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

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

Status PubMed-not-MEDLINE Jazyk angličtina Země Nizozemsko Médium electronic-ecollection

Typ dokumentu časopisecké články, přehledy

Perzistentní odkaz   https://www.medvik.cz/link/pmid34712401
Odkazy

PubMed 34712401
PubMed Central PMC8529026
DOI 10.1016/j.csbj.2021.10.012
PII: S2001-0370(21)00434-7
Knihovny.cz E-zdroje

Single-celled yeasts form spatially structured populations - colonies and biofilms, either alone (single-species biofilms) or in cooperation with other microorganisms (mixed-species biofilms). Within populations, yeast cells develop in a coordinated manner, interact with each other and differentiate into specialized cell subpopulations that can better adapt to changing conditions (e.g. by reprogramming metabolism during nutrient deficiency) or protect the overall population from external influences (e.g. via extracellular matrix). Various omics tools together with specialized techniques for separating differentiated cells and in situ microscopy have revealed important processes and cell interactions in these structures, which are summarized here. Nevertheless, current knowledge is still only a small part of the mosaic of complexity and diversity of the multicellular structures that yeasts form in different environments. Future challenges include the use of integrated multi-omics approaches and a greater emphasis on the analysis of differentiated cell subpopulations with specific functions.

Zobrazit více v PubMed

Tarnita C.E. The ecology and evolution of social behavior in microbes. J Exp Biol. 2017;220:18–24. PubMed

West S.A., Diggle S.P., Buckling A., Gardner A., Griffin A.S. Annual Review of Ecology Evolution and Systematics, Annual Reviews: Palo Alto. 2007. The social lives of microbes; pp. 53–77. 1.

Palková Z., Váchová L. Yeast cell differentiation: Lessons from pathogenic and non-pathogenic yeasts. Semin Cell Dev Biol. 2016;57:110–119. PubMed

Vachova L., Palkova Z. How structured yeast multicellular communities live, age and die? FEMS Yeast Res. 2018;18(4):foy033. PubMed

Čáp M., Štěpánek L., Harant K., Váchová L., Palková Z. Cell differentiation within a yeast colony: metabolic and regulatory parallels with a tumor-affected organism. Mol Cell. 2012;46(4):436–448. PubMed

Maršíková J., Pavlíčková M., Wilkinson D., Váchová L., Hlaváček O., Hatáková L. The Whi2p-Psr1p/Psr2p complex regulates interference competition and expansion of cells with competitive advantage in yeast colonies. Proc Natl Acad Sci U S A. 2020;117(26):15123–15131. PubMed PMC

Maršíková J., Wilkinson D., Hlaváček O., Gilfillan G.D., Mizeranschi A., Hughes T. Metabolic differentiation of surface and invasive cells of yeast colony biofilms revealed by gene expression profiling. BMC Genomics. 2017;18(1):814. PubMed PMC

Piccirillo S., Morales R., White M.G., Smith K., Kapros T., Honigberg S.M. Cell differentiation and spatial organization in yeast colonies: role of cell-wall integrity pathway. Genetics. 2015;201(4):1427–1438. PubMed PMC

Podholová K., Plocek V., Rešetárová S., Kučerová H., Hlaváček O., Váchová L. Divergent branches of mitochondrial signaling regulate specific genes and the viability of specialized cell types of differentiated yeast colonies. Oncotarget. 2016;7(13):15299–15314. PubMed PMC

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(7):1866–1877. 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(5):679–687. PubMed PMC

Plocek V., Váchová L., Šťovíček V., Palková Z. Cell distribution within yeast colonies and colony biofilms: how structure develops. Int J Mol Sci. 2020;21(11):3873. PubMed PMC

Alves R., Barata-Antunes C., Casal M., Brown A.J.P., Van Dijck P., Paiva S. Adapting to survive: How Candida overcomes host-imposed constraints during human colonization. PLoS Pathog. 2020;16(5):e1008478. PubMed PMC

Atriwal T., Azeem K., Husain F.M., Hussain A., Khan M.N., Alajmi M.F. Mechanistic understanding of Candida albicans biofilm formation and approaches for its inhibition. Front Microbiol. 2021;12:638609. PubMed PMC

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(1):19–31. PubMed PMC

Váchová L., Hatáková L., Čáp M., Pokorná M., Palková Z. Rapidly developing yeast microcolonies differentiate in a similar way to aging giant colonies. Oxid Med Cell Longev. 2013;2013:1–9. PubMed PMC

Palková Z., Janderová B., Gabriel Jir̂í, Zikánová B., Pospíŝek M., Forstová J. Ammonia mediates communication between yeast colonies. Nature. 1997;390(6659):532–536. PubMed

Palkova Z., Forstova J. Yeast colonies synchronise their growth and development. J Cell Sci. 2000;113(11):1923–1928. PubMed

Vachova L., Palkova Z. Physiological regulation of yeast cell death in multicellular colonies is triggered by ammonia. J Cell Biol. 2005;169(5):711–717. PubMed PMC

Palková Z., Devaux F., R̆ic̆icová M., Mináriková L., Le Crom S., Jacq C. Ammonia pulses and metabolic oscillations guide yeast colony development. Mol Biol Cell. 2002;13(11):3901–3914. PubMed PMC

Vachova L., Kucerova H., Devaux F., Ulehlova M., Palkova Z. Metabolic diversification of cells during the development of yeast colonies. Environ Microbiol. 2009;11(2):494–504. PubMed

Plocek V., Fadrhonc K., Maršíková J., Váchová L., Pokorná A., Hlaváček O. Mitochondrial retrograde signaling contributes to metabolic differentiation in yeast colonies. Int J Mol Sci. 2021;22(11):5597. PubMed PMC

Wilkinson D., Marsikova J., Hlavacek O., Gilfillan G.D., Jezkova E., Aaløkken R. Transcriptome remodeling of differentiated cells during chronological ageing of yeast colonies: new insights into metabolic differentiation. Oxid Med Cell Longev. 2018;2018 PubMed PMC

DeBerardinis R.J., Cheng T. Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene. 2010;29(3):313–324. PubMed PMC

Čáp M., Váchová L., Palková Z. Longevity of U cells of differentiated yeast colonies grown on respiratory medium depends on active glycolysis. Cell Cycle. 2015;14(21):3488–3497. PubMed PMC

Traven A., Jänicke A., Harrison P., Swaminathan A., Seemann T., Beilharz T.H. Transcriptional profiling of a yeast colony provides new insight into the heterogeneity of multicellular fungal communities. PLoS ONE. 2012;7(9):e46243. PubMed PMC

Alves R., Kastora S.L., Gomes-Gonçalves A., Azevedo N., Rodrigues C.F., Silva S. Transcriptional responses of Candida glabrata biofilm cells to fluconazole are modulated by the carbon source. NPJ Biofilms Microbiomes. 2020;6(1):4. PubMed PMC

Mancera E., Nocedal I., Hammel S., Gulati M., Mitchell K.F., Andes D.R. Evolution of the complex transcription network controlling biofilm formation in Candida species. Elife. 2021;10:e64682. PubMed PMC

Št’ovíček V., Váchová L., Kuthan M., Palková Z. General factors important for the formation of structured biofilm-like yeast colonies. Fungal Genet Biol. 2010;47(12):1012–1022. 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(1):7. PubMed PMC

Reynolds T.B. Going with the Flo: the role of Flo11-dependent and independent interactions in yeast mat formation. J Fungi. 2018;4(4):132. PubMed PMC

Tek E.L., Sundstrom J.F., Gardner J.M., Oliver S.G., Jiranek V. Evaluation of the ability of commercial wine yeasts to form biofilms (mats) and adhere to plastic: implications for the microbiota of the winery environment. FEMS Microbiol Ecol. 2018;94(2):fix188. PubMed

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(3):745–754. PubMed

Stovicek V., Vachova L., Begany M., Wilkinson D., Palkova Z. Global changes in gene expression associated with phenotypic switching of wild yeast. BMC Genomics. 2014;15:136. PubMed PMC

Voordeckers K., De Maeyer D., van der Zande E., Vinces M.D., Meert W., Cloots L. Identification of a complex genetic network underlying Saccharomyces cerevisiae colony morphology. Mol Microbiol. 2012;86(1):225–239. PubMed 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(1):264–277. PubMed

Brückner S., Mösch H.U. Choosing the right lifestyle: adhesion and development in Saccharomyces cerevisiae. FEMS Microbiol Rev. 2012;36(1):25–58. PubMed

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(7) PubMed PMC

Chow J., Starr I., Jamalzadeh S., Muniz O., Kumar A., Gokcumen O., Ferkey D.M., Cullen P.J. Filamentation regulatory pathways control adhesion-dependent surface responses in yeast. Genetics. 2019;212:667–690. PubMed PMC

Araujo D., Henriques M., Silva S. Portrait of Candida species biofilm regulatory network genes. Trends Microbiol. 2017;25(1):62–75. PubMed

Gulati M., Nobile C.J. Candida albicans biofilms: development, regulation, and molecular mechanisms. Microbes Infect. 2016;18(5):310–321. PubMed PMC

Li P., Seneviratne C.J., Alpi E., Vizcaino J.A., Jin L. Delicate metabolic control and coordinated stress response critically determine antifungal tolerance of Candida albicans biofilm persisters. Antimicrob Agents Chemother. 2015;59(10):6101–6112. PubMed PMC

Wuyts J., Van Dijck P., Holtappels M. Fungal persister cells: the basis for recalcitrant infections? PLoS Pathog. 2018;14(10) PubMed PMC

Tsui C., Kong E.F., Jabra-Rizk M.A. Pathogenesis of Candida albicans biofilm. Pathog Dis. 2016;74(4):ftw018. PubMed PMC

Wall G., Montelongo-Jauregui D., Vidal Bonifacio B., Lopez-Ribot J.L., Uppuluri P. Candida albicans biofilm growth and dispersal: contributions to pathogenesis. Curr Opin Microbiol. 2019;52:1–6. PubMed PMC

Nobile C.J., Mitchell A.P. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr Biol. 2005;15(12):1150–1155. PubMed

Yang L., Zheng C., Chen Y., Ying H. FLO genes family and transcription factor MIG1 Regulate Saccharomyces cerevisiae biofilm formation during immobilized fermentation. Front Microbiol. 1860;2018:9. PubMed PMC

Fox E.P., Bui C.K., Nett J.E., Hartooni N., Mui M.C., Andes D.R., Nobile C.J., Johnson A.D. An expanded regulatory network temporally controls Candida albicans biofilm formation. Mol Microbiol. 2015;96(6):1226–1239. PubMed PMC

He J., Kim D., Zhou X., Ahn S.J., Burne R.A., Richards V.P. RNA-Seq reveals enhanced sugar metabolism in Streptococcus mutans co-cultured with Candida albicans within mixed-species biofilms. Front Microbiol. 2017;8:1036. PubMed PMC

Vila T., Kong E.F., Montelongo-Jauregui D., Van Dijck P., Shetty A.C., McCracken C. Therapeutic implications of C. albicans-S. aureus mixed biofilm in a murine subcutaneous catheter model of polymicrobial infection. Virulence. 2021;12(1):835–851. PubMed PMC

Zarnowski R., Westler W.M., Lacmbouh G.A., Marita J.M., Bothe J.R., Bernhardt J. Novel entries in a fungal biofilm matrix encyclopedia. MBio. 2014;5(4):e01333–14. PubMed PMC

Nett J.E., Zarnowski R., Cabezas-Olcoz J., Brooks E.G., Bernhardt J., Marchillo K., Mosher D.F., Andes D.R. Host contributions to construction of three device-associated Candida albicans biofilms. Infect Immun. 2015;83(12):4630–4638. PubMed PMC

Satala D., Karkowska-Kuleta J., Zelazna A., Rapala-Kozik M., Kozik A. Moonlighting Proteins at the Candidal cell surface. Microorganisms. 2020;8(7):1046. PubMed PMC

Zarnowski R., Sanchez H., Covelli A.S., Dominguez E., Jaromin A., Bernhardt J. Candida albicans biofilm-induced vesicles confer drug resistance through matrix biogenesis. PLoS Biol. 2018;16(10) PubMed PMC

Liebana-Jordan M., Brotons B., Falcon-Perez J.M., Gonzalez E. Extracellular vesicles in the fungi kingdom. Int J Mol Sci. 2021;22:7221. PubMed PMC

Rizzo J., Taheraly A., Janbon G. Structure, composition and biological properties of fungal extracellular vesicles. microLife. 2021;2:uqab009. PubMed PMC

Bleackley M.R., Dawson C.S., Anderson M.A. Fungal extracellular vesicles with a focus on proteomic analysis. Proteomics. 2019;19(8) PubMed

Nobile C.J., Fox E.P., Nett J.E., Sorrells T.R., Mitrovich Q.M., Hernday A.D. A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell. 2012;148(1–2):126–138. PubMed PMC

Finkel J.S., Xu W., Huang D., Hill E.M., Desai J.V., Woolford C.A. Portrait of Candida albicans adherence regulators. PLoS Pathog. 2012;8(2) PubMed PMC

Holland L.M., Schroder M.S., Turner S.A., Taff H., Andes D., Grozer Z. Comparative phenotypic analysis of the major fungal pathogens Candida parapsilosis and Candida albicans. PLoS Pathog. 2014;10(9) PubMed PMC

d'Enfert C., Janbon G. Biofilm formation in Candida glabrata: What have we learnt from functional genomics approaches? FEMS Yeast Res. 2016;16(1):fov111. PubMed

Bojsen R.K., Andersen K.S., Regenberg B. Saccharomyces cerevisiae - a model to uncover molecular mechanisms for yeast biofilm biology. FEMS Immunol Med Microbiol. 2012;65(2):169–182. PubMed

Reynolds T.B., Fink G.R. Bakers' yeast, a model for fungal biofilm formation. Science. 2001;291(5505):878–881. PubMed

Andersen S.K., Bojsen R, Gro L, Sorensen Rejkjaer, Nielsen Weiss M, Lisby M, Folkesson A, Regenberg B. Genetic basis for Saccharomyces cerevisiae biofilm in liquid medium. G3 (Bethesda) 2014;4(9):1671–1680. PubMed PMC

Yang L., Zheng C., Chen Y., Shi X., Ying Z., Ying H. Nitric oxide increases biofilm formation in Saccharomyces cerevisiae by activating the transcriptional factor Mac1p and thereby regulating the transmembrane protein Ctr1. Biotechnol Biofuels. 2019;12:30. PubMed PMC

Uppuluri P., Acosta Zaldivar M., Anderson M.Z., Dunn M.J., Berman J., Lopez Ribot J.L. Candida albicans dispersed cells are developmentally distinct from biofilm and planktonic cells. MBio. 2018;9(4):e01338–18. PubMed PMC

Ponde N.O., Lortal L., Ramage G., Naglik J.R., Richardson J.P. Candida albicans biofilms and polymicrobial interactions. Crit Rev Microbiol. 2021;47(1):91–111. PubMed PMC

Ellepola K., Truong T., Liu Y., Lin Q., Lim T.K., Lee Y.M. Multi-omics analyses reveal synergistic carbohydrate metabolism in Streptococcus mutans - Candida albicans mixed - species biofilms. Infect Immun. 2019;87(10):e00339–19. PubMed PMC

Legras J.L., Moreno-Garcia J., Zara S., Zara G., Garcia-Martinez T., Mauricio J.C. Flor Yeast: New perspectives beyond wine aging. Front Microbiol. 2016;7:503. PubMed 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(6):2934–2939. PubMed PMC

Moreno-Garcia J., Garcia-Martinez T., Moreno J., Mauricio J.C. Proteins involved in flor yeast carbon metabolism under biofilm formation conditions. Food Microbiol. 2015;46:25–33. PubMed

Moreno-Garcia J., Garcia-Martinez T., Moreno J., Millan M.C., Mauricio J.C. A proteomic and metabolomic approach for understanding the role of the flor yeast mitochondria in the velum formation. Int J Food Microbiol. 2014;172:21–29. PubMed

Moreno-Garcia J., Mauricio J.C., Moreno J., Garcia-Martinez T. Differential proteome analysis of a flor yeast strain under biofilm formation. Int J Mol Sci. 2017;18(4):720. PubMed PMC

Zarnowski R., Sanchez H., Andreu C., Andes D., Del Olmo M.L. Formation and characterization of biofilms formed by salt-tolerant yeast strains in seawater-based growth medium. Appl Microbiol Biotechnol. 2021;105(6):2411–2426. PubMed PMC

Freimoser F.M., Rueda-Mejia M.P., Tilocca B., Migheli Q. Biocontrol yeasts: mechanisms and applications. World J Microbiol Biotechnol. 2019;35(10):154. PubMed PMC

Giobbe S., Marceddu S., Scherm B., Zara G., Mazzarello V.L., Budroni M., Migheli Q. The strange case of a biofilm-forming strain of Pichia fermentans, which controls Monilinia brown rot on apple but is pathogenic on peach fruit. FEMS Yeast Res. 2007;7(8):1389–1398. PubMed

Nadal-Ribelles M., Islam S., Wei W., Latorre P., Nguyen M., de Nadal E. Sensitive high-throughput single-cell RNA-seq reveals within-clonal transcript correlations in yeast populations. Nat Microbiol. 2019;4(4):683–692. PubMed PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...