Kluyveromyces marxianus CCT7735: uma revisão sobre os mecanismos de respostas ao estresse por etanol com aplicação na produção de biocombustível
Palavras-chave:
Etanol, Resíduos agroindustriais, Estresse
Resumo
A produção do etanol como combustível é uma alternativa promissora a utilização dos combustíveis fósseis. Nesse contexto, os resíduos agroindustriais têm despontado como matérias-primas capazes de aumentar a produção de etanol sem competir com a produção de alimentos. Assim, tanto o soro de queijo, quanto subprodutos lignocelulósicos podem ser utilizados como substratos para a produção de etanol. No entanto, a levedura Saccharomyces cerevisiae é incapaz de metabolizar a lactose presente no soro de queijo e de crescer nas elevadas temperaturas requeridas no processo de Sacarificação e Fermentação Simultâneas (SSF) de biomassa lignocelulósica. Por outro lado, Kluyveromyces marxianusCCT7735 é uma linhagem desta levedura, que apresenta potencial para produzir etanol tanto a partir de soro de queijo quanto de subprodutos lignocelulósicos. Isto porque ela fermenta lactose e cresce em altas temperaturas. Todavia, ela tem o seu crescimento inibido em altas concentrações de etanol. Portanto, para viabilizar a produção de etanol, torna-se necessário compreender os mecanismos de resposta ao estresse por etanol em K. marxianus. Sendo assim, este trabalho teve como objetivo descrever e analisar os principais mecanismos de resposta ao estresse por etanol em leveduras,descritos na literatura, através de uma revisão bibliográfica, a fim de compreender como K. marxianus responde ao estresse etanólico. Nesse sentido, a abordagem utilizada nesta pesquisa foi do tipo exploratório, descritivo e bibliográfico.Desta forma, os artigos obtidos a partir das bases de dados eletrônicos foram analisados e sistematizados de acordo com a sua relevância para a compreensão dos mecanismos de respostas ao estresse por etanol em leveduras. A partir da análise dos mecanismos envolvidos na tolerância ao etanol descritos na literatura concluiu-se que eles contribuem para o entendimento das respostas moleculares ao estresse etanólico em K. marxianus. Entretanto, devido à complexidade destes mecanismos torna-se necessário fazer um estudo mais detalhado a nível molecular a fim de compreendê-los melhor.Referências
AGUILERA, F.; PEINADO, R.A.; MILLÁN, C.; ORTEGA, J.M.; MAURICIO, J. C. Relation ship between ethanol tolerance, H+-ATPase activity and the lipid composition of the plasma membrane in different wine yeast strains. International Journal of Food Microbiology, v. 110, p. 34–42, 2006.
ALEXANDRE, H.; ANSANAY-GALEOTE, V.; BLONDIN, S.D.B. Global gene expression during short-term ethanol stress in Saccharomyces cerevisiae. FEBS Letters, v. 498, p. 98-103, 2001.
ANDERSON, M. J.; BARKER, S. L.; BOONE, C.; MEASDAY, V. Identification of RCN1 and RSA3 as ethanol-tolerant genes in Saccharomyces cerevisiae using a high copy barcoded library. FEMS Yeast Research, v. 12, p.48–60, 2012.
ARAKI, Y.; WU, H.; KITAGAKI, H.; AKAO, T.; TAKAGI, T e SHIMOI, H. Ethanol stress stimulates the Ca2+-mediated calcineurin/Crz1 pathway in Saccharomyces cerevisiae. Journal of Bioscience and Bioengineering, v. 107, p. 1–6, 2009.
ARIYANTI, D e HADIYANTO, H. Ethanol Production from Whey by Kluyveromyces marxianus in Batch Fermentation System: Kinetics Parameters Estimation. Bulletin of Chemical Reaction Engineering & Catalysis, v. 7, p. 179-184, 2013.
AUESUKAREE, C.; DAMNERNSAWAD, A.; KRUATRACHUE, M.; POKETHITIYOOK, P.; BOONCHIRD, C.; KANEKO, Y.; HARASHIMA, S. Genome-wide identification of genes involved in tolerance to various environmental stresses in Saccharomyces cerevisiae. Journal Applied Genetic, v. 50, p. 301-310, 2009.
BAI, F. W.; ANDERSON, W. A.; MOO-YOUNG, M. Ethanol fermentation technologies from sugar and starch feedstocks. Biotechnology Advances, v. 26, p. 89-105, 2008.
BERRY, D. B.; GUAN, Q.; HOSE, J.; HAROON, S.; GEBBIA, M.; HEISLER2, L.E.; NISLOW, C.; GIAEVER, G.; GASCH, A.P. Multiple means to the same end: the genetic basis of acquired stress resistance in yeast. PLOS Genetics, v. 7, p. 1-11, 2011.
BLEOANCA, I.; SILVA, A.R.C.; PIMENTEL, C.; POUSADA, C. R.; MENEZES, R. A. Relationship between ethanol and oxidative stress in laboratory and brewing yeast strains. Journal of Bioscience and Bioengineering, v. 116, p. 697-705, 2013.
CASTRO, R. C. A.; ROBERTO, I. C. Selection of a thermotolerant Kluyveromyces marxianus strain with potential application for cellulosic ethanol production by simultaneous saccharification and fermentation. Applied Biochemistry and Biotechnology, v. 172, p. 1553-1564, 2014.
DICKEY, A. N.; YIM, W. S.; FALLER, R. Using ergosterol to mitigate the deleterious effects of ethanol on bilayer structure. The Journal of Physical Chemistry B, v.113, p. 2388-2397, 2010.
DING, J.; HUANG, X.; ZHANG, L.; ZHAO, N.; YANG, D.; ZHANG, K. Tolerance and stress response to ethanol in the yeast Saccharomyces cerevisiae. Applied Microbiology and Biotechnology, v. 85, p.253-263, 2009.
DING, M. Z.; LI, B. Z.; CHENG, J.S.; YUAN, Y. J. Metabolome analysis of differential responses of diploid and haploid yeast to ethanol stress. OMICS, v.14, p. 553-561, 2010.
DINIZ, R. H. S.; RODRIGUES, M. Q. R. B.; FIETTO, L.G.; PASSOS, F.M.L.; SILVEIRA, W. B. Optimizing and validating the production of ethanol from cheese
whey permeate by Kluyveromyces marxianus UFV-3. Biocatalysis and Agricultural Biotechnology, v.3, p.111–117, 2014.
DOĞAN, A.; DEMIRCI, S.; AYTEKIN, A. O.; ŞAHIN, F. Improvements of tolerance to stress conditions by genetic engineering in Saccharomyces cerevisiae during ethanol production. Applied Biochemistry and Biotechnology, v.174, p.28–42, 2014.
FLORÊNCIO, I. M.; FLORENTINO, E. R.; SILVA, F. L. H.; MARTINS, R. S.; CAVALCANTI, M. T.; GOMES, J. Production of ethanol from industrial whey. Revista Basileira Engenharia Agrícola e Ambiental, v.17, p. 1088-1092, 2013.
FONSECA, G. G.; HEINZLE, E.; WITTMANN, C.; GOMBERT, A. K. The yeast Kluyveromyces marxianus and its biotechnological potential. Applied Microbiology and Biotechnology, v. 79, p. 339-354, 2008.
GABARDO, S.; RECH, R.; ROSA, C. A.; AYUB, M. A. Z. Dynamics of ethanol production from whey and whey permeate by immobilized strains of Kluyveromyces marxianus in batch and continuous bioreactors. Renewable Energy, v. 69, p. 89-96, 2014.
GIL, J. V.; JIMENEZ, M. M.; PASTOR, A.; HUERTA, T. Aroma compounds in wine as influenced by apiculate yeasts. Journal of Food Science, v. 61, p. 1247–1250, 1996.
GONG, Y.; KAKIHARA, Y.; KROGAN, N.; GREENBLAT, T. J.; EMILI, A.; ZHANG, Z.; HOURY, W. A. An atlas of chaperone-protein interactions in Saccharomyces cerevisiae: implications to protein folding pathways in the cell. Molecular Systems Biology, v. 5, p. 1-14, 2009.
GUIMARÃES, P. M. R.; TEIXEIRA, J. A.; DOMINGUES. L. Fermentation of lactose to bio-ethanol by yeasts as part of integrated solutions for the valorization of cheese whey. Biotechnology Advances, v. 28, p. 375-384, 2010.
HENDERSON, C.M.; LOZADA-CONTRERAS, M.; NARAVANE, Y.; LONGO, M. L.; BLOCK, D. E. Analysis of major phospholipid species and ergosterol in fermenting industrial yeast strains using atmospheric pressure ionization ion-trap mass spectrometry. Journal of Agricultural and Food Chemistry, v. 59, p. 12761–12770, 2011.
HONG, M. F.; LEE, K-S.; YUB, B. J.; SUNGA, Y-J.; PARK, S. M.; KOO, H. M.; KWEONA, H-D.; PARK, J. C.; JINC, Y-S. Identification of gene targets eliciting improved alcohol tolerance in Saccharomyces cerevisiae through inverse metabolic engineering. Journal of Biotechnology, v. 149, p. 52–59, 2010.
KAHR, H.; HELMBERGER, S.; JÄGER, A. G. Yeast adaptation on the substrate straw. Bioenergy Technology, v. 8, p. 492-499, 2011.
KIM, S.; KIM, Y.S.; KIM, H.; JIN, I.; YOON, H. S. Saccharomyces cerevisiae KNU5377 stress response during high-temperature ethanol fermentation. Molecules and Cells, v. 35, p. 210-218, 2013a.
KIM, S.; PARK, J. M.; KIM, C.H. Ethanol production using whole plant biomass of jerusalem artichoke by Kluyveromyces marxianus CBS1555. Applied Biochemistry and Biotechnology, v. 169, p.1531-1545, 2013b.
KITAGAKI, H e TAKAGI, H. Mitochondrial metabolism and stress response of yeast: Applications in fermentation technologies. Journal of Bioscience and Bioengineering, v. 117, p. 383-393, 2014.
KOUSHKI, M.; JAFARI, M.; AZIZI, M. Comparison of ethanol production from cheese whey permeate by two yeast strains. Journal of Food Science Technology, v. 49, p. 614–619, 2012.
LANE, M. M e MORRISSEY, J. P. Kluyveromyces marxianus: A yeast emerging from its sister’s shadow. Fungal Biology Reviews, v. 24, p. 17–26, 2010.
LANE, M. M.; BURKE, N.; KARREMAN, R.; WOLFE, K. H.; O’BYRNE, C. P.; MORRISSEY, J. P. Physiological and metabolic diversity in the yeast Kluyveromyces marxianus. Antonie van Leeuwenhoek, v.100, p. 507-519, 2011.
LEI, J.; ZHAO, X.; GE, X.; BAI, F. Ethanol tolerance and the variation of plasma membrane composition of yeast floc populations with different size distribution. Journal of Biotechnology, v. 131, p. 270–275, 2007.
LEWIS, J.A.; ELKON, I.M.; McGEE, M.A.; HIGBEE, A.J.; GASCH, A.P. Exploiting natural variation in Saccharomyces cerevisiae to identify genes for increased ethanol resistance. Genetics, v. 186, p.1197-205, 2010.
LI, H.; MA, M.L.; LUO, S.; ZHANG, R.M.; HAN, P.; HU, W. Metabolic responses to ethanol in Saccharomyces cerevisiae using a gas chromatography tandem mass spectrometry-based metabolomics approach. The International Journal of Biochemistry & Cell Biology, v. 44, p. 1087– 1096, 2012.
LIU, Z. L.; MA, M.; SONG, M. Evolutionarily engineered ethanologenic yeast detoxifies lignocellulosic biomass conversion inhibitors by reprogrammed pathways. Molecular Genetics and Genomics, v. 282, p. 233-244, 2009.
LOURENÇO, A. B.; ROQUE, F.C.; TEIXEIRA, M. C.; ASCENSO, J. R.; CORREIA, I. S. Quantitative 1 H-NMR-Metabolomics Reveals Extensive Metabolic Reprogramming and the Effect of the Aquaglyceroporin FPS1 in Ethanol-Stressed Yeast Cells. PLOS ONE, v. 8, p. 1-12, 2013.
MA, M e LIU, L.Z. Quantitative transcription dynamic analysis reveals candidate genes and key regulators for etanol tolerance in Saccharomyces cerevisiae. BMC Microbiology, v. 10, p. 1471-2180, 2010b.
MA, M e LIU, Z. L. Mechanisms of ethanol tolerance in Saccharomyces cerevisiae. Applied Microbiology Biotechnology, v. 87 p.829-845, 2010a.
MAHMUD, S. A.; HIRASAWA, T.; FURUSAWA, C.; YOSHIKAWA, K.; SHIMIZU, H. Understanding the mechanism of heat stress tolerance caused by high trehalose accumulation in Saccharomyces cerevisiae using DNA microarray. Journal of Bioscience and Bioengineering, v. 113, p. 526-528, 2012.
MARYANA, R.; MA’RIFATUNB, D.; WHENI, I. A.; SATRIYO, K. W; RIZALA, W. A. Alkaline Pretreatment on Sugarcane Bagasse for Bioethanol Production. Energy Procedia, v. 47, p. 250–254, 2014.
MCCLELLAN, A. J.; XIA, Y.; DEUTSCHBAUER, A. M.; DAVIS, R.W.; GERSTEIN, M.; FRYDMAN, J. Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell, v. 5, p. 121-135, 2007.
NICOLAOU, S. A.; GAIDA, S. M.; PAPOUTSAKIS, E.T. A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: From biofuels and chemicals, to biocatalysis and bioremediation. Metabolic Engineering, v. 12, p.307-331, 2010.
NOGUCHI, C.; WATANABE, D.; ZHOU, Y.; AKAO, K.; SHIMOI, H. Association of Constitutive Hyperphosphorylation of Hsf1p with a Defective Ethanol Stress Response in Saccharomyces cerevisiae Sake Yeast Strains. Applied and Environmental Microbiology, p. 385–392, 2011.
OHTA, E.; NAKAYAMA, Y.; MUKAI, Y.; BAMBA, T e FUKUSAK, E. Metabolomic approach for improving ethanol stress tolerance in Saccharomyces cerevisiae. Journal of Bioscience and Bioengineering, v. 15, p. 1-7, 2015.
PASCHOS, T.; XIROS, C.; CHRISTAKOPOULOS, P. Ethanol effect on metabolic activity of the ethalogenic fungus Fusarium oxysporum. BMC Biotechnology, v.15, p.1-12, 2015.
PATRA, M.; SALONEN, E.; TERAMA, E.; VATTULAINEN, I.; FALLER, R.; LEE, B. W.; HOLOPAINEN, J e KARTTUNEN, M. Under the Influence of Alcohol: The Effect of Ethanol and Methanol on Lipid Bilayers. Biophysical Journal, v. 90, p. 1121–1135, 2006.
PÉREZ-GALLARDO, R. V.; BRIONES, L.S.; DÍAZ-PÉREZ, A. L.; GUTIÉRREZ, S.; RODRIGUEZ-ZAVALA, J.S.; CAMPOS-GARCIA, J. Reactive oxygen species production induced by ethanol in Saccharomyces cerevisiae increases because of a dysfunctional mitochondrial iron–sulfur cluster assembly system. FEMS, v. 13, p. 804–819, 2013.
PFEIFFER, T e MORLEY, A. An evolutionary perspective on the Crabtree effect. Frontiers in Molecular Biosciences, v. 1, p. 1-6, 2014.
PHAM, T. K e WRIGHT, P. C. Proteomic Analysis of Calcium Alginate-Immobilized Saccharomyces cerevisiae under High-Gravity Fermentation Conditions. Journal Proteome Research, v.2, p. 515-25, 2008.
PINA, C.; ANTÓNIO, J.; HOGG, T. Ethanol tolerance of five non-Saccharomyces wine yeasts in comparison with a strain of Saccharomyces cerevisiae - influence of different culture conditions. Food Microbiology, v. 21, p. 439–447, 2004.
PLAZA, M, A.; MATHIS, A. G.; CISNEROS, R. N.; GUERRERO, M. C.; MANZO- ÁVALOS, S.; HERNANDEZ, J. C. G.; SAAVEDRA-MOLINA, A. Respiratory capacity of the Kluyveromyces marxianus yeast isolated from the mescal process during oxidative stress. World Journal Microbiology and Biotechnology, v. 29, p.1279-1287, 2013.
PURIA, R.; MANNAN, M. A.; CHOPRA-DEWASTHALY, R.; GANESAN, K. Critical role of RPI1 in the stress tolerance of yeast during ethanolic fermentation. FEMS Yeast Research, v. 9, p. 1161-1171, 2009.
PUROHIT, G.K.; MAHANTY, A.; MOHANTY, B.P.; MOHANTY, S. Evaluation of housekeeping genes as references for quantitative real-time PCR analysis of gene expression in the murrel Channa striatus under high-temperature stress. Fish Physiology and Biochemistry, p. 1-11, 2015.
RICCI. M.; AGGRAVI, M.; BONECHI, C.; MARTINI, S.; ALOISI, A.M.; ROSSI, C. Metabolic response to exogenous ethanol in yeast: An in vivo statistical total correlation NMR spectroscopy approach. Journal Bioscience, v. 37, p. 749–755, 2012.
RODRUSSAMEE, N.; LERTWATTANASAKUL, N.; HIRATA, K.; SUPRAYOGI.; LIMTONG, S.; KOSAKA, T.; YAMADA, M. Growth and ethanol fermentation ability on hexose and pentose sugars and glucose effect under various conditions in thermotolerant yeast Kluyveromyces marxianus. Applied Microbiology and Biotechnology, v. 90, p.1573-1586, 2011.
SASANO, Y.; HAITANI, Y.; HASHIDA, K.; OHTSU, I.; SHIMA, J.; TAKAGI, H. Enhancement of the proline and nitric oxide synthetic pathway improves fermentation ability under multiple baking-associated stress conditions in industrial baker’s yeast. Microbial Cell Factories, v.11, p.1-8, 2012a.
SASANO, Y.; HAITANI, Y.; OHTSU, I.; SHIMA, J.; TAKAGI, H. Proline accumulation in baker's yeast enhances high-sucrose stress tolerance and fermentation ability in sweet dough. International Journal of Food Microbiology, v. 152, p. 40-43, 2012b.
SEIBOTH, B.; PAKDAMAN, B. S.; HARTL, L.; KUBICEK, C.P. Lactose metabolism in filamentous fungi: how to deal with an unknown substrate. Fungal Biology Reviews, v. 21, p.42 - 48, 2007.
SENGUPTA, S.; LAHIRI, S.; BANERJEE, S.; BASHISTHA, B.; GHOSH, A.K. Arginine mediated purification of trehalose-6-phosphate synthase (TPS) from Candida utilis: Its characterization and regulation. Biochimica et Biophysica Acta, v. 1810, p.1346–1354, 2011.
SEKINE, T.; KAWAGUCHI, A.; HAMANO, Y e TAKAGI, H. Desensitization of Feedback Inhibition of the Saccharomyces cerevisiae -Glutamyl Kinase Enhances Proline Accumulation and Freezing Tolerance. Applied and Environmental Microbiology, v.73, p. 4011–4019, 2007.
SIGNORI, L.; PASSOLUNGHI, S.; RUOHONEN, L.; PORRO, D.; BRANDUARDI, P. Effect of oxygenation and temperature on glucose-xylose fermentation in Kluyveromyces marxianus CBS712 strain. Microbial Cell Factories, v, 51, p. 1-13, 2014.
SILVEIRA, W. B.; PASSOS, F. J. V.; MANTOVANI, H. C.; PASSOS, F. M. L. Ethanol production from cheese whey permeate by Kluyveromyces marxianus UFV-3: A flux analysis of oxido-reductive metabolism as a function of lactose concentration and oxygen levels. Enzyme and Microbial Technology, v. 36, p. 930–936, 2005.
SOUZA, C. J. A.; COSTA, D. A.; RODRIGUES, M. Q. R. B.; SANTOS, A. F.; LOPES, M. R.; ABRANTES, A. B. P.; COSTA, P. S.; SILVEIRA, W. B.; PASSOS, F. M. L.; FIETTO, L. G. The influence of presaccharification, fermentation temperature and yeast strain on etanol production from sugarcane bagasse. Bioresourse and Biotecnology, v. 109, p. 63-69, 2012.
STANLEY, D.; BANDARA, A.; FRASER, S.; CHAMBERS. P. J.; STANLEY, G.A. The ethanol stress response and ethanol tolerance of Saccharomyces cerevisiae. Journal of Applied Microbiology, v.109, p. 13-24, 2010.
SYRIOPOULOS, C.; PANAYOTAROU, A.; LAI, K.; KLAPA, M. I. Transcriptomic analysis of Saccharomyces cerevisiae physiology in the context of galactose assimilation perturbations. Molecular BioSystems, v. 4, p. 937–949, 2008.
TAKAGI, H. Proline as a stress protectant in yeast: physiological functions, metabolic regulations, and biotechnological applications. Applied Microbiology and Biotechnology, v. 81, p. 211–223, 2008.
TAKAGI, H.; TAKAOKA, M.; KAWAGUCHI, M e KUBO, Y. Effect of L-Proline on Sake Brewing and Ethanol Stress in Saccharomyces cerevisiae. Applied and Environmental Microbiology, v.71, p. 8656-8662, 2005.
TANG, M.; WARING, A.J.; HONG, M. Trehalose-protected lipid membranes for determining membrane protein structure and insertion. Journal of Magnetic Resonance, v. 184, p. 222–227, 2007.
TEIXEIRA, M. C.; R, L. R.; MIRA, N. P; LOURENÇO, A. B.; SÁ-CORREIA, I. Genome-wide identification of Saccharomyces cerevisiae genes required for maximal tolerance to ethanol. Applied and Environment Microbiology, v. 75, p. 5761-5772, 2009.
VANEGAS, J. M.; CONTRERAS, M. F.; FALLER, R.; LONGO, M. L. Role of unsaturated lipid and ergosterol in ethanol tolerance of model yeast biomembranes. Biophysical Journal, v.102, p. 507-16, 2012.
VANEGAS, J. M.; FALLER, R.; LONGO, M.L. Influence of ethanol on lipid/sterol membranes: phase diagram construction from AFM imaging. Langmuir Letter, v. 26, p. 10415-10418, 2010.
VOORST, F. V.; HOUGHTON-LARSEN, J.; JONSON, L.; KIELLAND-BRANDT, M.C e BRANDT, A. Genome-wide identification of genes required for growth of Saccharomyces cerevisiae under etanol stress. Yeast, v. 23, p. 351–359, 2006.
WANG, M.; ZHAO, J.; YANG, Z.; DUD, Z.; YANG, Z. Electrochemical insights into the etanol tolerance of Saccharomyces cerevisiae. Bioelectrochemistry, v. 71, p. 107–112, 2007.
WANG, P.M.; ZHENG, D.Q.; CHI, X.Q.; LI, O.; QIAN, C.D.; LIU, T.Z.; ZHANG, X.Y.; DU, F.G.; SUN, P.Y.; QU, A.M.; WU, X.C. Relationship of trehalose accumulation with ethanol fermentation in industrial Saccharomyces cerevisiae yeast strains. Bioresource Technology, v. 152, p.371–376, 2014.
WATANABE, M.; WATANABE, D.; AKAO, T.; SHIMOI, H. Overexpression of MSN2 in a sake yeast strain promotes ethanol tolerance and increases ethanol production in sake brewing. Journal of Bioscience Bioengineering, v. 107, p. 516-8, 2009.
YOSHIKAWA, K.; TANAKA, T.; FURUSAWA, C.; NAGAHISA, K.; HIRASAWA, T.; SHIMIZU, H. Comprehensive phenotypic analysis for identi¢cation of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. FEMS Yeast Research, v. 9, p. 32–44, 2009.
YOU, K. M.; ROSENFIELD, C. L.; KNIPPLE, D. C. Ethanol tolerance in the yeast saccharomyces cerevisiae is dependent on cellular oleic acid content. Applied and Environmental Microbiology, v. 69, p. 1499-1503, 2003.
YU, K.O.; JUNG, J.; RAMZI, A. B.; CHOE, S.H.; KIM, S. W.; PARK, C.; HAN, S. O. Increased ethanol production from glycerol by Saccharomyces cerevisiae strains with enhanced stress tolerance from the overexpression of SAGA complex components. Enzyme and Microbial Technology, v. 51, p. 237– 243, 2012.
ZHANG, K.; TONG, M.; GAO, K.; DI, Y.; WANG, P.; ZHANG, C.; WU, X.; ZHENG, D. Genomic reconstruction to improve bioethanol and ergosterol production of industrial yeast Saccharomyces cerevisiae. Journal Industrial Microbiology and Biotechnology, v. 42, p. 207-218, 2015.
ZHAO, X. Q.; BAI, F.W. Mechanisms of yeast stress tolerance and its manipulation for efficient fuel ethanol production. Journal of Biotechnology, v. 144, p. 23–30, 2009.
ZHENG, D. Q.; LIU, T. Z.; CHEN, J.; ZHANG, K.; LI, O.; ZHU, L.; ZHAO, Y.H; WU, X. C.; WANG, P. M. Comparative functional genomics to reveal the
molecular basis of phenotypic diversities and guide the genetic breeding of industrial yeast strains. Applied Microbiology and Biotechnology, v. 97, p. 2067-2076, 2013.
ALEXANDRE, H.; ANSANAY-GALEOTE, V.; BLONDIN, S.D.B. Global gene expression during short-term ethanol stress in Saccharomyces cerevisiae. FEBS Letters, v. 498, p. 98-103, 2001.
ANDERSON, M. J.; BARKER, S. L.; BOONE, C.; MEASDAY, V. Identification of RCN1 and RSA3 as ethanol-tolerant genes in Saccharomyces cerevisiae using a high copy barcoded library. FEMS Yeast Research, v. 12, p.48–60, 2012.
ARAKI, Y.; WU, H.; KITAGAKI, H.; AKAO, T.; TAKAGI, T e SHIMOI, H. Ethanol stress stimulates the Ca2+-mediated calcineurin/Crz1 pathway in Saccharomyces cerevisiae. Journal of Bioscience and Bioengineering, v. 107, p. 1–6, 2009.
ARIYANTI, D e HADIYANTO, H. Ethanol Production from Whey by Kluyveromyces marxianus in Batch Fermentation System: Kinetics Parameters Estimation. Bulletin of Chemical Reaction Engineering & Catalysis, v. 7, p. 179-184, 2013.
AUESUKAREE, C.; DAMNERNSAWAD, A.; KRUATRACHUE, M.; POKETHITIYOOK, P.; BOONCHIRD, C.; KANEKO, Y.; HARASHIMA, S. Genome-wide identification of genes involved in tolerance to various environmental stresses in Saccharomyces cerevisiae. Journal Applied Genetic, v. 50, p. 301-310, 2009.
BAI, F. W.; ANDERSON, W. A.; MOO-YOUNG, M. Ethanol fermentation technologies from sugar and starch feedstocks. Biotechnology Advances, v. 26, p. 89-105, 2008.
BERRY, D. B.; GUAN, Q.; HOSE, J.; HAROON, S.; GEBBIA, M.; HEISLER2, L.E.; NISLOW, C.; GIAEVER, G.; GASCH, A.P. Multiple means to the same end: the genetic basis of acquired stress resistance in yeast. PLOS Genetics, v. 7, p. 1-11, 2011.
BLEOANCA, I.; SILVA, A.R.C.; PIMENTEL, C.; POUSADA, C. R.; MENEZES, R. A. Relationship between ethanol and oxidative stress in laboratory and brewing yeast strains. Journal of Bioscience and Bioengineering, v. 116, p. 697-705, 2013.
CASTRO, R. C. A.; ROBERTO, I. C. Selection of a thermotolerant Kluyveromyces marxianus strain with potential application for cellulosic ethanol production by simultaneous saccharification and fermentation. Applied Biochemistry and Biotechnology, v. 172, p. 1553-1564, 2014.
DICKEY, A. N.; YIM, W. S.; FALLER, R. Using ergosterol to mitigate the deleterious effects of ethanol on bilayer structure. The Journal of Physical Chemistry B, v.113, p. 2388-2397, 2010.
DING, J.; HUANG, X.; ZHANG, L.; ZHAO, N.; YANG, D.; ZHANG, K. Tolerance and stress response to ethanol in the yeast Saccharomyces cerevisiae. Applied Microbiology and Biotechnology, v. 85, p.253-263, 2009.
DING, M. Z.; LI, B. Z.; CHENG, J.S.; YUAN, Y. J. Metabolome analysis of differential responses of diploid and haploid yeast to ethanol stress. OMICS, v.14, p. 553-561, 2010.
DINIZ, R. H. S.; RODRIGUES, M. Q. R. B.; FIETTO, L.G.; PASSOS, F.M.L.; SILVEIRA, W. B. Optimizing and validating the production of ethanol from cheese
whey permeate by Kluyveromyces marxianus UFV-3. Biocatalysis and Agricultural Biotechnology, v.3, p.111–117, 2014.
DOĞAN, A.; DEMIRCI, S.; AYTEKIN, A. O.; ŞAHIN, F. Improvements of tolerance to stress conditions by genetic engineering in Saccharomyces cerevisiae during ethanol production. Applied Biochemistry and Biotechnology, v.174, p.28–42, 2014.
FLORÊNCIO, I. M.; FLORENTINO, E. R.; SILVA, F. L. H.; MARTINS, R. S.; CAVALCANTI, M. T.; GOMES, J. Production of ethanol from industrial whey. Revista Basileira Engenharia Agrícola e Ambiental, v.17, p. 1088-1092, 2013.
FONSECA, G. G.; HEINZLE, E.; WITTMANN, C.; GOMBERT, A. K. The yeast Kluyveromyces marxianus and its biotechnological potential. Applied Microbiology and Biotechnology, v. 79, p. 339-354, 2008.
GABARDO, S.; RECH, R.; ROSA, C. A.; AYUB, M. A. Z. Dynamics of ethanol production from whey and whey permeate by immobilized strains of Kluyveromyces marxianus in batch and continuous bioreactors. Renewable Energy, v. 69, p. 89-96, 2014.
GIL, J. V.; JIMENEZ, M. M.; PASTOR, A.; HUERTA, T. Aroma compounds in wine as influenced by apiculate yeasts. Journal of Food Science, v. 61, p. 1247–1250, 1996.
GONG, Y.; KAKIHARA, Y.; KROGAN, N.; GREENBLAT, T. J.; EMILI, A.; ZHANG, Z.; HOURY, W. A. An atlas of chaperone-protein interactions in Saccharomyces cerevisiae: implications to protein folding pathways in the cell. Molecular Systems Biology, v. 5, p. 1-14, 2009.
GUIMARÃES, P. M. R.; TEIXEIRA, J. A.; DOMINGUES. L. Fermentation of lactose to bio-ethanol by yeasts as part of integrated solutions for the valorization of cheese whey. Biotechnology Advances, v. 28, p. 375-384, 2010.
HENDERSON, C.M.; LOZADA-CONTRERAS, M.; NARAVANE, Y.; LONGO, M. L.; BLOCK, D. E. Analysis of major phospholipid species and ergosterol in fermenting industrial yeast strains using atmospheric pressure ionization ion-trap mass spectrometry. Journal of Agricultural and Food Chemistry, v. 59, p. 12761–12770, 2011.
HONG, M. F.; LEE, K-S.; YUB, B. J.; SUNGA, Y-J.; PARK, S. M.; KOO, H. M.; KWEONA, H-D.; PARK, J. C.; JINC, Y-S. Identification of gene targets eliciting improved alcohol tolerance in Saccharomyces cerevisiae through inverse metabolic engineering. Journal of Biotechnology, v. 149, p. 52–59, 2010.
KAHR, H.; HELMBERGER, S.; JÄGER, A. G. Yeast adaptation on the substrate straw. Bioenergy Technology, v. 8, p. 492-499, 2011.
KIM, S.; KIM, Y.S.; KIM, H.; JIN, I.; YOON, H. S. Saccharomyces cerevisiae KNU5377 stress response during high-temperature ethanol fermentation. Molecules and Cells, v. 35, p. 210-218, 2013a.
KIM, S.; PARK, J. M.; KIM, C.H. Ethanol production using whole plant biomass of jerusalem artichoke by Kluyveromyces marxianus CBS1555. Applied Biochemistry and Biotechnology, v. 169, p.1531-1545, 2013b.
KITAGAKI, H e TAKAGI, H. Mitochondrial metabolism and stress response of yeast: Applications in fermentation technologies. Journal of Bioscience and Bioengineering, v. 117, p. 383-393, 2014.
KOUSHKI, M.; JAFARI, M.; AZIZI, M. Comparison of ethanol production from cheese whey permeate by two yeast strains. Journal of Food Science Technology, v. 49, p. 614–619, 2012.
LANE, M. M e MORRISSEY, J. P. Kluyveromyces marxianus: A yeast emerging from its sister’s shadow. Fungal Biology Reviews, v. 24, p. 17–26, 2010.
LANE, M. M.; BURKE, N.; KARREMAN, R.; WOLFE, K. H.; O’BYRNE, C. P.; MORRISSEY, J. P. Physiological and metabolic diversity in the yeast Kluyveromyces marxianus. Antonie van Leeuwenhoek, v.100, p. 507-519, 2011.
LEI, J.; ZHAO, X.; GE, X.; BAI, F. Ethanol tolerance and the variation of plasma membrane composition of yeast floc populations with different size distribution. Journal of Biotechnology, v. 131, p. 270–275, 2007.
LEWIS, J.A.; ELKON, I.M.; McGEE, M.A.; HIGBEE, A.J.; GASCH, A.P. Exploiting natural variation in Saccharomyces cerevisiae to identify genes for increased ethanol resistance. Genetics, v. 186, p.1197-205, 2010.
LI, H.; MA, M.L.; LUO, S.; ZHANG, R.M.; HAN, P.; HU, W. Metabolic responses to ethanol in Saccharomyces cerevisiae using a gas chromatography tandem mass spectrometry-based metabolomics approach. The International Journal of Biochemistry & Cell Biology, v. 44, p. 1087– 1096, 2012.
LIU, Z. L.; MA, M.; SONG, M. Evolutionarily engineered ethanologenic yeast detoxifies lignocellulosic biomass conversion inhibitors by reprogrammed pathways. Molecular Genetics and Genomics, v. 282, p. 233-244, 2009.
LOURENÇO, A. B.; ROQUE, F.C.; TEIXEIRA, M. C.; ASCENSO, J. R.; CORREIA, I. S. Quantitative 1 H-NMR-Metabolomics Reveals Extensive Metabolic Reprogramming and the Effect of the Aquaglyceroporin FPS1 in Ethanol-Stressed Yeast Cells. PLOS ONE, v. 8, p. 1-12, 2013.
MA, M e LIU, L.Z. Quantitative transcription dynamic analysis reveals candidate genes and key regulators for etanol tolerance in Saccharomyces cerevisiae. BMC Microbiology, v. 10, p. 1471-2180, 2010b.
MA, M e LIU, Z. L. Mechanisms of ethanol tolerance in Saccharomyces cerevisiae. Applied Microbiology Biotechnology, v. 87 p.829-845, 2010a.
MAHMUD, S. A.; HIRASAWA, T.; FURUSAWA, C.; YOSHIKAWA, K.; SHIMIZU, H. Understanding the mechanism of heat stress tolerance caused by high trehalose accumulation in Saccharomyces cerevisiae using DNA microarray. Journal of Bioscience and Bioengineering, v. 113, p. 526-528, 2012.
MARYANA, R.; MA’RIFATUNB, D.; WHENI, I. A.; SATRIYO, K. W; RIZALA, W. A. Alkaline Pretreatment on Sugarcane Bagasse for Bioethanol Production. Energy Procedia, v. 47, p. 250–254, 2014.
MCCLELLAN, A. J.; XIA, Y.; DEUTSCHBAUER, A. M.; DAVIS, R.W.; GERSTEIN, M.; FRYDMAN, J. Diverse cellular functions of the Hsp90 molecular chaperone uncovered using systems approaches. Cell, v. 5, p. 121-135, 2007.
NICOLAOU, S. A.; GAIDA, S. M.; PAPOUTSAKIS, E.T. A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: From biofuels and chemicals, to biocatalysis and bioremediation. Metabolic Engineering, v. 12, p.307-331, 2010.
NOGUCHI, C.; WATANABE, D.; ZHOU, Y.; AKAO, K.; SHIMOI, H. Association of Constitutive Hyperphosphorylation of Hsf1p with a Defective Ethanol Stress Response in Saccharomyces cerevisiae Sake Yeast Strains. Applied and Environmental Microbiology, p. 385–392, 2011.
OHTA, E.; NAKAYAMA, Y.; MUKAI, Y.; BAMBA, T e FUKUSAK, E. Metabolomic approach for improving ethanol stress tolerance in Saccharomyces cerevisiae. Journal of Bioscience and Bioengineering, v. 15, p. 1-7, 2015.
PASCHOS, T.; XIROS, C.; CHRISTAKOPOULOS, P. Ethanol effect on metabolic activity of the ethalogenic fungus Fusarium oxysporum. BMC Biotechnology, v.15, p.1-12, 2015.
PATRA, M.; SALONEN, E.; TERAMA, E.; VATTULAINEN, I.; FALLER, R.; LEE, B. W.; HOLOPAINEN, J e KARTTUNEN, M. Under the Influence of Alcohol: The Effect of Ethanol and Methanol on Lipid Bilayers. Biophysical Journal, v. 90, p. 1121–1135, 2006.
PÉREZ-GALLARDO, R. V.; BRIONES, L.S.; DÍAZ-PÉREZ, A. L.; GUTIÉRREZ, S.; RODRIGUEZ-ZAVALA, J.S.; CAMPOS-GARCIA, J. Reactive oxygen species production induced by ethanol in Saccharomyces cerevisiae increases because of a dysfunctional mitochondrial iron–sulfur cluster assembly system. FEMS, v. 13, p. 804–819, 2013.
PFEIFFER, T e MORLEY, A. An evolutionary perspective on the Crabtree effect. Frontiers in Molecular Biosciences, v. 1, p. 1-6, 2014.
PHAM, T. K e WRIGHT, P. C. Proteomic Analysis of Calcium Alginate-Immobilized Saccharomyces cerevisiae under High-Gravity Fermentation Conditions. Journal Proteome Research, v.2, p. 515-25, 2008.
PINA, C.; ANTÓNIO, J.; HOGG, T. Ethanol tolerance of five non-Saccharomyces wine yeasts in comparison with a strain of Saccharomyces cerevisiae - influence of different culture conditions. Food Microbiology, v. 21, p. 439–447, 2004.
PLAZA, M, A.; MATHIS, A. G.; CISNEROS, R. N.; GUERRERO, M. C.; MANZO- ÁVALOS, S.; HERNANDEZ, J. C. G.; SAAVEDRA-MOLINA, A. Respiratory capacity of the Kluyveromyces marxianus yeast isolated from the mescal process during oxidative stress. World Journal Microbiology and Biotechnology, v. 29, p.1279-1287, 2013.
PURIA, R.; MANNAN, M. A.; CHOPRA-DEWASTHALY, R.; GANESAN, K. Critical role of RPI1 in the stress tolerance of yeast during ethanolic fermentation. FEMS Yeast Research, v. 9, p. 1161-1171, 2009.
PUROHIT, G.K.; MAHANTY, A.; MOHANTY, B.P.; MOHANTY, S. Evaluation of housekeeping genes as references for quantitative real-time PCR analysis of gene expression in the murrel Channa striatus under high-temperature stress. Fish Physiology and Biochemistry, p. 1-11, 2015.
RICCI. M.; AGGRAVI, M.; BONECHI, C.; MARTINI, S.; ALOISI, A.M.; ROSSI, C. Metabolic response to exogenous ethanol in yeast: An in vivo statistical total correlation NMR spectroscopy approach. Journal Bioscience, v. 37, p. 749–755, 2012.
RODRUSSAMEE, N.; LERTWATTANASAKUL, N.; HIRATA, K.; SUPRAYOGI.; LIMTONG, S.; KOSAKA, T.; YAMADA, M. Growth and ethanol fermentation ability on hexose and pentose sugars and glucose effect under various conditions in thermotolerant yeast Kluyveromyces marxianus. Applied Microbiology and Biotechnology, v. 90, p.1573-1586, 2011.
SASANO, Y.; HAITANI, Y.; HASHIDA, K.; OHTSU, I.; SHIMA, J.; TAKAGI, H. Enhancement of the proline and nitric oxide synthetic pathway improves fermentation ability under multiple baking-associated stress conditions in industrial baker’s yeast. Microbial Cell Factories, v.11, p.1-8, 2012a.
SASANO, Y.; HAITANI, Y.; OHTSU, I.; SHIMA, J.; TAKAGI, H. Proline accumulation in baker's yeast enhances high-sucrose stress tolerance and fermentation ability in sweet dough. International Journal of Food Microbiology, v. 152, p. 40-43, 2012b.
SEIBOTH, B.; PAKDAMAN, B. S.; HARTL, L.; KUBICEK, C.P. Lactose metabolism in filamentous fungi: how to deal with an unknown substrate. Fungal Biology Reviews, v. 21, p.42 - 48, 2007.
SENGUPTA, S.; LAHIRI, S.; BANERJEE, S.; BASHISTHA, B.; GHOSH, A.K. Arginine mediated purification of trehalose-6-phosphate synthase (TPS) from Candida utilis: Its characterization and regulation. Biochimica et Biophysica Acta, v. 1810, p.1346–1354, 2011.
SEKINE, T.; KAWAGUCHI, A.; HAMANO, Y e TAKAGI, H. Desensitization of Feedback Inhibition of the Saccharomyces cerevisiae -Glutamyl Kinase Enhances Proline Accumulation and Freezing Tolerance. Applied and Environmental Microbiology, v.73, p. 4011–4019, 2007.
SIGNORI, L.; PASSOLUNGHI, S.; RUOHONEN, L.; PORRO, D.; BRANDUARDI, P. Effect of oxygenation and temperature on glucose-xylose fermentation in Kluyveromyces marxianus CBS712 strain. Microbial Cell Factories, v, 51, p. 1-13, 2014.
SILVEIRA, W. B.; PASSOS, F. J. V.; MANTOVANI, H. C.; PASSOS, F. M. L. Ethanol production from cheese whey permeate by Kluyveromyces marxianus UFV-3: A flux analysis of oxido-reductive metabolism as a function of lactose concentration and oxygen levels. Enzyme and Microbial Technology, v. 36, p. 930–936, 2005.
SOUZA, C. J. A.; COSTA, D. A.; RODRIGUES, M. Q. R. B.; SANTOS, A. F.; LOPES, M. R.; ABRANTES, A. B. P.; COSTA, P. S.; SILVEIRA, W. B.; PASSOS, F. M. L.; FIETTO, L. G. The influence of presaccharification, fermentation temperature and yeast strain on etanol production from sugarcane bagasse. Bioresourse and Biotecnology, v. 109, p. 63-69, 2012.
STANLEY, D.; BANDARA, A.; FRASER, S.; CHAMBERS. P. J.; STANLEY, G.A. The ethanol stress response and ethanol tolerance of Saccharomyces cerevisiae. Journal of Applied Microbiology, v.109, p. 13-24, 2010.
SYRIOPOULOS, C.; PANAYOTAROU, A.; LAI, K.; KLAPA, M. I. Transcriptomic analysis of Saccharomyces cerevisiae physiology in the context of galactose assimilation perturbations. Molecular BioSystems, v. 4, p. 937–949, 2008.
TAKAGI, H. Proline as a stress protectant in yeast: physiological functions, metabolic regulations, and biotechnological applications. Applied Microbiology and Biotechnology, v. 81, p. 211–223, 2008.
TAKAGI, H.; TAKAOKA, M.; KAWAGUCHI, M e KUBO, Y. Effect of L-Proline on Sake Brewing and Ethanol Stress in Saccharomyces cerevisiae. Applied and Environmental Microbiology, v.71, p. 8656-8662, 2005.
TANG, M.; WARING, A.J.; HONG, M. Trehalose-protected lipid membranes for determining membrane protein structure and insertion. Journal of Magnetic Resonance, v. 184, p. 222–227, 2007.
TEIXEIRA, M. C.; R, L. R.; MIRA, N. P; LOURENÇO, A. B.; SÁ-CORREIA, I. Genome-wide identification of Saccharomyces cerevisiae genes required for maximal tolerance to ethanol. Applied and Environment Microbiology, v. 75, p. 5761-5772, 2009.
VANEGAS, J. M.; CONTRERAS, M. F.; FALLER, R.; LONGO, M. L. Role of unsaturated lipid and ergosterol in ethanol tolerance of model yeast biomembranes. Biophysical Journal, v.102, p. 507-16, 2012.
VANEGAS, J. M.; FALLER, R.; LONGO, M.L. Influence of ethanol on lipid/sterol membranes: phase diagram construction from AFM imaging. Langmuir Letter, v. 26, p. 10415-10418, 2010.
VOORST, F. V.; HOUGHTON-LARSEN, J.; JONSON, L.; KIELLAND-BRANDT, M.C e BRANDT, A. Genome-wide identification of genes required for growth of Saccharomyces cerevisiae under etanol stress. Yeast, v. 23, p. 351–359, 2006.
WANG, M.; ZHAO, J.; YANG, Z.; DUD, Z.; YANG, Z. Electrochemical insights into the etanol tolerance of Saccharomyces cerevisiae. Bioelectrochemistry, v. 71, p. 107–112, 2007.
WANG, P.M.; ZHENG, D.Q.; CHI, X.Q.; LI, O.; QIAN, C.D.; LIU, T.Z.; ZHANG, X.Y.; DU, F.G.; SUN, P.Y.; QU, A.M.; WU, X.C. Relationship of trehalose accumulation with ethanol fermentation in industrial Saccharomyces cerevisiae yeast strains. Bioresource Technology, v. 152, p.371–376, 2014.
WATANABE, M.; WATANABE, D.; AKAO, T.; SHIMOI, H. Overexpression of MSN2 in a sake yeast strain promotes ethanol tolerance and increases ethanol production in sake brewing. Journal of Bioscience Bioengineering, v. 107, p. 516-8, 2009.
YOSHIKAWA, K.; TANAKA, T.; FURUSAWA, C.; NAGAHISA, K.; HIRASAWA, T.; SHIMIZU, H. Comprehensive phenotypic analysis for identi¢cation of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. FEMS Yeast Research, v. 9, p. 32–44, 2009.
YOU, K. M.; ROSENFIELD, C. L.; KNIPPLE, D. C. Ethanol tolerance in the yeast saccharomyces cerevisiae is dependent on cellular oleic acid content. Applied and Environmental Microbiology, v. 69, p. 1499-1503, 2003.
YU, K.O.; JUNG, J.; RAMZI, A. B.; CHOE, S.H.; KIM, S. W.; PARK, C.; HAN, S. O. Increased ethanol production from glycerol by Saccharomyces cerevisiae strains with enhanced stress tolerance from the overexpression of SAGA complex components. Enzyme and Microbial Technology, v. 51, p. 237– 243, 2012.
ZHANG, K.; TONG, M.; GAO, K.; DI, Y.; WANG, P.; ZHANG, C.; WU, X.; ZHENG, D. Genomic reconstruction to improve bioethanol and ergosterol production of industrial yeast Saccharomyces cerevisiae. Journal Industrial Microbiology and Biotechnology, v. 42, p. 207-218, 2015.
ZHAO, X. Q.; BAI, F.W. Mechanisms of yeast stress tolerance and its manipulation for efficient fuel ethanol production. Journal of Biotechnology, v. 144, p. 23–30, 2009.
ZHENG, D. Q.; LIU, T. Z.; CHEN, J.; ZHANG, K.; LI, O.; ZHU, L.; ZHAO, Y.H; WU, X. C.; WANG, P. M. Comparative functional genomics to reveal the
molecular basis of phenotypic diversities and guide the genetic breeding of industrial yeast strains. Applied Microbiology and Biotechnology, v. 97, p. 2067-2076, 2013.
Publicado
2021-05-02
Como Citar
BRITO, A. Kluyveromyces marxianus CCT7735: uma revisão sobre os mecanismos de respostas ao estresse por etanol com aplicação na produção de biocombustível. Revista Científica do UBM, v. 19, n. 37, p. 39-60, 2 maio 2021.
Edição
Seção
Artigos