multicellular organism in which specialized cells jointly execute multiple protection strategies. These include a Pdr1p-regulated mechanism whereby multidrug resistance transporters Pdr5p and Snq2p expel external compounds solely within the surface cell layers as well as developmentally regulated production by internal cells of a selectively permeable extracellular matrix. The two mechanisms act in concert during colony development, allowing growth of new cell generations in a well-protected internal cavity of the colony. Colony architecture is strengthened by intercellular fiber connections.
See more in PubMed
Al-Fattani M.A., Douglas L.J. 2006. Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J. Med. Microbiol. 55:999–1008 10.1099/jmm.0.46569-0 PubMed DOI
Baillie G.S., Douglas L.J. 2000. Matrix polymers of Candida biofilms and their possible role in biofilm resistance to antifungal agents. J. Antimicrob. Chemother. 46:397–403 10.1093/jac/46.3.397 PubMed DOI
Balzi E., Chen W., Ulaszewski S., Capieaux E., Goffeau A. 1987. The multidrug resistance gene PDR1 from Saccharomyces cerevisiae. J. Biol. Chem. 262:16871–16879 PubMed
Balzi E., Wang M., Leterme S., Van Dyck L., Goffeau A. 1994. PDR5, a novel yeast multidrug resistance conferring transporter controlled by the transcription regulator PDR1. J. Biol. Chem. 269:2206–2214 PubMed
Bayly J.C., Douglas L.M., Pretorius I.S., Bauer F.F., Dranginis A.M. 2005. Characteristics of Flo11-dependent flocculation in Saccharomyces cerevisiae. FEM. Yeast Res. 5:1151–1156 10.1016/j.femsyr.2005.05.004 PubMed DOI
Beauvais A., Loussert C., Prevost M.C., Verstrepen K., Latgé J.P. 2009. Characterization of a biofilm-like extracellular matrix in FLO1-expressing Saccharomyces cerevisiae cells. FEM. Yeast Res. 9:411–419 10.1111/j.1567-1364.2009.00482.x PubMed DOI
Blankenship J.R., Mitchell A.P. 2006. How to build a biofilm: a fungal perspective. Curr. Opin. Microbiol. 9:588–594 10.1016/j.mib.2006.10.003 PubMed DOI
Decho A.W. 2000. Microbial biofilms in intertidal systems: an overview. Cont. Shelf Res. 20:1257–1273 10.1016/S0278-4343(00)00022-4 DOI
Donlan R.M., Costerton J.W. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15:167–193 10.1128/CMR.15.2.167-193.2002 PubMed DOI PMC
Douglas L.J. 2003. Candida biofilms and their role in infection. Trends Microbiol. 11:30–36 10.1016/S0966-842X(02)00002-1 PubMed DOI
Douglas L.M., Li L., Yang Y., Dranginis A.M. 2007. Expression and characterization of the flocculin Flo11/Muc1, a Saccharomyces cerevisiae mannoprotein with homotypic properties of adhesion. Eukaryot. Cell. 6:2214–2221 10.1128/EC.00284-06 PubMed DOI PMC
Dranginis A.M., Rauceo J.M., Coronado J.E., Lipke P.N. 2007. A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol. Mol. Biol. Rev. 71:282–294 10.1128/MMBR.00037-06 PubMed DOI PMC
Fardeau V., Lelandais G., Oldfield A., Salin H., Lemoine S., Garcia M., Tanty V., Le Crom S., Jacq C., Devaux F. 2007. The central role of PDR1 in the foundation of yeast drug resistance. J. Biol. Chem. 282:5063–5074 10.1074/jbc.M610197200 PubMed DOI
Flemming H.C., Wingender J. 2010. The biofilm matrix. Nat. Rev. Microbiol. 8:623–633 PubMed
Gietz R.D., Woods R.A. 2002. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350:87–96 10.1016/S0076-6879(02)50957-5 PubMed DOI
Gimeno C.J., Ljungdahl P.O., Styles C.A., Fink G.R. 1992. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell. 68:1077–1090 10.1016/0092-8674(92)90079-R PubMed DOI
Greenspan P., Fowler S.D. 1985. Spectrofluorometric studies of the lipid probe, nile red. J. Lipid Res. 26:781–789 PubMed
Gueldener U., Heinisch J., Koehler G.J., Voss D., Hegemann J.H. 2002. A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res. 30:e23 10.1093/nar/30.6.e23 PubMed DOI PMC
Guo B., Styles C.A., Feng Q., Fink G.R. 2000. A Saccharomyces gene family involved in invasive growth, cell-cell adhesion, and mating. Proc. Natl. Acad. Sci. USA. 97:12158–12163 10.1073/pnas.220420397 PubMed DOI PMC
Hartwell L.H. 1971. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp. Cell Res. 69:265–276 10.1016/0014-4827(71)90223-0 PubMed DOI
Ishigami M., Nakagawa Y., Hayakawa M., Iimura Y. 2004. FLO11 is essential for flor formation caused by the C-terminal deletion of NRG1 in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 237:425–430 PubMed
Joubert L.M., Wolfaardt G.M., Botha A. 2006. Microbial exopolymers link predator and prey in a model yeast biofilm system. Microb. Ecol. 52:187–197 10.1007/s00248-006-9063-7 PubMed DOI
Jungwirth H., Kuchler K. 2006. Yeast ABC transporters–a tale of sex, stress, drugs and aging. FEBS Lett. 580:1131–1138 10.1016/j.febslet.2005.12.050 PubMed DOI
Klis F.M., Sosinska G.J., de Groot P.W., Brul S. 2009. Covalently linked cell wall proteins of Candida albicans and their role in fitness and virulence. FEM. Yeast Res. 9:1013–1028 10.1111/j.1567-1364.2009.00541.x PubMed DOI
Koning A.J., Roberts C.J., Wright R.L. 1996. Different subcellular localization of Saccharomyces cerevisiae HMG-CoA reductase isozymes at elevated levels corresponds to distinct endoplasmic reticulum membrane proliferations. Mol. Biol. Cell. 7:769–789 PubMed PMC
Kuthan M., Devaux F., Janderová B., Slaninová I., Jacq C., Palková Z. 2003. Domestication of wild Saccharomyces cerevisiae is accompanied by changes in gene expression and colony morphology. Mol. Microbiol. 47:745–754 10.1046/j.1365-2958.2003.03332.x PubMed DOI
Lambrechts M.G., Bauer F.F., Marmur J., Pretorius I.S. 1996. Muc1, a mucin-like protein that is regulated by Mss10, is critical for pseudohyphal differentiation in yeast. Proc. Natl. Acad. Sci. USA. 93:8419–8424 10.1073/pnas.93.16.8419 PubMed DOI PMC
Mukherjee P.K., Chandra J., Kuhn D.M., Ghannoum M.A. 2003. Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect. Immun. 71:4333–4340 10.1128/IAI.71.8.4333-4340.2003 PubMed DOI PMC
Nett J.E., Sanchez H., Cain M.T., Andes D.R. 2010. Genetic basis of Candida biofilm resistance due to drug-sequestering matrix glucan. J. Infect. Dis. 202:171–175 10.1086/651200 PubMed DOI PMC
Nobile C.J., Schneider H.A., Nett J.E., Sheppard D.C., Filler S.G., Andes D.R., Mitchell A.P. 2008. Complementary adhesin function in C. albicans biofilm formation. Curr. Biol. 18:1017–1024 10.1016/j.cub.2008.06.034 PubMed DOI PMC
Palková Z. 2004. Multicellular microorganisms: laboratory versus nature. EMBO Rep. 5:470–476 10.1038/sj.embor.7400145 PubMed DOI PMC
Ramage G., Bachmann S., Patterson T.F., Wickes B.L., López-Ribot J.L. 2002. Investigation of multidrug efflux pumps in relation to fluconazole resistance in Candida albicans biofilms. J. Antimicrob. Chemother. 49:973–980 10.1093/jac/dkf049 PubMed DOI
Ramsook C.B., Tan C., Garcia M.C., Fung R., Soybelman G., Henry R., Litewka A., O’Meally S., Otoo H.N., Khalaf R.A., et al. 2010. Yeast cell adhesion molecules have functional amyloid-forming sequences. Eukaryot. Cell. 9:393–404 10.1128/EC.00068-09 PubMed DOI PMC
Reynolds T.B., Fink G.R. 2001. Bakers’ yeast, a model for fungal biofilm formation. Science. 291:878–881 10.1126/science.291.5505.878 PubMed DOI
Rogers B., Decottignies A., Kolaczkowski M., Carvajal E., Balzi E., Goffeau A. 2001. The pleitropic drug ABC transporters from Saccharomyces cerevisiae. J. Mol. Microbiol. Biotechnol. 3:207–214 PubMed
Servos J., Haase E., Brendel M. 1993. Gene SNQ2 of Saccharomyces cerevisiae, which confers resistance to 4-nitroquinoline-N-oxide and other chemicals, encodes a 169 kDa protein homologous to ATP-dependent permeases. Mol. Gen. Genet. 236:214–218 10.1007/BF00277115 PubMed DOI
Sheff M.A., Thorn K.S. 2004. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast. 21:661–670 10.1002/yea.1130 PubMed DOI
Sipos G., Kuchler K. 2006. Fungal ATP-binding cassette (ABC) transporters in drug resistance & detoxification. Curr. Drug Targets. 7:471–481 10.2174/138945006776359403 PubMed DOI
Smukalla S., Caldara M., Pochet N., Beauvais A., Guadagnini S., Yan C., Vinces M.D., Jansen A., Prevost M.C., Latgé J.P., et al. 2008. FLO1 is a variable green beard gene that drives biofilm-like cooperation in budding yeast. Cell. 135:726–737 10.1016/j.cell.2008.09.037 PubMed DOI PMC
Šťovíček V., Váchová L., Kuthan M., Palková Z. 2010. General factors important for the formation of structured biofilm-like yeast colonies. Fungal Genet. Biol. 47:1012–1022 10.1016/j.fgb.2010.08.005 PubMed DOI
Tokunaga M., Kusamichi M., Koike H. 1986. Ultrastructure of outermost layer of cell wall in Candida albicans observed by rapid-freezing technique. J. Electron Microsc. (Tokyo). 35:237–246 PubMed
Uppuluri P., Chaturvedi A.K., Lopez-Ribot J.L. 2009. Design of a simple model of Candida albicans biofilms formed under conditions of flow: development, architecture, and drug resistance. Mycopathologia. 168:101–109 10.1007/s11046-009-9205-9 PubMed DOI PMC
Váchová L., Chernyavskiy O., Strachotová D., Bianchini P., Burdíková Z., Fercíková I., Kubínová L., Palková Z. 2009. Architecture of developing multicellular yeast colony: spatio-temporal expression of Ato1p ammonium exporter. Environ. Microbiol. 11:1866–1877 10.1111/j.1462-2920.2009.01911.x PubMed DOI
Verstrepen K.J., Reynolds T.B., Fink G.R. 2004. Origins of variation in the fungal cell surface. Nat. Rev. Microbiol. 2:533–540 10.1038/nrmicro927 PubMed DOI
Vopálenská I., Šťovíček V., Janderová B., Váchová L., Palková Z. 2010. Role of distinct dimorphic transitions in territory colonizing and formation of yeast colony architecture. Environ. Microbiol. 12:264–277 10.1111/j.1462-2920.2009.02067.x PubMed DOI
Wolfger H., Mahé Y., Parle-McDermott A., Delahodde A., Kuchler K. 1997. The yeast ATP binding cassette (ABC) protein genes PDR10 and PDR15 are novel targets for the Pdr1 and Pdr3 transcriptional regulators. FEBS Lett. 418:269–274 10.1016/S0014-5793(97)01382-3 PubMed DOI
Wright R. 2000. Transmission electron microscopy of yeast. Microsc. Res. Tech. 51:496–510 10.1002/1097-0029(20001215)51:6<496::AID-JEMT2>3.0.CO;2-9 PubMed DOI
Zara G., Zara S., Pinna C., Marceddu S., Budroni M. 2009. FLO11 gene length and transcriptional level affect biofilm-forming ability of wild flor strains of Saccharomyces cerevisiae. Microbiology. 155:3838–3846 10.1099/mic.0.028738-0 PubMed DOI
Non-Coding RNAs: Regulators of Stress, Ageing, and Developmental Decisions in Yeast?
Mitochondrial Retrograde Signaling Contributes to Metabolic Differentiation in Yeast Colonies
Cell Distribution within Yeast Colonies and Colony Biofilms: How Structure Develops
Glucose, Cyc8p and Tup1p regulate biofilm formation and dispersal in wild Saccharomyces cerevisiae
Long Noncoding RNAs in Yeast Cells and Differentiated Subpopulations of Yeast Colonies and Biofilms
Global changes in gene expression associated with phenotypic switching of wild yeast
Rapidly developing yeast microcolonies differentiate in a similar way to aging giant colonies
Yeast colonies: a model for studies of aging, environmental adaptation, and longevity
Reactive oxygen species in the signaling and adaptation of multicellular microbial communities