The characteristics of differentiated yeast subpopulations depend on their lifestyle and available nutrients

. 2024 Feb 14 ; 14 (1) : 3681. [epub] 20240214

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38355943

Grantová podpora
19-09381S Grantová Agentura České Republiky
19-09381S Grantová Agentura České Republiky

Odkazy

PubMed 38355943
PubMed Central PMC10866891
DOI 10.1038/s41598-024-54300-9
PII: 10.1038/s41598-024-54300-9
Knihovny.cz E-zdroje

Yeast populations can undergo diversification during their growth and ageing, leading to the formation of different cell-types. Differentiation into two major subpopulations, differing in cell size and density and exhibiting distinct physiological and metabolic properties, was described in planktonic liquid cultures and in populations of colonies growing on semisolid surfaces. Here, we compare stress resistance, metabolism and expression of marker genes in seven differentiated cell subpopulations emerging during cultivation in liquid fermentative or respiratory media and during colony development on the same type of solid media. The results show that the more-dense cell subpopulations are more stress resistant than the less-dense subpopulations under all cultivation conditions tested. On the other hand, respiratory capacity, enzymatic activities and marker gene expression differed more between subpopulations. These characteristics are more influenced by the lifestyle of the population (colony vs. planktonic cultivation) and the medium composition. Only in the population growing in liquid respiratory medium, two subpopulations do not form as in the other conditions tested, but all cells exhibit a range of characteristics of the more-dense subpopulations. This suggests that signals for cell differentiation may be triggered by prior metabolic reprogramming or by an unknown signal from the structured environment in the colony.

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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;46:436–448. doi: 10.1016/j.molcel.2012.04.001. PubMed DOI

Čáp M, Váchová L, Palková Z. Yeast colony survival depends on metabolic adaptation and cell differentiation rather than on stress defense. J. Biol. Chem. 2009;284:32572–32581. doi: 10.1074/jbc.M109.022871. PubMed DOI PMC

Benbadis L, Cot M, Rigoulet M, Francois J. Isolation of two cell populations from yeast during high-level alcoholic fermentation that resemble quiescent and nonquiescent cells from the stationary phase on glucose. FEMS Yeast Res. 2009;9:1172–1186. doi: 10.1111/j.1567-1364.2009.00553.x. PubMed DOI

Maršíková J, et al. Metabolic differentiation of surface and invasive cells of yeast colony biofilms revealed by gene expression profiling. BMC Genom. 2017;18:814. doi: 10.1186/s12864-017-4214-4. PubMed DOI PMC

Traven A, et al. Transcriptional profiling of a yeast colony provides new insight into the heterogeneity of multicellular fungal communities. PLoS ONE. 2012;7:e46243. doi: 10.1371/journal.pone.0046243. PubMed DOI PMC

Allen C, et al. Isolation of quiescent and nonquiescent cells from yeast stationary-phase cultures. J. Cell Biol. 2006;174:89–100. doi: 10.1083/jcb.200604072. PubMed DOI PMC

Svenkrtova A, et al. Stratification of yeast cells during chronological aging by size points to the role of trehalose in cell vitality. Biogerontology. 2016;17:395–408. doi: 10.1007/s10522-015-9625-5. PubMed DOI 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. doi: 10.1155/2013/102485. PubMed DOI 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;14:3488–3497. doi: 10.1080/15384101.2015.1093706. PubMed DOI PMC

Gray JV, et al. ‘Sleeping beauty’: Quiescence in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 2004;68:187–206. doi: 10.1128/MMBR.68.2.187-206.2004. PubMed DOI PMC

François J, Parrou JL. Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol. Rev. 2001;25:125–145. doi: 10.1111/j.1574-6976.2001.tb00574.x. PubMed DOI

Davidson GS, et al. The proteomics of quiescent and nonquiescent cell differentiation in yeast stationary-phase cultures. Mol. Biol. Cell. 2011;22:988–998. doi: 10.1091/mbc.e10-06-0499. PubMed DOI PMC

Sagot I, Laporte D. The cell biology of quiescent yeast - a diversity of individual scenarios. J. Cell Sci. 2019;132:jcs213025. doi: 10.1242/jcs.213025. PubMed DOI

Sun S, Gresham D. Cellular quiescence in budding yeast. Yeast. 2021;38:12–29. doi: 10.1002/yea.3545. PubMed DOI PMC

Klosinska MM, Crutchfield CA, Bradley PH, Rabinowitz JD, Broach JR. Yeast cells can access distinct quiescent states. Genes Dev. 2011;25:336–349. doi: 10.1101/gad.2011311. PubMed DOI PMC

Boer VM, Crutchfield CA, Bradley PH, Botstein D, Rabinowitz JD. Growth-limiting intracellular metabolites in yeast growing under diverse nutrient limitations. Mol. Biol. Cell. 2010;21:198–211. doi: 10.1091/mbc.e09-07-0597. PubMed DOI PMC

Váchová L, Čáp M, Palková Z. Yeast colonies: A model for studies of aging, environmental adaptation, and longevity. Oxid. Med. Cell. Longev. 2012;2012:1–8. doi: 10.1155/2012/601836. PubMed DOI PMC

Shi L, Sutter BM, Ye X, Tu BP. Trehalose is a key determinant of the quiescent metabolic state that fuels cell cycle progression upon return to growth. Mol. Biol. Cell. 2010;21:1982–1990. doi: 10.1091/mbc.e10-01-0056. PubMed DOI PMC

Li L, et al. Key events during the transition from rapid growth to quiescence in budding yeast require posttranscriptional regulators. Mol. Biol. Cell. 2013;24:3697–3709. doi: 10.1091/mbc.e13-05-0241. PubMed DOI PMC

Lillie SH, Pringle JR. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: Responses to nutrient limitation. J. Bacteriol. 1980;143:1384–1394. doi: 10.1128/jb.143.3.1384-1394.1980. PubMed DOI PMC

de Assis LJ, Zingali RB, Masuda CA, Rodrigues SP, Montero-Lomelí M. Pyruvate decarboxylase activity is regulated by the Ser/Thr protein phosphatase Sit4p in the yeast Saccharomyces cerevisiae. FEMS Yeast Res. 2013;13:518–528. doi: 10.1111/1567-1364.12052. PubMed DOI

Orlandi I, Ronzulli R, Casatta N, Vai M. Ethanol and acetate acting as carbon/energy sources negatively affect yeast chronological aging. Oxid. Med. Cell. Longev. 2013 doi: 10.1155/2013/802870. PubMed DOI PMC

Goldberg AA, et al. Effect of calorie restriction on the metabolic history of chronologically aging yeast. Exp. Gerontol. 2009;44:555–571. doi: 10.1016/j.exger.2009.06.001. PubMed DOI

Burtner CR, Murakami CJ, Kennedy BK, Kaeberlein M. A molecular mechanism of chronological aging in yeast. Cell Cycle. 2009;8:1256–1270. doi: 10.4161/cc.8.8.8287. PubMed DOI PMC

Wei M, et al. Tor1/Sch9-regulated carbon source substitution is as effective as calorie restriction in life span extension. PLoS Genet. 2009;5:e1000467. doi: 10.1371/journal.pgen.1000467. PubMed DOI PMC

Kwon YY, et al. Long-living budding yeast cell subpopulation induced by ethanol/acetate and respiration. J. Gerontol. Ser. A. 2020;75:1448–1456. doi: 10.1093/gerona/glz202. PubMed DOI

Sun S, Baryshnikova A, Brandt N, Gresham D. Genetic interaction profiles of regulatory kinases differ between environmental conditions and cellular states. Mol. Syst. Biol. 2020;16:e9167. doi: 10.15252/msb.20199167. PubMed DOI PMC

Smith DL, Maharrey CH, Carey CR, White RA, Hartman JL. Gene-nutrient interaction markedly influences yeast chronological lifespan. Exp. Gerontol. 2016;86:113–123. doi: 10.1016/j.exger.2016.04.012. PubMed DOI PMC

Apweiler E, et al. Yeast glucose pathways converge on the transcriptional regulation of trehalose biosynthesis. BMC Genom. 2012;13:1–14. doi: 10.1186/1471-2164-13-239. PubMed DOI PMC

Kyryakov P, et al. Caloric restriction extends yeast chronological lifespan by altering a pattern of age-related changes in trehalose concentration. Front. Physiol. 2012;3:29404. doi: 10.3389/fphys.2012.00256. PubMed DOI PMC

Aragon AD, et al. Characterization of differentiated quiescent and nonquiescent cells in yeast stationary-phase cultures. Mol. Biol. Cell. 2008;19:1271–1280. doi: 10.1091/mbc.e07-07-0666. PubMed DOI PMC

Palková Z, Wilkinson D, Váchová L. Aging and differentiation in yeast populations: Elders with different properties and functions. FEMS Yeast Res. 2014;14:96–108. doi: 10.1111/1567-1364.12103. PubMed DOI

Correia-Melo C, et al. Cell–cell metabolite exchange creates a pro-survival metabolic environment that extends lifespan. Cell. 2023;186:63–79.e21. doi: 10.1016/j.cell.2022.12.007. PubMed DOI

Kamrad S, et al. Metabolic heterogeneity and cross-feeding within isogenic yeast populations captured by DILAC. Nat. Microbiol. 2023;8:441–454. doi: 10.1038/s41564-022-01304-8. PubMed DOI PMC

Váchová L, Palková Z. How structured yeast multicellular communities live, age and die? FEMS Yeast Res. 2018;18:foy033. doi: 10.1093/femsyr/foy033. PubMed DOI

Podholová K, et al. Divergent branches of mitochondrial signaling regulate specific genes and the viability of specialized cell types of differentiated yeast colonies. Oncotarget. 2016;7:15299–15314. doi: 10.18632/oncotarget.8084. PubMed DOI PMC

Sheff MA, Thorn KS. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast. 2004;21:661–670. doi: 10.1002/yea.1130. PubMed DOI

Srere PA. Citrate synthase: EC 4.1.3.7 Citrate oxaloacetate-lyase (CoA-acetylating) Methods Enzymol. 1969;13:3–11. doi: 10.1016/0076-6879(69)13005-0. DOI

Illingworth JA. Purification of yeast isocitrate dehydrogenase. Biochem. J. 1972;129:1119–1124. doi: 10.1042/bj1291119. PubMed DOI PMC

Grisolia S, Quijada CL, Fernandez M. Glutamate dehydrogenase from yeast and from animal tissues. BBA Enzymol. Sub. 1964;81:61–70.

Frieden C, Bock RM, Alberty RA. Studies of the enzyme fumarase. II.1 isolation and physical properties of crystalline enzyme. J. Am. Chem. Soc. 1954;76:2482–2484. doi: 10.1021/ja01638a052. DOI

Bergmeyer H, Gawehn K, Grassl M. Malate dehydrogenase. In: Bergmeyer HU, Gawehn K, editors. Methods of enzymatic analysis. Berlin: Academic Press; 1974. pp. 485–486.

Chell RM, Sundaram TK, Wilkinson AE. Isolation and characterization of isocitrate lyase from a thermophilic Bacillus sp. Biochem. J. 1978;173:165. doi: 10.1042/bj1730165. PubMed DOI PMC

Masuko T, et al. Carbohydrate analysis by a phenol-sulfuric acid method in microplate format. Anal. Biochem. 2005;339:69–72. doi: 10.1016/j.ab.2004.12.001. PubMed DOI

Řičicová M, Kučerová H, Váchová L, Palková Z. Association of putative ammonium exporters Ato with detergent-resistant compartments of plasma membrane during yeast colony development: pH affects Ato1p localisation in patches. Biochim. Biophys. Acta Biomembr. 2007;1768:1170–1178. doi: 10.1016/j.bbamem.2007.02.011. PubMed DOI

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Differential stability of Gcn4p controls its cell-specific activity in differentiated yeast colonies

. 2024 May 08 ; 15 (5) : e0068924. [epub] 20240416

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