Improving ribonucleic acid production in Saccharomyces pastorianus via in silico genome-scale metabolic network model.


Journal

Biotechnology journal
ISSN: 1860-7314
Titre abrégé: Biotechnol J
Pays: Germany
ID NLM: 101265833

Informations de publication

Date de publication:
Nov 2023
Historique:
revised: 12 07 2023
received: 24 05 2023
accepted: 30 07 2023
medline: 13 11 2023
pubmed: 31 7 2023
entrez: 31 7 2023
Statut: ppublish

Résumé

Ribonucleic acid (RNA) and its degradation products are important biomolecules widely used in the food and pharmaceutical industries for their flavoring and nutritional functions. In this study, we used a genome-scale metabolic network model (GSMM) to explore genetic targets for nucleic acid synthesis in a Saccharomyces pastorianus strain (G03). Yeast 8.5.0 was used as the base model, which accurately predicted G03's growth. Using OptForce, we found that overexpression of ARO8 and ATP1 among six different strategies increased the RNA content of G03 by 58.0% and 74.8%, respectively. We also identified new metabolic targets for improved RNA production using a modified GSMM called TissueModel, constructed using the GIMME transcriptome constraint tool to remove low-expressed reactions in the model. After running OptKnock, the RNA content of G03-△BNA1 and G03-△PMA1 increased by 44.6% and 39.8%, respectively, compared to G03. We suggest that ATP1, ARO8, BNA1, and PMA1 regulate cell fitness, which affects RNA content. This study is the first to identify strategies for RNA overproduction using GSMM and to report that regulation of ATP1, ARO8, BNA1, and PMA1 can increase RNA content in S. pastorianus. These findings also provide valuable knowledge on model reconstruction for S. pastorianus.

Identifiants

pubmed: 37522392
doi: 10.1002/biot.202300240
doi:

Substances chimiques

RNA 63231-63-0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e2300240

Informations de copyright

© 2023 Wiley-VCH GmbH.

Références

Kurihara, K., & Kashiwayanagi, M. (2000). Physiological studies on umami taste. Journal of Nutrition, 130, 931S-934S.
Kato, M., Shiode, N., Teragawa, H., Hirao, H., Yamagata, T., Matsuura, H., & Kajiyama, G. (1999). Adenosine 5-triphosphate induced dilation of human coronary microvessels in vivo. Internal Medicine, 38, 324-329.
Knight, W., & Yan, C. (2013). Therapeutic potential of PDE modulation in treating heart disease. Future Medicinal Chemistry, 5, 1607-1620.
Zhang, P., Chen, J., Li, T., & Zhu, Y. Y. (2013). Use of small RNA as antiaging cosmeceuticals. Journal of Cosmetic Science, 64, 455-468.
Warner, J. R. (1999). The economics of ribosome biosynthesis in yeast. Trends in Biochemical Sciences, 24, 437-440.
Chen, H., Wang, J., Li, Q., Xu, X., Niu, C., Zheng, F., & Liu, C. (2022). Fed-batch fermentation of Saccharomyces pastorianus with high ribonucleic acid yield. Foods, 11, 11182742.
Chuwattanakul, V., Sugiyama, M., Khatun, F., Kurata, K., Tomita, I., Kaneko, Y., & Harashima, S. (2012). Increased transcription of NOP15, involved in ribosome biogenesis in Saccharomyces cerevisiae, enhances the production yield of RNA as a source of nucleotide seasoning. Journal of Bioscience and Bioengineering, 114, 17-22.
Chuwattanakul, V., Kim, Y.-H., Sugiyama, M., Nishiuchi, H., Nishiuchi, H., Miwa, H., Kaneko, Y., & Harashima, S. (2011). Construction of a Saccharomyces cerevisiae strain with a high level of RNA. Journal of Bioscience and Bioengineering, 112, 1-7.
Guo, X., Zhao, B., Zhou, X., Lu, D., Wang, Y., Chen, Y., & Xiao, D. (2021). Analysis of the molecular basis of Saccharomyces cerevisiae mutant with high nucleic acid content by comparative transcriptomics. Food Research International, 142, 110118.
Durot, M., Bourguignon, P.-Y., & Schachter, V. (2009). Genome-scale models of bacterial metabolism: Reconstruction and applications. FEMS Microbiology Review, 33, 164-190.
Vikromvarasiri, N., Noda, S., Shirai, T., & Kondo, A. (2023). Investigation of two metabolic engineering approaches for (R,R)-2,3-butanediol production from glycerol in Bacillus subtilis. Journal of Biological Engineering, 17, 3.
Yim, H., Haselbeck, R., Niu, W., Pujol-Baxley, C., Burgard, A., Boldt, J., Khandurina, J., Trawick, J. D., Osterhout, R. E., Stephen, R., Estadilla, J., Teisan, S., Schreyer, H. B., Andrae, S., Yang, T. H., Lee, S. Y., Burk, M. J., & Van Dien, S. (2011). Metabolic engineering of Escherichia coli for direct production of 1,4-butanediol. Nature Chemical Biology, 7, 445-452.
Paramasivan, K., Abdulla, A., Gupta, N., & Mutturi, S. (2022). In silico target-based strain engineering of Saccharomyces cerevisiae for terpene precursor improvement. Integrative Biology, 14, 25-36.
Ng, C. Y., Jung, M. Y., Lee, J., & Oh, M. K. (2012). Production of 2,3-butanediol in Saccharomyces cerevisiae by in silico aided metabolic engineering. Microbial Cell Factories, 11, 68.
Ranganathan, S., Suthers, P. F., & Maranas, C. D. (2010). OptForce: An optimization procedure for identifying all genetic manipulations leading to targeted overproductions. PLoS Computational Biology, 6, e1000744.
Burgard, A. P., Pharkya, P., & Maranas, C. D. (2003). OptKnock: A bilevel programming framework for identifying gene knockout strategies for microbial strain optimization. Biotechnology and Bioengineering, 84, 647-657.
Sasano, Y., Kariya, T., Usugi, S., Sugiyama, M., & Harashima, S. (2017). Molecular breeding of Saccharomyces cerevisiae with high RNA content by harnessing essential ribosomal RNA transcription regulator. AMB Express, 7, 32.
Gueldener, U., Heinisch, J., Koehler, G. J., Voss, D., & Hegemann, J. H. (2002). A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Research, 30, e23.
Zhang, G.-C., Kong, I. I., Kim, H., Liu, J.-J., Cate, J. H. D., & Jin, Y.-S. (2014). Construction of a quadruple auxotrophic mutant of an industrial polyploid Saccharomyces cerevisiae strain by using RNA-guided Cas9 nuclease. Applied and Environmental Microbiology, 80, 7694-7701.
Wang, M., Wu, F., & Gu, Z. (2022). Flow cytometric resolution of yeast is affected by enzymatic treatment and culture media. FEBS Open Bio, 12, 1623-1633.
Ludwig, C., Gillet, L., Rosenberger, G., Amon, S., & Collins, B. C., & Aebersold, R. (2018). Data-independent acquisition-based SWATH - MS for quantitative proteomics: A tutorial. Molecular Systems Biology, 14, e8126.
Nassar, A. F., Wu, T., Nassar, S. F., & Wisnewski, A. V. (2017). UPLC-MS for metabolomics: A giant step forward in support of pharmaceutical research. Drug Discovery Today, 22, 463-470.
Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M., & Tanabe, M. (2016). KEGG as a reference resource for gene and protein annotation. Nucleic Acid Research, 44, D457-D462.
Sayers, E. W., Bolton, E. E., Brister, J. R., Canese, K., Chan, J., Comeau, D. C., Connor, R., Funk, K., Kelly, C., Kim, S., Madej, T., Marchler-Bauer, A., Lanczycki, C., Lathrop, S., Lu, Z., Thibaud-Nissen, F., Murphy, T., Phan, L., Skripchenko, Y., … Sherry, S. T. (2022). Database resources of the National Center for Biotechnology Information. Nucleic Acid Research, 50, D20-D26.
DeJongh, M., Formsma, K., Boillot, P., Gould, J., Rycenga, M., & Best, A. (2007). Toward the automated generation of genome-scale metabolic networks in the SEED. BMC Bioinformatics, 8, 1-17.
Bordbar, A., Monk, J. M., King, Z. A., & Palsson, B. O. (2014). Constraint-based models predict metabolic and associated cellular functions. Nature Reviews Genetics, 15, 107-120.
Varvassori, S., Wang, K., Schweizer, L. M., & Schweizer, M. (2005). Ramifications of impaired PRPP synthesis in Saccharomyces cerevisiae. Biochemical Society Transactions, 33, 1418-1420.
Andre, B., & Jauniaux, J. C. (1990). Nucleotide sequence of the yeast UGA1 gene encoding GABA transaminase. Nucleic Acid Research, 18, 3049-3049.
Coleman, S. T., Fang, T. K., Rovinsky, S. A., Turano, F. J., & Moye-Rowley, W. S. (2001). Expression of a glutamate decarboxylase homologue is required for normal oxidative stress tolerance in Saccharomyces cerevisiae. Journal of Biological Chemistry, 276, 244-250.
Magarifuchi, T., Goto, K., Iimura, Y., Tadenuma, M., & Tamura, G. (1995). Effect of yeast fumarase gene (FUM1) disruption on production of malic, fumaric and succinic acids in sake mash. Journal of Fermentation and Bioengineering, 80, 355-361.
Paul, D., Chatterjee, A., Begley, T. P., & Ealick, S. E. (2010). Domain organization in Candida glabrata THI6, a bifunctional enzyme required for thiamin biosynthesis in eukaryotes. Biochemistry, 49, 9922-9934.
Förster, J., Famili, I., Fu, P., Palsson, B. O., & Nielsen, J. (2003). Genome-scale reconstruction of the Saccharomyces cerevisiae metabolic network. Genome Research, 13, 244-253.
Nandi, S., Subramanian, A., & Sarkar, R. R. (2017). An integrative machine learning strategy for improved prediction of essential genes in Escherichia coli metabolism using flux-coupled features. Molecular Biosystems, 13, 1584-1596.
Takeda, M., Chen, W. J., Saltzgaber, J., & Douglas, M. G. (1986). Nuclear genes encoding the yeast mitochondrial ATPase complex. Analysis of ATP1 coding the F1-ATPase alpha-subunit and its assembly. The Journal of Biological Chemistry, 261, 15126-15133.
Boyer, P. D. (1997). The ATP synthase - A splendid molecular machine. Annual Review of Biochemistry, 66, 717-749.
Abrahams, J. P., Lutter, R., Todd, R. J., Vanraaij, M. J., Leslie, A. G., & Walker, J. E. (1993). Inherent asymmetry of the structure of F1-ATPase from bovine heart mitochondria at 6.5 A resolution. The EMBO Journal, 12, 1775-1780.
Abrahams, J. P., Leslie, A. G. W., Lutter, R., & Walker, J. E. (1994). Structure at 2.8 Â resolution of F1-ATPase from bovine heart mitochondria. Nature, 370, 621-628.
Yin, S., Zhou, H., Xiao, X., Lang, T., Leslie, A. G., & Walker, J. E. (2015). Improving 2-phenylethanol production via ehrlich pathway using genetic engineered Saccharomyces cerevisiae strains. Current Microbiology, 70, 762-767.
Romagnoli, G., Knijnenburg, T. A., Liti, G., Louis, E. J., Pronk, J. T., & Daran, J.-M. (2015). Deletion of the Saccharomyces cerevisiae ARO8 gene, encoding an aromatic amino acid transaminase, enhances phenylethanol production from glucose. Yeast, 32, 29-45.
Etschmann, M. M. W., Bluemke, W., Sell, D., & Schrader, J. (2002). Biotechnological production of 2-phenylethanol. Applied Microbiology and Biotechnology, 59, 1-8.
Bedalov, A., Hirao, M., Posakony, J., Nelson, M., & Simon, J. A. (2003). NAD+-dependent deacetylase Hst1p controls biosynthesis and cellular NAD+ levels in Saccharomyces cerevisiae. Molecular & Cellular Biology, 23, 7044.
Kucharczyk, R., Zagulski, M., Rytka, J., & Herbert, C. J. (1998). The yeast gene YJR025c encodes a 3-hydroxyanthranilic acid dioxygenase and is involved in nicotinic acid biosynthesis. FEBS Letters, 424, 127-130.
dExaerde, A. D., Supply, P., & Goffeau, A. (1996). Review: Subcellular traffic of the plasma membrane H+-ATPase in Saccharomyces cerevisiae. Yeast, 12, 907-916.
Bertoli, C., Skotheim, J. M., & de Bruin, R. A. M. (2013). Control of cell cycle transcription during G1 and S phases. Nature Reviews Molecular Cell Biology, 14, 518-528.
Muro, M., Izumi, K., Imai, T., Ogawa, Y., & Ohkochi, M. (2006). Yeast cell cycle during fermentation and beer quality. Journal of the American Society of Brewing Chemists, 64, 151-154.

Auteurs

Hao Chen (H)

Key Laboratory of Industrial Biotechnology, School of Biotechnology, Ministry of Education, Jiangnan University, Wuxi, China.
Lab of Brewing Science and Technology, School of Biotechnology, Jiangnan University, Wuxi, China.
School of Biotechnology, Jiangnan University, Wuxi, Jiangsu, China.

Qi Li (Q)

Key Laboratory of Industrial Biotechnology, School of Biotechnology, Ministry of Education, Jiangnan University, Wuxi, China.
Lab of Brewing Science and Technology, School of Biotechnology, Jiangnan University, Wuxi, China.
School of Biotechnology, Jiangnan University, Wuxi, Jiangsu, China.

Jinjing Wang (J)

Key Laboratory of Industrial Biotechnology, School of Biotechnology, Ministry of Education, Jiangnan University, Wuxi, China.
Lab of Brewing Science and Technology, School of Biotechnology, Jiangnan University, Wuxi, China.
School of Biotechnology, Jiangnan University, Wuxi, Jiangsu, China.

Chengtuo Niu (C)

Key Laboratory of Industrial Biotechnology, School of Biotechnology, Ministry of Education, Jiangnan University, Wuxi, China.
Lab of Brewing Science and Technology, School of Biotechnology, Jiangnan University, Wuxi, China.
School of Biotechnology, Jiangnan University, Wuxi, Jiangsu, China.

Feiyun Zheng (F)

Key Laboratory of Industrial Biotechnology, School of Biotechnology, Ministry of Education, Jiangnan University, Wuxi, China.
Lab of Brewing Science and Technology, School of Biotechnology, Jiangnan University, Wuxi, China.
School of Biotechnology, Jiangnan University, Wuxi, Jiangsu, China.

Chunfeng Liu (C)

Key Laboratory of Industrial Biotechnology, School of Biotechnology, Ministry of Education, Jiangnan University, Wuxi, China.
Lab of Brewing Science and Technology, School of Biotechnology, Jiangnan University, Wuxi, China.
School of Biotechnology, Jiangnan University, Wuxi, Jiangsu, China.

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Classifications MeSH