Life-history strategies and carbon metabolism gene dosage in the Nakaseomyces yeasts
Abstract
The Nakaseomyces clade consists of a group of six hemiascomyceteous yeasts (Candida glabrata, Nakaseomyces delphensis, C. nivarensis, C. bracarensis, C. castelli, N. bacillisporus), phylogenetically close to the yeast Saccharomyces cerevisiae, their representative being the well-known pathogenic yeast C. glabrata. Four species had been previously examined for their carbon assimilation properties and found to have similar properties to S. cerevisiae (repression of respiration in high glucose-i.e. Crabtree positivity-and being a facultative anaerobe). We examined here the complete set of the six species for their carbon metabolic gene content. We also measured different metabolic and life-history traits (glucose consumption rate, population growth rate, carrying capacity, cell size, cell and biomass yield). We observed deviations from the glycolytic gene redundancy observed in S. cerevisiae presumed to be an important property for the Crabtree positivity, especially for the two species C. castelli and N. bacillisporus which frequently have only one gene copy, but different life strategies. Therefore, we show that the decrease in carbon metabolic gene copy cannot be simply associated with a reduction of glucose consumption rate and can be counterbalanced by other beneficial genetic variations.
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C. glabrata is a facultatively anaerobic, crabtree-positive yeast which prefers fermentation over respiration in the presence of oxygen.
“C. glabrata is a facultatively anaerobic, crabtree-positive yeast which prefers fermentation over respiration in the presence of oxygen [110,111].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [111]
Cites
Basic local alignment search tool
Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990) · Journal of Molecular Biology · doi:10.1006/jmbi.1990.9999 · Cited by 98,669 · see citing works
Phylogeny.fr: robust phylogenetic analysis for the non-specialist
Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J.-F., Guindon, S., Lefort, V., Lescot, M., et al. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn180 · Cited by 4,700 · see citing works
Kurtzman, C. P., & Lodder, J. (1972) · Mycologia · doi:10.2307/3758036 · Cited by 3,441 · see citing works
The evolution of gene duplications: classifying and distinguishing between models
Innan, H., & Kondrashov, F. (2010) · Nature reviews genetics · doi:10.1038/nrg2689 · Cited by 1,320 · see citing works
How did Saccharomyces evolve to become a good brewer?
Piškur, J., Rozpędowska, E., Poláková, S., Merico, A., & Compagno, C. (2006) · Trends in Genetics · doi:10.1016/j.tig.2006.02.002 · Cited by 514 · see citing works
Gresham, D., Desai, M. M., Tucker, C. M., Jenq, H. T., Pai, D. A., Ward, A., DeSevo, C. G., Botstein, D., & Dunham, M. J. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000303 · Cited by 482 · see citing works
The Yeasts, a Taxonomic Study, 5th ed
Kurtzman, C. P., Fell, J. W., & Boekhout, T. (2011) · Data Archiving and Networked Services (DANS) · Cited by 447 · see citing works
The molecular genetics of hexose transport in yeasts
Boles, E., & Hollenberg, C. P. (1997) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.1997.tb00346.x · Cited by 425 · see citing works
Brown, C. J., Todd, K., & Rosenzweig, R. F. (1998) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026009 · Cited by 307 · see citing works
Resource competition and social conflict in experimental populations of yeast
MacLean, R. C., & Gudelj, I. (2006) · Nature · doi:10.1038/nature04624 · Cited by 285 · see citing works
Fermentative lifestyle in yeasts belonging to the Saccharomyces complex
Merico, A., Sulo, P., Piškur, J., & Compagno, C. (2007) · FEBS Journal · doi:10.1111/j.1742-4658.2007.05645.x · Cited by 245 · see citing works
Carbohydrate and energy-yielding metabolism in non-conventional yeasts: Figure 1
Flores, C., Rodrı́guez, C., Petit, T., & Gancedo, C. (2000) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2000.tb00553.x · Cited by 227 · see citing works
Increased glycolytic flux as an outcome of whole-genome duplication in yeast
Conant, G. C., & Wolfe, K. H. (2007) · Molecular Systems Biology · doi:10.1038/msb4100170 · Cited by 222 · see citing works
Hagman, A., Säll, T., Compagno, C., & Piskur, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068734 · Cited by 219 · see citing works
Comparative genomics of emerging pathogens in the Candida glabrata clade.
Gabaldón, T., Martin, T., Marcet-Houben, M., Durrens, P., Bolotin-Fukuhara, M., Lespinet, O., Arnaise, S., Boisnard, S., Aguileta, G., Atanasova, R., et al. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-623 · Cited by 198 · see citing works
Self-citationTilloy, V., Ortiz-Julien, A., & Dequin, S. (2014) · Applied and Environmental Microbiology · doi:10.1128/aem.03710-13 · Cited by 185 · see citing works
Cormack, B. P., & Falkow, S. (1999) · Genetics · doi:10.1093/genetics/151.3.979 · Cited by 180 · see citing works
Alcoba-Flórez, J., Méndez-Álvarez, S., Cano, J., Guarro, J., Pérez-Roth, E., & Arévalo, M. D. P. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.8.4107-4111.2005 · Cited by 160 · see citing works
Daniel, H., Lachance, M., & Kurtzman, C. P. (2014) · Antonie van Leeuwenhoek · doi:10.1007/s10482-014-0170-z · Cited by 155 · see citing works
Roetzer, A., Gabaldón, T., & Schüller, C. (2011) · FEMS Microbiology Letters · doi:10.1111/j.1574-6968.2010.02102.x · Cited by 154 · see citing works
Bianchi, M. M., Tizzani, L., Destruelle, M., Frontali, L., & Wésolowski‐Louvel, M. (1996) · Molecular Microbiology · doi:10.1046/j.1365-2958.1996.346875.x · Cited by 126 · see citing works
Regulation of primary carbon metabolism in Kluyveromyces lactis
Breunig, K. D., Bolotin‐Fukuhara, M., Bianchi, M. M., Bourgarel, D., Falcone, C., Ferrero, I., Frontali, L., Goffrini, P., Krijger, J., Mazzoni, C., et al. (2000) · Enzyme and Microbial Technology · doi:10.1016/s0141-0229(00)00170-8 · Cited by 110 · see citing works
Self-citationRespirofermentative metabolism in Kluyveromyces lactis:
González-Siso, M.-I., Freire-Picos, M. Á., Ramil, E., González‐Domínguez, M., Torres, A. M. R., & Cerdán, M. E. (2000) · Enzyme and Microbial Technology · doi:10.1016/s0141-0229(00)00161-7 · Cited by 107 · see citing works
Schemes of flux control in a model of Saccharomyces cerevisiae glycolysis
Pritchard, L., & Kell, D. B. (2002) · European Journal of Biochemistry · doi:10.1046/j.1432-1033.2002.03055.x · Cited by 104 · see citing works
Pacheco, A., Talaia, G., Sá-Pessoa, J., Bessa, D., Gonçalves, M. J., Moreira, R., Paiva, S., Casal, M., & Queirós, O. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2012.00790.x · Cited by 104 · see citing works
de Smidt, O., du Preez, J. C., & Albertyn, J. (2011) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00760.x · Cited by 99 · see citing works
Glucose transport in the yeastKluyveromyces lactis
Chen, X. J., Wésolowski‐Louvel, M., & Fukuhara, H. (1992) · Molecular and General Genetics MGG · doi:10.1007/bf00587566 · Cited by 97 · see citing works
Glucose uptake in Kluyveromyces lactis: role of the HGT1 gene in glucose transport
Billard, P., Ménart, S., Blaisonneau, J., Bolotin‐Fukuhara, M., Fukuhara, H., & Wésolowski‐Louvel, M. (1996) · Journal of Bacteriology · doi:10.1128/jb.178.20.5860-5866.1996 · Cited by 95 · see citing works
Self-citationEvolutionary Genomics: Yeasts Accelerate beyond BLAST
Wolfe, K. H. (2004) · Current Biology · doi:10.1016/j.cub.2004.05.015 · Cited by 89 · see citing works
Lin, Z., & Li, W. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq184 · Cited by 89 · see citing works
Fukuhara, H. (2003) · FEMS Yeast Research · doi:10.1016/s1567-1356(03)00112-0 · Cited by 79 · see citing works
Spor, A., Kvitek, D. J., Nidelet, T., Martin, J., Legrand, J., Dillmann, C., Bourgais, A., de Vienne, D., Sherlock, G., & Sicard, D. (2013) · Evolution · doi:10.1111/evo.12302 · Cited by 79 · see citing works
Self-citationA phosphoglucose isomerase gene is involved in the Rag phenotype of the yeast Kluyveromyces lactis
Goffrini, P., Wésolowski‐Louvel, M., & Ferrero, I. (1991) · Molecular and General Genetics MGG · doi:10.1007/bf00260633 · Cited by 78 · see citing works
Constraints on microbial metabolism drive evolutionary diversification in homogeneous environments
Gudelj, I., Beardmore, R., Arkin, S. S., & MacLean, R. C. (2007) · Journal of Evolutionary Biology · doi:10.1111/j.1420-9101.2007.01376.x · Cited by 66 · see citing works
Kok, S., Nijkamp, J. F., Oud, B., Roque, F. C., Ridder, D., Daran, J.-M., Pronk, J. T., & Maris, A. J. A. (2012) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2011.00787.x · Cited by 65 · see citing works
Respiration-Dependent Utilization of Sugars in Yeasts: a Determinant Role for Sugar Transporters
Goffrini, P., Ferrero, I., & Donnini, C. (2002) · Journal of Bacteriology · doi:10.1128/jb.184.2.427-432.2002 · Cited by 64 · see citing works
Spor, A., Nidelet, T., Simon, J., Bourgais, A., de Vienne, D., & Sicard, D. (2009) · BMC Evolutionary Biology · doi:10.1186/1471-2148-9-296 · Cited by 63 · see citing works
Self-citationAlbertin, W., Marullo, P., Aigle, M., Dillmann, C., de Vienne, D., Bely, M., & Sicard, D. (2011) · Applied and Environmental Microbiology · doi:10.1128/aem.02547-10 · Cited by 59 · see citing works
Self-citationSolis-Escalante, D., Kuijpers, N. G. A., Barrajón, N., van den Broek, M. A., Pronk, J. T., Daran, J.-M. G., & Daran-Lapujade, P. A. S. (2015) · Eukaryotic Cell · doi:10.1128/ec.00064-15 · Cited by 46 · see citing works
Emergence of Species-Specific Transporters During Evolution of the Hemiascomycete Phylum
Hertogh, B. D., Hancy, F., Goffeau, A., & Baret, P. V. (2005) · Genetics · doi:10.1534/genetics.105.046813 · Cited by 44 · see citing works
Candida glabrata : a deadly companion?
Bolotin‐Fukuhara, M., & Fairhead, C. (2014) · Yeast · doi:10.1002/yea.3019 · Cited by 42 · see citing works
Self-citation“Ant” and “Grasshopper” Life-History Strategies in Saccharomyces cerevisiae
Spor, A., Wang, S., Dillmann, C., de Vienne, D., & Sicard, D. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001579 · Cited by 41 · see citing works
Self-citationEcology of pathogenic yeasts in Amazonian soil
Mok, W. Y., Luizão, R. C. C., da Silva, M. D. S. B., Teixeira, M. F. S., & Muñiz, E. (1984) · Applied and Environmental Microbiology · doi:10.1128/aem.47.2.390-394.1984 · Cited by 39 · see citing works
Yeast Proteome Variations Reveal Different Adaptive Responses to Grape Must Fermentation
Blein‐Nicolas, M., Albertin, W., Valot, B., Marullo, P., Sicard, D., Giraud, C., Huet, S., Bourgais, A., Dillmann, C., de Vienne, D., et al. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst050 · Cited by 36 · see citing works
Self-citationDiderich, J. A., Teusink, B., Valkier, J., Anjos, J., Spencer‐Martins, I., DAM, K. V., & Walsh, M. C. (1999) · Microbiology · doi:10.1099/00221287-145-12-3447 · Cited by 35 · see citing works
The yield of experimental yeast populations declines during selection
Jasmin, J., Dillon, M. M., & Zeyl, C. (2012) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2012.1659 · Cited by 35 · see citing works
Kangwa, M., Yelemane, V., Polat, A. N., Gorrepati, K. D. D., Grasselli, M., & Fernández‐Lahore, M. (2015) · AMB Express · doi:10.1186/s13568-015-0155-y · Cited by 29 · see citing works
Limtong, S., & Yongmanitchai, W. (2010) · Antonie van Leeuwenhoek · doi:10.1007/s10482-010-9451-3 · Cited by 26 · see citing works
Genome evolution: Lessons from Genolevures
Bolotin‐Fukuhara, M., Casarégola, S., & Aigle, M. (2005) · Topics in current genetics · doi:10.1007/b136677 · Cited by 17 · see citing works
Self-citationSzeto, S. S. W., Reinke, S. N., Oyedotun, K. S., Sykes, B. D., & Lemire, B. D. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.344275 · Cited by 14 · see citing works
Saccharomyces delphensis Nov. Spec. A new yeast from South African dried figs
van der Walt, J. P., & Tscheuschner, I. T. (1956) · Antonie van Leeuwenhoek · doi:10.1007/bf02538323 · Cited by 13 · see citing works
Kluyveromyces bacillisporus sp. nov., a Yeast from Emory Oak Exudate
Lachance, M., Phaff, H. J., & Starmer, W. T. (1993) · International Journal of Systematic Bacteriology · doi:10.1099/00207713-43-1-115 · Cited by 13 · see citing works
Merikanto, I., Laakso, J. T., & Kaitala, V. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113436 · Cited by 11 · see citing works
Limtong, S., Jindamorakot, S., Am-In, S., Kaewwichian, R., Nitiyon, S., Yongmanitchai, W., & Nakase, T. (2011) · Antonie van Leeuwenhoek · doi:10.1007/s10482-011-9561-6 · Cited by 10 · see citing works
Torulopsis castellii sp.nov., a Yeast Isolated from a Finnish Soil
Capriotti, A. (1961) · Journal of General Microbiology · doi:10.1099/00221287-26-1-41 · Cited by 8 · see citing works
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- Authors
- Legrand, J., Bolotin-Fukuhara, M., Bourgais, A., Fairhead, C., & Sicard, D.
- Affiliations
- Université Paris-Saclay (FR)
- Université Paris-Sud (FR)
- Venue
- FEMS Yeast Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2015-12-17
- Volume
- 16
- Issue
- 2
- Pages
- fov112
- ISSN
- 1567-1356 (ISSN-L)
- 1567-1364
- OpenAlex
- W2220941193
- Cited by
- 8
- References
- 55
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2022: 1 · 2019: 2
- FWCI
- 0.00
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- FEMS Yeast Research (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Yeasts and Rust Fungi Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
- Keywords
- Candida glabrata, hemiascomycetes, carbon metabolism, gene dosage, Crabtree effect, facultative anaerobes, life history strategies, population growth rate, carrying capacity, glucose consumption rate, cell size, biomass yield
- MeSH terms
- Aerobiosis, Anaerobiosis, Carbon, Saccharomycetales, Fermentation, Glucose, Glycolysis, Oxidative Phosphorylation, Biomass, Gene Dosage, Metabolic Networks and Pathways
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