Proteomic and metabolomic analysis of the carotenogenic yeast Xanthophyllomyces dendrorhous using different carbon sources

Martinez-Moya P, Niehaus K, Alcaino J, Baeza M, Cifuentes V (2015)
BMC Genomics 16(1): 289.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Martinez-Moya, Pilar; Niehaus, KarstenUniBi; Alcaino, Jennifer; Baeza, Marcelo; Cifuentes, Victor
Abstract / Bemerkung
Background: Astaxanthin is a potent antioxidant with increasing biotechnological interest. In Xanthophyllomyces dendrorhous, a natural source of this pigment, carotenogenesis is a complex process regulated through several mechanisms, including the carbon source. X. dendrorhous produces more astaxanthin when grown on a non-fermentable carbon source, while decreased astaxanthin production is observed in the presence of high glucose concentrations. In the present study, we used a comparative proteomic and metabolomic analysis to characterize the yeast response when cultured in minimal medium supplemented with glucose (fermentable) or succinate (non-fermentable). Results: A total of 329 proteins were identified from the proteomic profiles, and most of these proteins were associated with carotenogenesis, lipid and carbohydrate metabolism, and redox and stress responses. The metabolite profiles revealed 92 metabolites primarily associated with glycolysis, the tricarboxylic acid cycle, amino acids, organic acids, sugars and phosphates. We determined the abundance of proteins and metabolites of the central pathways of yeast metabolism and examined the influence of these molecules on carotenogenesis. Similar to previous proteomic-stress response studies, we observed modulation of abundance from several redox, stress response, carbohydrate and lipid enzymes. Additionally, the accumulation of trehalose, absence of key ROS response enzymes, an increased abundance of the metabolites of the pentose phosphate pathway and tricarboxylic acid cycle suggested an association between the accumulation of astaxanthin and oxidative stress in the yeast. Moreover, we observed the increased abundance of late carotenogenesis enzymes during astaxanthin accumulation under succinate growth conditions. Conclusions: The use of succinate as a carbon source in X. dendrorhous cultures increases the availability of acetyl-CoA for the astaxanthin production compared with glucose, likely reflecting the positive regulation of metabolic enzymes of the tricarboxylic acid and glyoxylate cycles. The high metabolite level generated in this pathway could increase the cellular respiration rate, producing reactive oxygen species, which induces carotenogenesis.
Stichworte
Astaxanthin; Carbon source; Metabolomics; Proteomics; Carotenogenesis; ROS
Erscheinungsjahr
2015
Zeitschriftentitel
BMC Genomics
Band
16
Ausgabe
1
Art.-Nr.
289
ISSN
1471-2164
Page URI
https://pub.uni-bielefeld.de/record/2736454

Zitieren

Martinez-Moya P, Niehaus K, Alcaino J, Baeza M, Cifuentes V. Proteomic and metabolomic analysis of the carotenogenic yeast Xanthophyllomyces dendrorhous using different carbon sources. BMC Genomics. 2015;16(1): 289.
Martinez-Moya, P., Niehaus, K., Alcaino, J., Baeza, M., & Cifuentes, V. (2015). Proteomic and metabolomic analysis of the carotenogenic yeast Xanthophyllomyces dendrorhous using different carbon sources. BMC Genomics, 16(1), 289. doi:10.1186/s12864-015-1484-6
Martinez-Moya, P., Niehaus, K., Alcaino, J., Baeza, M., and Cifuentes, V. (2015). Proteomic and metabolomic analysis of the carotenogenic yeast Xanthophyllomyces dendrorhous using different carbon sources. BMC Genomics 16:289.
Martinez-Moya, P., et al., 2015. Proteomic and metabolomic analysis of the carotenogenic yeast Xanthophyllomyces dendrorhous using different carbon sources. BMC Genomics, 16(1): 289.
P. Martinez-Moya, et al., “Proteomic and metabolomic analysis of the carotenogenic yeast Xanthophyllomyces dendrorhous using different carbon sources”, BMC Genomics, vol. 16, 2015, : 289.
Martinez-Moya, P., Niehaus, K., Alcaino, J., Baeza, M., Cifuentes, V.: Proteomic and metabolomic analysis of the carotenogenic yeast Xanthophyllomyces dendrorhous using different carbon sources. BMC Genomics. 16, : 289 (2015).
Martinez-Moya, Pilar, Niehaus, Karsten, Alcaino, Jennifer, Baeza, Marcelo, and Cifuentes, Victor. “Proteomic and metabolomic analysis of the carotenogenic yeast Xanthophyllomyces dendrorhous using different carbon sources”. BMC Genomics 16.1 (2015): 289.

11 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

CAR gene cluster and transcript levels of carotenogenic genes in Rhodotorula mucilaginosa.
Landolfo S, Ianiri G, Camiolo S, Porceddu A, Mulas G, Chessa R, Zara G, Mannazzu I., Microbiology 164(1), 2018
PMID: 29219805
A common mechanism explains the induction of aerobic fermentation and adaptive antioxidant response in Phaffia rhodozyma.
Martínez-Cárdenas A, Chávez-Cabrera C, Vasquez-Bahena JM, Flores-Cotera LB., Microb Cell Fact 17(1), 2018
PMID: 29615045
Proteomic analysis of astaxanthin biosynthesis in Xanthophyllomyces dendrorhous in response to low carbon levels.
Pan X, Wang B, Gerken HG, Lu Y, Ling X., Bioprocess Biosyst Eng 40(7), 2017
PMID: 28455664
Mining terpenoids production and biosynthetic pathway in thraustochytrids.
Xie Y, Sen B, Wang G., Bioresour Technol 244(pt 2), 2017
PMID: 28549813
Biosynthesis of Astaxanthin as a Main Carotenoid in the Heterobasidiomycetous Yeast Xanthophyllomyces dendrorhous.
Barredo JL, García-Estrada C, Kosalkova K, Barreiro C., J Fungi (Basel) 3(3), 2017
PMID: 29371561
Proteomic analysis of Rhodotorula mucilaginosa: dealing with the issues of a non-conventional yeast.
Addis MF, Tanca A, Landolfo S, Abbondio M, Cutzu R, Biosa G, Pagnozzi D, Uzzau S, Mannazzu I., Yeast 33(8), 2016
PMID: 26987668
Comparative genomics provides new insights into the diversity, physiology, and sexuality of the only industrially exploited tremellomycete: Phaffia rhodozyma.
Bellora N, Moliné M, David-Palma M, Coelho MA, Hittinger CT, Sampaio JP, Gonçalves P, Libkind D., BMC Genomics 17(1), 2016
PMID: 27829365
Red yeasts and carotenoid production: outlining a future for non-conventional yeasts of biotechnological interest.
Mannazzu I, Landolfo S, Lopes da Silva T, Buzzini P., World J Microbiol Biotechnol 31(11), 2015
PMID: 26335057
Red yeasts and carotenoid production: outlining a future for non-conventional yeasts of biotechnological interest
Mannazzu I, Landolfo S, da Silva TL, Buzzini P., World J Microbiol Biotechnol 31(11), 2015
PMID: IND604401108

55 References

Daten bereitgestellt von Europe PubMed Central.

Biotechnological production of astaxanthin with Phaffia rhodozyma/Xanthophyllomyces dendrorhous.
Schmidt I, Schewe H, Gassel S, Jin C, Buckingham J, Humbelin M, Sandmann G, Schrader J., Appl. Microbiol. Biotechnol. 89(3), 2010
PMID: 21046372
Xanthophyllomyces dendrorhous for the industrial production of astaxanthin.
Rodriguez-Saiz M, de la Fuente JL, Barredo JL., Appl. Microbiol. Biotechnol. 88(3), 2010
PMID: 20711573
Enhancement of carotenoid production by disrupting the C22-sterol desaturase gene (CYP61) in Xanthophyllomyces dendrorhous.
Loto I, Gutierrez MS, Barahona S, Sepulveda D, Martinez-Moya P, Baeza M, Cifuentes V, Alcaino J., BMC Microbiol. 12(), 2012
PMID: 23075035
Increase in the astaxanthin synthase gene (crtS) dose by in vivo DNA fragment assembly in Xanthophyllomyces dendrorhous.
Contreras G, Barahona S, Rojas MC, Baeza M, Cifuentes V, Alcaino J., BMC Biotechnol. 13(), 2013
PMID: 24103677
Regulation of the mevalonate pathway.
Goldstein JL, Brown MS., Nature 343(6257), 1990
PMID: 1967820
Isolation and functional characterisation of a novel type of carotenoid biosynthetic gene from Xanthophyllomyces dendrorhous.
Verdoes JC, Krubasik KP, Sandmann G, van Ooyen AJ., Mol. Gen. Genet. 262(3), 1999
PMID: 10589832
Cloning of the astaxanthin synthase gene from Xanthophyllomyces dendrorhous (Phaffia rhodozyma) and its assignment as a beta-carotene 3-hydroxylase/4-ketolase.
Ojima K, Breitenbach J, Visser H, Setoguchi Y, Tabata K, Hoshino T, van den Berg J, Sandmann G., Mol. Genet. Genomics 275(2), 2006
PMID: 16416328
Cloning of the cytochrome p450 reductase (crtR) gene and its involvement in the astaxanthin biosynthesis of Xanthophyllomyces dendrorhous.
Alcaino J, Barahona S, Carmona M, Lozano C, Marcoleta A, Niklitschek M, Sepulveda D, Baeza M, Cifuentes V., BMC Microbiol. 8(), 2008
PMID: 18837978
Singlet oxygen and peroxyl radicals regulate carotenoid biosynthesis in Phaffia rhodozyma.
Schroeder WA, Johnson EA., J. Biol. Chem. 270(31), 1995
PMID: 7629161
Effects of oxygen supply on growth and carotenoids accumulation by Xanthophyllomyces dendrorhous.
Wang W, Yu L., Z. Naturforsch., C, J. Biosci. 64(11-12), 2009
PMID: 20158157
Influence of oxygen and glucose on primary metabolism and astaxanthin production by Phaffia rhodozyma in batch and fed-batch cultures: kinetic and stoichiometric analysis
Yamane Y, Higashida K, Nakashimada Y, Kakizono T, Nishio N., 1997
"Glucose and ethanol-dependent transcriptional regulation of the astaxanthin biosynthesis pathway in Xanthophyllomyces dendrorhous".
Marcoleta A, Niklitschek M, Wozniak A, Lozano C, Alcaino J, Baeza M, Cifuentes V., BMC Microbiol. 11(), 2011
PMID: 21861883
Proteomic analysis of the carotenogenic yeast Xanthophyllomyces dendrorhous.
Martinez-Moya P, Watt SA, Niehaus K, Alcaino J, Baeza M, Cifuentes V., BMC Microbiol. 11(), 2011
PMID: 21669001
Differential carotenoid production and gene expression in Xanthophyllomyces dendrorhous grown in a nonfermentable carbon source.
Wozniak A, Lozano C, Barahona S, Niklitschek M, Marcoleta A, Alcaino J, Sepulveda D, Baeza M, Cifuentes V., FEMS Yeast Res. 11(3), 2011
PMID: 21205159
A parallel proteomic and metabolomic analysis of the hydrogen peroxide- and Sty1p-dependent stress response in Schizosaccharomyces pombe.
Weeks ME, Sinclair J, Butt A, Chung YL, Worthington JL, Wilkinson CR, Griffiths J, Jones N, Waterfield MD, Timms JF., Proteomics 6(9), 2006
PMID: 16548067
Proteomics and redox-proteomics of the effects of herbicides on a wild-type wine Saccharomyces cerevisiae strain.
Braconi D, Bernardini G, Possenti S, Laschi M, Arena S, Scaloni A, Geminiani M, Sotgiu M, Santucci A., J. Proteome Res. 8(1), 2009
PMID: 19032026
Mitochondrial oxidative phosphorylation is regulated by fructose 1,6-bisphosphate. A possible role in Crabtree effect induction?
Diaz-Ruiz R, Averet N, Araiza D, Pinson B, Uribe-Carvajal S, Devin A, Rigoulet M., J. Biol. Chem. 283(40), 2008
PMID: 18682403
Regulation of xylose metabolism in recombinant Saccharomyces cerevisiae.
Salusjarvi L, Kankainen M, Soliymani R, Pitkanen JP, Penttila M, Ruohonen L., Microb. Cell Fact. 7(), 2008
PMID: 18533012
Comparative proteome analysis of Saccharomyces cerevisiae grown in chemostat cultures limited for glucose or ethanol.
Kolkman A, Olsthoorn MM, Heeremans CE, Heck AJ, Slijper M., Mol. Cell Proteomics 4(1), 2004
PMID: 15502163
A proteomic view of Candida albicans yeast cell metabolism in exponential and stationary growth phases.
Kusch H, Engelmann S, Bode R, Albrecht D, Morschhauser J, Hecker M., Int. J. Med. Microbiol. 298(3-4), 2007
PMID: 17588813
A comparative transcriptomic, fluxomic and metabolomic analysis of the response of Saccharomyces cerevisiae to increases in NADPH oxidation.
Celton M, Sanchez I, Goelzer A, Fromion V, Camarasa C, Dequin S., BMC Genomics 13(), 2012
PMID: 22805527
Posttranslational, translational, and transcriptional responses to nitric oxide stress in Cryptococcus neoformans: implications for virulence.
Missall TA, Pusateri ME, Donlin MJ, Chambers KT, Corbett JA, Lodge JK., Eukaryotic Cell 5(3), 2006
PMID: 16524907
Succinate modulation of H2O2 release at NADH:ubiquinone oxidoreductase (Complex I) in brain mitochondria.
Zoccarato F, Cavallini L, Bortolami S, Alexandre A., Biochem. J. 406(1), 2007
PMID: 17477844
Metabolic network analysis on Phaffia rhodozyma yeast using 13C-labeled glucose and gas chromatography-mass spectrometry.
Cannizzaro C, Christensen B, Nielsen J, von Stockar U., Metab. Eng. 6(4), 2004
PMID: 15491863
Functional analyses of two acetyl coenzyme A synthetases in the ascomycete Gibberella zeae.
Lee S, Son H, Lee J, Min K, Choi GJ, Kim JC, Lee YW., Eukaryotic Cell 10(8), 2011
PMID: 21666077
ATP-citrate lyase activity and carotenoid production in batch cultures of Phaffia rhodozyma under nitrogen-limited and nonlimited conditions.
Chavez-Cabrera C, Flores-Bustamante ZR, Marsch R, Montes Mdel C, Sanchez S, Cancino-Diaz JC, Flores-Cotera LB., Appl. Microbiol. Biotechnol. 85(6), 2009
PMID: 19809811
Effects of excess succinate and retrograde control of metabolite accumulation in yeast tricarboxylic cycle mutants.
Lin AP, Anderson SL, Minard KI, McAlister-Henn L., J. Biol. Chem. 286(39), 2011
PMID: 21841001
Reactive oxygen species in regulation of fungal development.
Gessler NN, Aver'yanov AA, Belozerskaya TA., Biochemistry Mosc. 72(10), 2007
PMID: 18021067
[The stress response in the yeast Saccharomyces cerevisiae].
Folch-Mallol JL, Garay-Arroyo A, Lledias F, Covarrubias Robles AA., Rev. Latinoam. Microbiol. 46(1-2), 2004
PMID: 17061523
Reactive oxygen species and cellular oxygen sensing.
Cash TP, Pan Y, Simon MC., Free Radic. Biol. Med. 43(9), 2007
PMID: 17893032
Redox control and oxidative stress in yeast cells.
Herrero E, Ros J, Belli G, Cabiscol E., Biochim. Biophys. Acta 1780(11), 2007
PMID: 18178164
Protection against oxidation during dehydration of yeast.
Pereira Ede J, Panek AD, Eleutherio EC., Cell Stress Chaperones 8(2), 2003
PMID: 14627197
NADH-reductive stress in Saccharomyces cerevisiae induces the expression of the minor isoform of glyceraldehyde-3-phosphate dehydrogenase (TDH1).
Valadi H, Valadi A, Ansell R, Gustafsson L, Adler L, Norbeck J, Blomberg A., Curr. Genet. 45(2), 2003
PMID: 14652693
Remodeling of yeast genome expression in response to environmental changes.
Causton HC, Ren B, Koh SS, Harbison CT, Kanin E, Jennings EG, Lee TI, True HL, Lander ES, Young RA., Mol. Biol. Cell 12(2), 2001
PMID: 11179418
Global transcriptional responses of fission yeast to environmental stress.
Chen D, Toone WM, Mata J, Lyne R, Burns G, Kivinen K, Brazma A, Jones N, Bahler J., Mol. Biol. Cell 14(1), 2003
PMID: 12529438
The mevalonate pathway in C. elegans.
Rauthan M, Pilon M., Lipids Health Dis 10(), 2011
PMID: 22204706
Controlling the false discovery rate: a practical and powerful approach to multiple testing
Benjamini Y, Hochberg Y., 1995

AUTHOR UNKNOWN, 0
Technical advance: simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry.
Roessner U, Wagner C, Kopka J, Trethewey RN, Willmitzer L., Plant J. 23(1), 2000
PMID: 10929108
Isolation of Phaffia rhodozyma Mutants with Increased Astaxanthin Content.
An GH, Schuman DB, Johnson EA., Appl. Environ. Microbiol. 55(1), 1989
PMID: 16347815

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