Flo11p, drug efflux pumps, and the extracellular matrix cooperate to form biofilm yeast colonies

. 2011 Sep 05 ; 194 (5) : 679-87. [epub] 20110829

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid21875945

Grantová podpora
Howard Hughes Medical Institute - United States

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.

Zobrazit více v PubMed

Al-Fattani M.A., Douglas L.J. 2006. Biofilm matrix of PubMed DOI

Baillie G.S., Douglas L.J. 2000. Matrix polymers of PubMed DOI

Balzi E., Chen W., Ulaszewski S., Capieaux E., Goffeau A. 1987. The multidrug resistance gene PubMed

Balzi E., Wang M., Leterme S., Van Dyck L., Goffeau A. 1994. PubMed

Bayly J.C., Douglas L.M., Pretorius I.S., Bauer F.F., Dranginis A.M. 2005. Characteristics of Flo11-dependent flocculation in PubMed DOI

Beauvais A., Loussert C., Prevost M.C., Verstrepen K., Latgé J.P. 2009. Characterization of a biofilm-like extracellular matrix in 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. PubMed DOI

Douglas L.M., Li L., Yang Y., Dranginis A.M. 2007. Expression and characterization of the flocculin Flo11/Muc1, a 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 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 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 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. 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 PubMed DOI

Koning A.J., Roberts C.J., Wright R.L. 1996. Different subcellular localization of PubMed PMC

Kuthan M., Devaux F., Janderová B., Slaninová I., Jacq C., Palková Z. 2003. Domestication of wild 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 PubMed DOI PMC

Nett J.E., Sanchez H., Cain M.T., Andes D.R. 2010. Genetic basis of 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 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 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 PubMed

Servos J., Haase E., Brendel M. 1993. Gene PubMed DOI

Sheff M.A., Thorn K.S. 2004. Optimized cassettes for fluorescent protein tagging in 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. 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 PubMed

Uppuluri P., Chaturvedi A.K., Lopez-Ribot J.L. 2009. Design of a simple model of 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 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. PubMed DOI

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Spatial structure of yeast biofilms and the role of cell adhesion across different media

. 2025 Dec ; 10 () : 100306. [epub] 20250714

Cell differentiation, aging, and death in spatially organized yeast communities: mechanisms and consequences

. 2025 Sep ; 32 (9) : 1557-1569. [epub] 20250329

Hostile Environments: Modifying Surfaces to Block Microbial Adhesion and Biofilm Formation

. 2025 May 23 ; 15 (6) : . [epub] 20250523

Non-Coding RNAs: Regulators of Stress, Ageing, and Developmental Decisions in Yeast?

. 2024 Mar 29 ; 13 (7) : . [epub] 20240329

Spatially structured yeast communities: Understanding structure formation and regulation with omics tools

. 2021 ; 19 () : 5613-5621. [epub] 20211009

Mitochondrial Retrograde Signaling Contributes to Metabolic Differentiation in Yeast Colonies

. 2021 May 25 ; 22 (11) : . [epub] 20210525

Cell Distribution within Yeast Colonies and Colony Biofilms: How Structure Develops

. 2020 May 29 ; 21 (11) : . [epub] 20200529

Glucose, Cyc8p and Tup1p regulate biofilm formation and dispersal in wild Saccharomyces cerevisiae

. 2020 Feb 13 ; 6 (1) : 7. [epub] 20200213

Diverse roles of Tup1p and Cyc8p transcription regulators in the development of distinct types of yeast populations

. 2019 Feb ; 65 (1) : 147-151. [epub] 20180906

Cyc8p and Tup1p transcription regulators antagonistically regulate Flo11p expression and complexity of yeast colony biofilms

. 2018 Jul ; 14 (7) : e1007495. [epub] 20180702

Long Noncoding RNAs in Yeast Cells and Differentiated Subpopulations of Yeast Colonies and Biofilms

. 2018 ; 2018 () : 4950591. [epub] 20180325

Metabolic differentiation of surface and invasive cells of yeast colony biofilms revealed by gene expression profiling

. 2017 Oct 23 ; 18 (1) : 814. [epub] 20171023

Global changes in gene expression associated with phenotypic switching of wild yeast

. 2014 Feb 17 ; 15 () : 136. [epub] 20140217

Rapidly developing yeast microcolonies differentiate in a similar way to aging giant colonies

. 2013 ; 2013 () : 102485. [epub] 20130721

Yeast colonies: a model for studies of aging, environmental adaptation, and longevity

. 2012 ; 2012 () : 601836. [epub] 20120813

Reactive oxygen species in the signaling and adaptation of multicellular microbial communities

. 2012 ; 2012 () : 976753. [epub] 20120701

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...