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Food Science and Human Wellness 2021, 10(1): 54-62 https://doi.org/10.1016/j.fshw.2020.05.006
Research Article | Open Access | Issue | Published: 03 June 2020

Comparative transcriptomics analysis of Zygosaccharomyces mellis under high-glucose stress

Show Author's Information Gongliang Liua,  Xinyu Bia,  Changli Taob,  Yongtao Feia( ),  Sujuan Gaoa,  Jinglong Lianga,  Weidong Baia( )
College of Light Industry and Food Science, Zhongkai University of Agriculture and Engineering, Guangzhou, 510225, China
Guangdong Province Key Laboratory for Biotechnology Drug Candidates, School of Biosciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, 510006, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Keywords:
Zygosaccharomyces mellis, Transcriptomics, High-glucose tolerance, HOG-MAPK, Trehalose
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Liu G, Bi X, Tao C, et al. Comparative transcriptomics analysis of Zygosaccharomyces mellis under high-glucose stress. Food Science and Human Wellness, 2021, 10(1): 54-62. https://doi.org/10.1016/j.fshw.2020.05.006
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Abstract Full text About this article

The high-glucose tolerance of yeast is the main factor determining the efficiency of high-density alcohol fermentation. Zygosaccharomyces mellis LGL-1 isolated from honey could survive under 700 g/L high-glucose stress and its tolerant characteristics were identified in our previous study. This study was performed to explore and clarify the high-glucose tolerance mechanism of Z. mellis LGL-1. Comparative transcriptomic analysis was used to analyze the genes with differential expression in Z. mellis under high-glucose conditions of 300, 500 and 700 g/L. With 300 g/L samples as reference, there were 937 and 2380 differentially expressed genes (DEGs) in the 500 and 700 g/L samples, respectively. Meanwhile, there was 825 significant DEGs in the 700 g/L samples compared with that of the 500 g/L samples. The result revealed that transcriptional changes in multiple metabolic pathways occur in response to high-glucose stress. q-RT PCR analysis further confirmed that several stress response pathways, such as the high osmolarity glycerol mitogen-activated protein kinase (HOG-MAPK) signal transduction pathway, trehalose synthesis pathway and oxidative stress response are closely related to high-glucose tolerance in Z. mellis. This study clarifies mechanisms of Z. mellis in response to high-glucose osmotic stress, providing theoretical basis for the process control of high-density alcohol fermentation.


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About this article

Comparative transcriptomics analysis of Zygosaccharomyces mellis under high-glucose stress

Show Author's information Gongliang Liua, Xinyu Bia, Changli Taob, Yongtao Feia( ), Sujuan Gaoa, Jinglong Lianga, Weidong Baia( )
College of Light Industry and Food Science, Zhongkai University of Agriculture and Engineering, Guangzhou, 510225, China
Guangdong Province Key Laboratory for Biotechnology Drug Candidates, School of Biosciences and Biopharmaceutics, Guangdong Pharmaceutical University, Guangzhou, 510006, China

Peer review under responsibility of KeAi Communications Co., Ltd.

Abstract

The high-glucose tolerance of yeast is the main factor determining the efficiency of high-density alcohol fermentation. Zygosaccharomyces mellis LGL-1 isolated from honey could survive under 700 g/L high-glucose stress and its tolerant characteristics were identified in our previous study. This study was performed to explore and clarify the high-glucose tolerance mechanism of Z. mellis LGL-1. Comparative transcriptomic analysis was used to analyze the genes with differential expression in Z. mellis under high-glucose conditions of 300, 500 and 700 g/L. With 300 g/L samples as reference, there were 937 and 2380 differentially expressed genes (DEGs) in the 500 and 700 g/L samples, respectively. Meanwhile, there was 825 significant DEGs in the 700 g/L samples compared with that of the 500 g/L samples. The result revealed that transcriptional changes in multiple metabolic pathways occur in response to high-glucose stress. q-RT PCR analysis further confirmed that several stress response pathways, such as the high osmolarity glycerol mitogen-activated protein kinase (HOG-MAPK) signal transduction pathway, trehalose synthesis pathway and oxidative stress response are closely related to high-glucose tolerance in Z. mellis. This study clarifies mechanisms of Z. mellis in response to high-glucose osmotic stress, providing theoretical basis for the process control of high-density alcohol fermentation.

Keywords: Zygosaccharomyces mellis, Transcriptomics, High-glucose tolerance, HOG-MAPK, Trehalose

References(49)

[1]

X. Li, D. Yongdong, Y. Ying, et al., Fermentation process and metabolic flux of ethanol production from the detoxified hydrolyzate of cassava residue, Front. Microbiol. 8 (2017) 1603–1615, http://dx.doi.org/10.3389/fmicb.2017.01603.
DOI Google Scholar
[2]

C. Ma, X. Wei, C. Sun, et al., Improvement of acetic acid tolerance ofSaccharomyces cerevisiae using a zinc-finger-based artificial transcription factor and identification of novel genes involved in acetic acid tolerance, Appl. Microbiol. Biotechnol. 99 (2015) 2441–2449, http://dx.doi.org/10.1007/s00253-014-6343-x.
DOI Google Scholar
[3]

A. Shitamukai, H. Dai, S. Sonobe, et al., Evidence for antagonistic regulation of Cell growth by the calcineurin and high osmolarity glycerol pathways in Saccharomyces cerevisiae, J. Biol. Chem. 279 (2004) 3651–3661, http://dx.doi.org/10.1074/jbc.M306098200.
DOI Google Scholar
[4]

M. Gomar Alba, E. Jiménez-Martí, M. del Olmo, The Saccharomyces cerevisiae Hot1p regulated geneYHR087W (HGI1) has a role in translation upon high glucose concentration stress, BMC Mol. Biol. 13 (2012) 19–29, http://dx.doi.org/10.1186/1471-2199-13-19.
DOI Google Scholar
[5]

G. Ramon, M. Pilar, T. Jordi, et al., New genes involved in osmotic stresstolerance in Saccharomyces cerevisiae, Front. Microbiol. 7 (2016) 1545–1557, http://dx.doi.org/10.3389/fmicb.2016.01545.
DOI Google Scholar
[6]

S.H. Mohd Azhar, R. Abdulla, S.A. Jambo, et al., Yeasts in sustainablebioethanol production: a review, Biochem. Biophys. Rep. 10 (2017) 52–61, http://dx.doi.org/10.1016/j.bbrep.2017.03.003.
DOI Google Scholar
[7]

T. Iwaki, S. Kurono, Y. Yokose, et al., Cloning of glycerol-3-phosphate dehydrogenase genes (ZrGPD1 and ZrGPD2) and glycerol dehydrogenase genes (ZrGCY1 and ZrGCY2) from the salt-tolerant yeast Zygosaccharomyces rouxii, Yeast 18 (2001) 737–744, http://dx.doi.org/10.1002/yea.722.
DOI Google Scholar
[8]

K. Matt, A.A. Andalis, G.R. Fink, et al., High osmolarity extends life span in Saccharomyces cerevisiae by a mechanism related to calorie restriction, Mol. Cell. Biol. 22 (2002) 8056–8066, http://dx.doi.org/10.1128/MCB.22.22.8056-8066.2002.
DOI Google Scholar
[9]

P.M. Wang, D.Q. Zheng, X.Q. Chi, et al., Relationship of trehalose accumulation with ethanol fermentation in industrial Saccharomyces cerevisiae yeast strains, Bioresour. Technol. 152 (2014) 371–376, http://dx.doi.org/10.1016/j.biortech.2013.11.033.
DOI Google Scholar
[10]

D.J. Erasmus, G.K. van der Merwe, H.J.J. van Vuuren, Genome-wide expression analyses: metabolic adaptation of Saccharomyces cerevisiae to high sugar stress, FEMS Yeast Res. 3 (2010) 375–399, http://dx.doi.org/10.1016/S1567-1356(02)00203-9.
DOI Google Scholar
[11]

E. Jiménez Martí, A. Zuzuarregui, M. Gomar-Alba, et al., Molecular response of Saccharomyces cerevisiae wine and laboratory strains to high sugar stress conditions, Int. J. Food Microbiol. 145 (2011) 211–220, http://dx.doi.org/10.1016/j.ijfoodmicro.2010.12.023.
DOI Google Scholar
[12]

L. Přibylová, V. Farkaš, I. Slaninova, et al., Differences in osmotolerant and cell-wall properties of two zygosaccharomyces rouxii strains, Folia Microbiol.52 (3) (2007) 241, http://dx.doi.org/10.1007/BF02931305.
DOI Google Scholar
[13]

G. Liu, C. Tao, B. Zhu, et al., Identification of Zygosaccharomyces mellisstrains instored honey and their stress tolerance, Food Sci. Biotechnol. 25 (2016)1645–1650, http://dx.doi.org/10.1007/s10068-016-0253-x.
DOI Google Scholar
[14]

G.L. Liu, Y.T. Fei, J.Y. Yu, et al., Nutrient utilization of Zygosaccharomyces mellis and its metabolic characteristics in response to high-glucose stress, Shipin Kexue/Food Science. 40 (2019) 166–171, http://dx.doi.org/10.7506/spkx1002-6630-20181202-008.
DOI Google Scholar
[15]

J. Vindeløv, N. Arneborg, Saccharomyces cerevisiae and Zygosaccharomyces mellis exhibit different hyperosmotic shock responses, Yeast 19 (2010) 429–439, http://dx.doi.org/10.1002/yea.844.
DOI Google Scholar
[16]

B.M. Bravo Ferrada, N. Brizuela, E. Gerbino, et al., Effect of protective agents and previous acclimation on ethanol resistance of frozen and freeze-dried Lactobacillus plantarum strains, Cryobiology 71 (2015) 522–528, http://dx.doi.org/10.1016/j.cryobiol.2015.10.154.
DOI Google Scholar
[17]

S.W. Lee, M.K. Oh, Improved production of N-acetylglucosamine in Saccharomyces cerevisiae by reducing glycolytic flux, Biotechnol. Bioeng. 113 (2016) 2524–2528, http://dx.doi.org/10.1002/bit.26014.
DOI Google Scholar
[18]

T. Vogl, L. Sturmberger, T. Kickenweiz, et al., A toolbox of diverse promoters related to methanol utilization – functionally verified parts for heterologous pathway expression in Pichia pastoris, ACS Synth. Biol. 5 (2015) 172–186.
DOI Google Scholar
[19]

R. Prielhofer, S.P. Cartwright, A.B. Graf, et al., Pichia pastoris regulates its gene-specific response to different carbon sources at the transcriptional, rather than the translational level, BMC Genomics 16 (2015) 167–176, http://dx.doi.org/10.1186/s12864-015-1393-8.
DOI Google Scholar
[20]

H. Stefan, Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae, FEBS Lett. 583 (2009) 4025–4029, http://dx.doi.org/10.1016/j.febslet.2009.10.069.
DOI Google Scholar
[21]

M.T. Martínezpastor, G. Marchler, C. Schüller, et al., The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE), EMBO J. 15 (1996) 2227–2235, http://dx.doi.org/10.1002/j.1460-2075.1996.tb00576.x.
DOI Google Scholar
[22]

D. Wang, Z. Hao, J. Zhao, et al., Comparative physiological and transcriptomic analyses reveal salt tolerance mechanisms of Zygosaccharomyces rouxii, Process. Biochem. 82 (2019) 59–67, http://dx.doi.org/10.1016/j.procbio.2019.04.009.
DOI Google Scholar
[23]

M. Guerfal, S. Ryckaert, P.P. Jacobs, et al., The HAC1 gene fromPichia pastoris: characterization and effect of its overexpression on the production of secreted, surface displayed and membrane proteins, Microb. Cell Fact. 9 (2010) 49–61, http://dx.doi.org/10.1186/1475-2859-9-49.
DOI Google Scholar
[24]

J.C. Argüelles, Physiological roles of trehalose in bacteria and yeasts: a comparative analysis, Arch. Microbiol. 174 (2000) 217–224, http://dx.doi.org/10.1007/s002030000192.
DOI Google Scholar
[25]

H. Rußmayer, M. Buchetics, C. Gruber, et al., Systems-level organization of yeast methylotrophic lifestyle, BMC Biol. 13 (2015) 80–90, http://dx.doi.org/10.1186/s12915-015-0186-5.
DOI Google Scholar
[26]

S.B. Azoun, A.E. Belhaj, R. Göngrich, et al., Molecular optimization of rabies virus glycoprotein expression in Pichia pastoris, Microb. Biotechnol. 9 (2016) 355–368, http://dx.doi.org/10.1111/1751-7915.12350.
DOI Google Scholar
[27]

K. Tokuoka, T. Ishitani, W.C. Chung, Accumulation of polyols and sugars in some sugar-tolerant yeasts, J. Gen. Appl. Microbiol. 38 (1992) 35–46.
DOI Google Scholar
[28]

C.G. Hounsa, E.V. Brandt, J. Thevelein, et al., Role of trehalose in survival of Saccharomyces cerevisiae under osmotic stress, Microbiology 144 (1998) 671–680, http://dx.doi.org/10.1099/00221287-144-3-671.
DOI Google Scholar
[29]

J.H. Duffus, C.J. Mitchell, Effect of high osmotic pressure on DNA synthesis in the fission yeast, Schizosaccharomyces pombe, Exp. Cell Res. 61 (1970) 213–216, http://dx.doi.org/10.1016/0014-4827(70)90279-X.
DOI Google Scholar
[30]

G. Sina, H. Won Ki, B. Kiowa, et al., Global analysis of protein expression inyeast, Nature 425 (2003) 737–741, http://dx.doi.org/10.1038/nature02046.
DOI Google Scholar
[31]

P.O. Ljungdahl, D.F. Bertrand, Regulation of amino acid, nucleotide, and phosphate metabolism in Saccharomyces cerevisiae, Genetics 190 (2012) 885–898, http://dx.doi.org/10.1534/genetics.111.133306.
DOI Google Scholar
[32]

N.C. Verma, R.K. Singh, Stress-inducible DNA repair in Saccharomyces cerevisiae, J. Environ. Pathol. Toxicol. Oncol. 20 (2001) 1321–1333.
DOI Google Scholar
[33]

T.C. Dakal, L. Solieri, P. Giudici, Adaptive response and tolerance to sugar and salt stress in the food yeast Zygosaccharomyces rouxii, Int. J. Food Microbiol. 185 (2014) 140–157, http://dx.doi.org/10.1016/j.ijfoodmicro.2014.05.015.
DOI Google Scholar
[34]

A. Plemenitaš, T. Vaupotič, M. Lenassi, et al., Adaptation of extremely halotolerant black yeast Hortaea werneckii to increased osmolarity: a molecular perspective at a glance, Stud. Mycol. 61 (2008) 67–75, http://dx. doi.org/10.3114/sim.2008.61.06.
DOI Google Scholar
[35]

P.H. Yancey, Organic osmolytes as compatible, metabolic and counteractingcytoprotectants in high osmolarity and other stresses, J. Exp. Biol. 208 (2005)2819–2830, http://dx.doi.org/10.1242/jeb.01730.
DOI Google Scholar
[36]

F. Martínez-Montañés, A. Pascual-Ahuir, M. Proft, Toward a genomic view of the gene expression program regulated by osmostress in yeast, Omics A J. Integr. Biol. 14 (2010) 619–627, http://dx.doi.org/10.1089/omi.2010.0046.
DOI Google Scholar
[37]

T. Iwaki, Y. Higashida, H. Tsuji, et al., Characterization of a second gene (ZSOD22) of Na+/H+ antiporter from salt-tolerant yeast Zygosaccharomyces rouxii and functional expression of ZSOD2 and ZSOD22 in Saccharomyces cerevisiae, Yeast 14 (2010) 1167–1174.
DOI
[38]

K.L. Träff, R.R. Otero Cordero, W.H. van Zyl, Deletion of the GRE3 aldose reductase gene and its influence on xylosemetabolism in recombinant strains of Saccharomyces cerevisiae expressingthe xylA and XKS1 genes, Appl. Environ. Microbiol. 67 (2001) 5668–5674, http://dx.doi.org/10.1128/AEM.67.12.5668- 5674.2001.
DOI Google Scholar
[39]

M. Dragosits, J. Stadlmann, A. Graf, et al., The response to unfolded protein isinvolved in osmotolerance of Pichia pastoris, BMC Genomics 11 (2010)207–219, http://dx.doi.org/10.1186/1471-2164-11-207.
DOI Google Scholar
[40]

H. Shao, W. Hongyan, T. Xiaoli, NAC transcription factors in plant multipleabiotic stress responses: progress and prospects, Front. Plant Sci. 6 (2015)902–911, http://dx.doi.org/10.3389/fpls.2015.00902.
DOI Google Scholar
[41]

P. Meaden, K. Hill, J. Wagner, et al., The yeast KRE5 gene encodes a probable endoplasmic reticulum protein required for (1-6)-β-D-glucan synthesis and normal cell growth, Mol. Cell. Biol. 10 (1990) 3013–3019.
DOI Google Scholar
[42]

D. Fox, A. Smulian, Mitogen-activated protein kinase Mkp1 of Pneumocystis carinii complements the slt2 defect in the cell integrity pathway of Saccharomyces cerevisiae, Mol. Microbiol. 34 (2010) 451–462, http://dx.doi.org/10.1046/j.1365-2958.1999.01606.x.
DOI Google Scholar
[43]

R.D. Lahondès, V. Ribes, B. Arcangioli, Fission yeast Sap1 protein is essential for chromosome stability, Eukaryot. Cell 2 (2003) 910–921, http://dx.doi.org/10.1128/EC.2.5.910-921.2003.
DOI Google Scholar
[44]

M.A. Collart, O.O. Panasenko, The Ccr4–not complex, Gene 492 (2012) 42–53, http://dx.doi.org/10.1016/j.gene.2011.09.033.
DOI Google Scholar
[45]

C. Belfiore, S. Fadda, R. Raya, et al., Molecular basis of the adaption of the anchovy isolate Lactobacillus sakei CRL1756 to salted environments through a proteomic approach, Food Res. Int. 54 (2013) 1334–1341, http://dx.doi.org/10.1016/j.foodres.2012.09.009.
DOI Google Scholar
[46]

L. Paulová, P. Patáková, B. Branská, et al., Lignocellulosic ethanol: technology design and its impact on process efficiency, Biotechnol. Adv. 33 (2014) 1091–1107, http://dx.doi.org/10.1016/j.biotechadv.2014.12.002.
DOI Google Scholar
[47]

B. Peng, S. Huang, T. Liu, et al., Bacterial xylose isomerases from the mammal gut Bacteroidetes cluster function in Saccharomyces cerevisiae for effective xylose fermentation, Microb. Cell Fact. 14 (2015) 70–83, http://dx.doi.org/10.1186/s12934-015-0253-1.
DOI Google Scholar
[48]

J.L. Botsford, T.A. Lewis, Osmoregulation in Rhizobium meliloti: production of glutamic acid in response to osmotic stress, Appl. Environ. Microbiol. 56 (1990) 488–499.
DOI Google Scholar
[49]

J. Norbeck, A. Blomberg, Amino acid uptake is strongly affected during exponential growth of Saccharomyces cerevisiae in 0.7 M NaCl medium, FEMS Microbiol. Lett. 158 (2010) 121–126, http://dx.doi.org/10.1016/S0378-1097(97)00511-9.
DOI Google Scholar
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Received: 26 October 2019
Revised: 09 March 2020
Accepted: 21 May 2020
Published: 03 June 2020
Issue date: January 2021

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