Palabras clave
levaduras cosmopolitas
microorganismos resilientes
ambientes extremos
Cómo citar
Resumen
Las levaduras son hongos unicelulares de uso común en la elaboración del pan, la cerveza y el vino. Sin embargo, cubren otras funciones esenciales en la naturaleza; estos microorganismos en los ecosistemas contribuyen a la descomposición de la materia orgánica y en el reciclaje de los nutrientes. Además, por su extraordinaria capacidad adaptativa, producto de la evolución, sobreviven en casi cualquier hábitat del planeta, incluidos los más extremos, como los climas polares, los desiertos con alta radiación solar e incluso el espacio exterior. Este artículo de revisión explora algunas de las estrategias que permiten a las levaduras prosperar en inhóspitas circunstancias al soportar el frío, la radiación ultravioleta, sobrevivir en lugares como el espacio sideral o en condiciones de estrés. Un análisis de su versatilidad refleja su impacto en la economía circular y su relevancia en la naturaleza.
Citas
Ali, S. S., Sun, J., Koutra, E., El-Zawawy, N., Elsamahy, T. & El-Shetehy, M. (2021). Construction of a novel cold-adapted oleaginous yeast consortium valued for textile azo dye wastewater processing and biorefinery. Fuel, 285, 119050. https://doi.org/10.1016/j.fuel.2020.119050
Alkalbani, N. S., Osaili, T. M., Al-Nabulsi, A. A., Olaimat, A. N., Liu, S.-Q., Shah, N. P., Apostolopoulos, V. & Ayyash, M. M. (2022). Assessment of Yeasts as Potential Probiotics: A Review of Gastrointestinal Tract Conditions and Investigation Methods. Journal of Fungi, 8(4), 365. https://doi.org/10.3390/jof8040365
Andreu C. & del Olmo M. (2024) Biocatalysis with Unconventional Yeasts. Catalysts, 14(11), 767. https://doi.org/10.3390/catal14110767
Anwar, H., Iftikhar, A., Muzaffar, H., Almatroudi, A., Allemailem, K. S., Navaid, S., Saleem, S. & Khurshid, M. (2021). Biodiversity of Gut Microbiota: Impact of Various Host and Environmental Factors. BioMed Research International, 2021(5575245), 9. https://doi.org/10.1155/2021/5575245
Aouizerat, T., Gutman, I., Paz, Y., Maeir, A. M., Gadot, Y., Gelman, D., Szitenberg, A., Drori, E., Pinkus, A., Schoemann, M., Kaplan, R., Ben-Gedalya, T., Coppenhagen-Glazer, S., Reich, E., Saragovi, A., Lipschits, O., Klutstein, M. & Hazan, R. (2019). Isolation and Characterization of Live Yeast Cells from Ancient Vessels as a Tool in Bio-Archaeology. mBio, 10(2), 10.1128/mbio.00388-19. https://doi.org/10.1128/mbio.00388-19
Arthur, H. & Watson, K. (1976). Thermal adaptation in yeast: growth temperatures, membrane lipid, and cytochrome composition of psychrophilic, mesophilic, and thermophilic yeasts. Journal of Bacteriology, 128(1), 56-68. https://doi.org/10.1128/jb.128.1.56-68.1976
Baedke, J., Fábregas-Tejeda, A. & Nieves Delgado, A. (2020). The holobiont concept before Margulis. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 334(3), 149-155. https://doi.org/10.1002/jez.b.22931
Boekhout, T., Amend, A. S., El Baidouri, F., Gabaldón, T., Geml, J., Mittelbach, M., Robert, V., Tan, C. S., Turchetti, B., Vu, D., Wang, Q.-M. & Yurkov, A. (2022). Trends in yeast diversity discovery. Fungal Diversity, 114(1), 491-537. https://doi.org/10.1007/s13225-021-00494-6
Bradford, L. L. & Ravel, J. (2017). The vaginal mycobiome: A contemporary perspective on fungi in women’s health and diseases. Virulence, 8(3), 342-351. https://doi.org/10.1080/21505594.2016.1237332
Brown, A. J. P., Cowen, L. E., di Pietro, A. & Quinn, J. (2017). Stress Adaptation. Microbiology Spectrum, 5(4), 10.1128/microbiolspec.funk-0048-2016. https://doi.org/10.1128/microbiolspec.funk-0048-2016
Buratti, S., Girometta, C. E., Baiguera, R. M., Barucco, B., Bernardi, M., De Girolamo, G., Malgaretti, M., Oliva, D., Picco, A. M. & Savino, E. (2022) Fungal Diversity in Two Wastewater Treatment Plants in North Italy. Microorganisms, 10(6),1096. https://doi.org/10.3390/microorganisms10061096
Buzzini, P. & Margesin, R. (Eds.). (2014). Cold-adapted Yeasts: Biodiversity, Adaptation Strategies and Biotechnological Significance. Springer nature, New York. https://doi.org/10.1007/978-3-642-39681-6
Buzzini, P., Turchetti, B. & Yurkov, A. (2018). Extremophilic yeasts: the toughest yeasts around? Yeast, 35(8), 487-497. https://doi.org/10.1002/yea.3314
de Marañón, I. M., Chaudanson, N., Joly, N. & Gervais, P. (1999). Slow heat rate increases yeast thermotolerance by maintaining plasma membrane integrity. Biotechnology and Bioengineering, 65(2), 176-181. https://doi.org/10.1002/(SICI)1097-0290(19991020)65:2<176::AID-BIT7>3.0.CO;2-5
Choudhary, J., Singh, S. & Nain, L. (2016). Thermotolerant fermenting yeasts for simultaneous saccharification fermentation of lignocellulosic biomass. Electronic Journal of Biotechnology, 21, 82-92.
Dias, B., Lopes, M., Ramôa, R., Pereira, A. S. & Belo, I. (2021). Candida tropicalis as a Promising Oleaginous Yeast for Olive Mill Wastewater Bioconversion. Energies, 14(3), Article 3. https://doi.org/10.3390/en14030640
Dunn, B. & Stambuk, B. U. (2022). Yeasts: From the Laboratory to Bioprocesses. En Yeasts: From Nature to Bioprocesses (pp. 396-430). Bentham Science Publishers. https://www.benthamdirect.com/content/books/9789815051063.chap14
Fiers, W. D., Gao, I. H. & Iliev, I. D. (2019). Gut mycobiota under scrutiny: fungal symbionts or environmental transients? Current Opinion in Microbiology, 50, 79-86. https://doi.org/10.1016/j.mib.2019.09.010
Garg, A., Sanchez, A. M., Miele, M., Schwer, B. & Shuman, S. (2023). Cellular responses to long-term phosphate starvation of fission yeast: Maf1 determines fate choice between quiescence and death associated with aberrant tRNA biogenesis. Nucleic Acids Research, 51(7), 3094-3115.
Genç, Y., Bardakci, H., Yücel, Ç., Karatoprak, G. Ş., Küpeli Akkol, E., Hakan Barak, T. & Sobarzo-Sánchez, E. (2020). Oxidative stress and marine carotenoids: Application by using nanoformulations. Marine Drugs, 18(8), 423.
González, J., Romero-Aguilar, L., Matus-Ortega, G., Pardo, J. P., Flores-Alanis, A., Segal-Kischinevzky, C., González, J., Romero-Aguilar, L., Matus-Ortega, G., Pardo, J. P., Flores-Alanis, A. & Segal-Kischinevzky, C. (2020). Levaduras adaptadas al frío: el tesoro biotecnológico de la Antártica. TIP Revista Especializada en Ciencias Químico-Biológicas, Vol. 23, 1-14. https://doi.org/10.22201/fesz.23958723e.2020.0.267
Gónzalez, J., Villarreal-Huerta, D., Rosas-Paz, M. & Segal-Kischinevzky, C (2025). Biotechnological applications of yeasts under extreme conditions. En: Extremophilic Yeasts. Buzzini, P. & Turchetti, B. Springer Nature. Switzerland
Grice, E. A. & Segre, J. A. (2011). The skin microbiome. Nature Reviews Microbiology, 9(4), 244-253. https://doi.org/10.1038/nrmicro2537
Hallen-Adams, H. E. & Suhr, M. J. (2017). Fungi in the healthy human gastrointestinal tract. Virulence, 8(3), 352-358. https://doi.org/10.1080/21505594.2016.1247140
Hammond, T. G. & Birdsall, H. H. (2022). Yeast in Space. En Y. V. Pathak, M. Araújo dos Santos & L. Zea (Eds.), Handbook of Space Pharmaceuticals (pp. 717-732). Springer International Publishing. Switzerland. https://doi.org/10.1007/978-3-030-05526-4_8
Hoffman, S. M., Alvarez, M., Alfassi, G., Rein, D. M., Garcia-Echauri, S., Cohen, Y. & Avalos, J. L. (2021). Cellulosic biofuel production using emulsified simultaneous saccharification and fermentation (eSSF) with conventional and thermotolerant yeasts. Biotechnology for Biofuels, 14(1), 157. https://doi.org/10.1186/s13068-021-02008-7
Igwegbe, C. A., Obiora-Okafo, I. A., Iwuozor, K. O., Ghosh, S., Kurniawan, S. B., Rangabhashiyam, S., Kanaoujiya, R. & Ighalo, J. O. (2022). Treatment technologies for bakers’ yeast production wastewater. Environmental Science and Pollution Research, 29(8), 11004-11026. https://doi.org/10.1007/s11356-021-17992-4
Kadkhodaei, S., Hatefi, A., Pedramnia, S., Godini, E., Khalili-Samani, S., Saniee, P., Sarrafnejad, A., Salmanian, A.-H., Sotoudeh, M., Graham, D. Y., Malekzadeh, R. & Siavoshi, F. (2024). Role of Oral Yeast in Replenishing Gastric Mucosa with Yeast and Helicobacter pylori. Yeast, 41(11-12), 645-657. https://doi.org/10.1002/yea.3983
Kim, H. J., Lee, J. H., Do, H. & Jung, W. (2014). Production of Antifreeze Proteins by Cold-Adapted Yeasts. En P. Buzzini y R. Margesin (Eds.), Cold-adapted Yeasts: Biodiversity, Adaptation Strategies and Biotechnological Significance (pp. 259-280). Springer, Berlin. https://doi.org/10.1007/978-3-642-39681-6_12
Kot, A. M., Błażejak, S., Kieliszek, M., Gientka, I. & Bryś, J. (2019). Simultaneous Production of Lipids and Carotenoids by the Red Yeast Rhodotorula from Waste Glycerol Fraction and Potato Wastewater. Applied Biochemistry and Biotechnology, 189(2), 589-607. https://doi.org/10.1007/s12010-019-03023-z
Kreusch, M. G. & Duarte, R. T. D. (2021). Photoprotective compounds and radioresistance in pigmented and non-pigmented yeasts. Applied Microbiology and Biotechnology, 105(9), 3521-3532. https://doi.org/10.1007/s00253-021-11271-5
Lahue, C., Madden, A., Dunn, R. R. & Smukowski Heil, C. (2020). History and Domestication of Saccharomyces cerevisiae in Bread Baking. Frontiers in Genetics, 11, 584718. https://doi.org/10.3389/fgene.2020.584718
Leach, M. D., Farrer, R. A., Tan, K., Miao, Z., Walker, L. A., Cuomo, C. A., Wheeler, R. T., Brown, A. J. P., Wong, K. H. & Cowen, L. E. (2016). Hsf1 and Hsp90 orchestrate temperature-dependent global transcriptional remodelling and chromatin architecture in Candida albicans. Nature Communications, 7(1), 11704. https://doi.org/10.1038/ncomms11704
Leach, M. D., Klipp, E., Cowen, L. E. & Brown, A. J. P. (2012). Fungal Hsp90: a biological transistor that tunes cellular outputs to thermal inputs. Nature Reviews Microbiology, 10(10), 693-704. https://doi.org/10.1038/nrmicro2875
Lee, J. H., Park, A. K., Do, H., Park, K. S., Moh, S. H., Chi, Y. M. & Kim, H. J. (2012). Structural Basis for Antifreeze Activity of Ice-binding Protein from Arctic Yeast*. Journal of Biological Chemistry, 287(14), 11460-11468. https://doi.org/10.1074/jbc.M111.331835
Leo, P. & Onofri, S. (2023). Yeasts in the Era of Astrobiological Research. Journal of the Indian Institute of Science, 103(3), 699-709. https://doi.org/10.1007/s41745-023-00378-5
Li, Z., Li, C., Cheng, P. & Yu, G. (2022). Rhodotorula mucilaginosa—alternative sources of natural carotenoids, lipids, and enzymes for industrial use. Heliyon, 8(11), e11505. https://doi.org/10.1016/j.heliyon.2022.e11505.
Lima, R., Ribeiro, F. C., Colombo, A. L. & de Almeida, J. N. (2022). The emerging threat antifungal-resistant Candida tropicalis in humans, animals, and environment. Frontiers in Fungal Biology, 3, 957021. https://doi.org/10.3389/ffunb.2022.957021
Mierzejewska, J., Kowalska, P., Marlicka, K., Dworakowska, S., Sitkiewicz, E., Trzaskowski, M., Głuchowska, A., Mosieniak, G. & Milner-Krawczyk, M. (2023). Exploring Extracellular Vesicles of Probiotic Yeast as Carriers of Biologically Active Molecules Transferred to Human Intestinal Cells. International Journal of Molecular Sciences, 24(14), 11340. https://doi.org/10.3390/ijms241411340
Mishra, A. A. & Koh, A. Y. (2018). Adaptation of Candida albicans During Gastrointestinal Tract Colonization. Current Clinical Microbiology Reports, 5(3), 165-172. https://doi.org/10.1007/s40588-018-0096-8
Naseeruddin, S., Goli, J. & Linga, V. (2014). Yeast diversity adaptation and thermotolerance. KAVAKA, 42, 87-100.
Nash, A. K., Auchtung, T. A., Wong, M. C., Smith, D. P., Gesell, J. R., Ross, M. C., Stewart, C. J., Metcalf, G. A., Muzny, D. M., Gibbs, R. A., Ajami, N. J. & Petrosino, J. F. (2017). The gut mycobiome of the Human Microbiome Project healthy cohort. Microbiome, 5(1), 153. https://doi.org/10.1186/s40168-017-0373-4
Nguyen, U. T. & Kalan, L. R. (2022). Forgotten fungi: the importance of the skin mycobiome. Current Opinion in Microbiology, 70, 102235. https://doi.org/10.1016/j.mib.2022.102235
Nicula, N. O., Lungulescu, E. M., Rîmbu, G. A., Marinescu, V., Corbu, V. M. & Csutak, O. (2023). Bioremediation of wastewater using yeast strains: an assessment of contaminant removal efficiency. International Journal of Environmental Research and Public Health, 20(6), 4795.
Nielsen, S., White, K., Preiss, K., Peart, D., Gianoulias, K., Juel, R., Sutton, J., McKinney, J., Bender, J., Pinc, G., Bergren, K., Gans, W., Kelley, J. & McQuaid, M. (2021). Growth and Antifungal Resistance of the Pathogenic Yeast, Candida Albicans, in the Microgravity Environment of the International Space Station: An Aggregate of Multiple Flight Experiences. Life, 11(4), 283. https://doi.org/10.3390/life11040283
Ohtsuka, H., Imada, K., Shimasaki, T. & Aiba, H. (2022). Sporulation: A response to starvation in the fission yeast Schizosaccharomyces pombe. MicrobiologyOpen, 11(3), e1303. https://doi.org/10.1002/mbo3.1303
Pérez, S. Á. (2022). Ecology: Yeasts on their Natural Environment. En Yeasts: From Nature to Bioprocesses (pp. 27-57). Bentham Science Publishers.Singapore. 10.2174/97898150510631220201
Pulschen, A. A., de Araujo, G. G., de Carvalho, A. C. S. R., Cerini, M. F., Fonseca, L. de M., Galante, D. & Rodrigues, F. (2018). Survival of Extremophilic Yeasts in the Stratospheric Environment during Balloon Flights and in Laboratory Simulations. Applied and Environmental Microbiology, 84(23), e01942-18. https://doi.org/10.1128/AEM.01942-18
Rastogi, R. P., Richa, Sinha, R. P., Singh, S. P. & Häder, D.-P. (2010). Photoprotective compounds from marine organisms. Journal of Industrial Microbiology and Biotechnology, 37(6), 537-558. https://doi.org/10.1007/s10295-010-0718-5
Romero-Frasca, E., Velasquez-Orta, S. B., Escobar-Sánchez, V., Tinoco-Valencia, R. & Orta Ledesma, M. T. (2021). Bioprospecting of wild type ethanologenic yeast for ethanol fuel production from wastewater-grown microalgae. Biotechnology for Biofuels, 14(1), 93. https://doi.org/10.1186/s13068-021-01925-x
Rosas-Paz, M., Zamora-Bello, A., Torres-Ramírez, N., Villarreal-Huerta, D., Romero-Aguilar, L., Pardo, J. P., El Hafidi, M., Sandoval, G., Segal-Kischinevzky, C. & González, J. (2024). Nitrogen limitation-induced adaptive response and lipogenesis in the Antarctic yeast Rhodotorula mucilaginosa M94C9. Frontiers in Microbiology, 15, 1416155. https://doi.org/10.3389/fmicb.2024.1416155
Rozaliyani, A., Antariksa, B., Nurwidya, F., Zaini, J., Setianingrum, F., Hasan, F., Nugrahapraja, H., Yusva, H., Wibowo, H., Bowolaksono, A. & Kosmidis, C. (2023). The Fungal and Bacterial Interface in the Respiratory Mycobiome with a Focus on Aspergillus spp. Life, 13(4), 1017. https://doi.org/10.3390/life13041017
Santacroce, L., Passarelli, P. C., Azzolino, D., Bottalico, L., Charitos, I. A., Cazzolla, A. P., Colella, M., Topi, S., Godoy, F. G. & D’Addona, A. (2023). Oral microbiota in human health and disease: A perspective. Experimental Biology and Medicine, 248(15), 1288-1301. https://doi.org/10.1177/15353702231187645
Segal-Kischinevzky, C., Romero-Aguilar, L., Alcaraz, L. D., López-Ortiz, G., Martínez-Castillo, B., Torres-Ramírez, N., Sandoval, G. & González, J. (2022). Yeasts Inhabiting Extreme Environments and Their Biotechnological Applications. Microorganisms, 10(4), 1-26. https://doi.org/10.3390/microorganisms10040794
Shen, L., Zhang, S. & Chen, G. (2021). Regulated strategies of cold-adapted microorganisms in response to cold: a review. Environmental Science and Pollution Research, 28(48), 68006-68024. https://doi.org/10.1007/s11356-021-16843-6
Shi, K., Gao, Z., Shi, T.-Q., Song, P., Ren, L.-J., Huang, H. & Ji, X.-J. (2017). Reactive Oxygen Species-Mediated Cellular Stress Response and Lipid Accumulation in Oleaginous Microorganisms: The State of the Art and Future Perspectives. Frontiers in Microbiology, 8(793), 1-9. https://doi.org/10.3389/fmicb.2017.00793
Starmer, W. T. & Lachance, M.-A. (2011). Chapter 6 - Yeast Ecology. En C. P. Kurtzman, J. W. Fell & T. Boekhout (Eds.), The Yeasts (Fifth Edition) (pp. 65-83). Elsevier. USA. https://doi.org/10.1016/B978-0-444-52149-1.00006-9
Sultan, A. S., Kong, E. F., Rizk, A. M. & Jabra-Rizk, M. A. (2018). The oral microbiome: A Lesson in coexistence. PLoS Pathogens, 14(1), e1006719. https://doi.org/10.1371/journal.ppat.1006719
Sun, S. & Gresham, D. (2021). Cellular quiescence in budding yeast. Yeast, 38(1), 12-29. https://doi.org/10.1002/yea.3545
Tang, W., Wang, Y., Zhang, J., Cai, Y. & He, Z. (2019). Biosynthetic Pathway of Carotenoids in Rhodotorula and Strategies for Enhanced Their Production. Journal of Microbiology and Biotechnology, 29(4), 507-517. https://doi.org/10.4014/jmb.1801.01022
Viñarta, S. C., Angelicola, M. V., Barros, J. M., Fernández, P. M., Mac Cormak, W., Aybar, M. J. & de Figueroa, L. I. C. (2016). Oleaginous yeasts from Antarctica: Screening and preliminary approach on lipid accumulation. Journal of Basic Microbiology, 56(12), 1360-1368. https://doi.org/10.1002/jobm.201600099
Whitesell, L., Robbins, N., Huang, D. S., McLellan, C. A., Shekhar-Guturja, T., LeBlanc, E. V., Nation, C. S., Hui, R., Hutchinson, A., Collins, C., Chatterjee, S., Trilles, R., Xie, J. L., Krysan, D. J., Lindquist, S., Porco, J. A., Tatu, U., Brown, L. E., Pizarro, J. & Cowen, L. E. (2019). Structural basis for species-selective targeting of Hsp90 in a pathogenic fungus. Nature Communications, 10(1), 402. https://doi.org/10.1038/s41467-018-08248-w
Zaragoza, O. & Nielsen, K. (2013). Titan cells in Cryptococcus neoformans: Cells with a giant impact. Current Opinion in Microbiology, 16(4), 409. https://doi.org/10.1016/j.mib.2013.03.006
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