Production of D-glucaric acid with phosphoglucose isomerase-deficient Saccharomyces cerevisiae.
Glucarate
Glucaric acid
Metabolic engineering
Myo-inositol
Phosphoglucose isomerase
Saccharomyces cerevisiae
Journal
Biotechnology letters
ISSN: 1573-6776
Titre abrégé: Biotechnol Lett
Pays: Netherlands
ID NLM: 8008051
Informations de publication
Date de publication:
08 Dec 2023
08 Dec 2023
Historique:
received:
19
04
2023
accepted:
17
10
2023
revised:
14
07
2023
medline:
8
12
2023
pubmed:
8
12
2023
entrez:
8
12
2023
Statut:
aheadofprint
Résumé
D-Glucaric acid is a potential biobased platform chemical. Previously mainly Escherichia coli, but also the yeast Saccharomyces cerevisiae, and Pichia pastoris, have been engineered for conversion of D-glucose to D-glucaric acid via myo-inositol. One reason for low yields from the yeast strains is the strong flux towards glycolysis. Thus, to decrease the flux of D-glucose to biomass, and to increase D-glucaric acid yield, the four step D-glucaric acid pathway was introduced into a phosphoglucose isomerase deficient (Pgi1p-deficient) Saccharomyces cerevisiae strain. High D-glucose concentrations are toxic to the Pgi1p-deficient strains, so various feeding strategies and use of polymeric substrates were studied. Uniformly labelled
Identifiants
pubmed: 38064042
doi: 10.1007/s10529-023-03443-2
pii: 10.1007/s10529-023-03443-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Academy of Finland
ID : 118573
Organisme : Academy of Finland
ID : 310191
Organisme : European comission
ID : FP7-241566
Informations de copyright
© 2023. The Author(s).
Références
Abbott DA, Zelle RM, Pronk JT, van Maris AJ (2009) Metabolic engineering of Saccharomyces cerevisiae for production of carboxylic acids: current status and challenges. FEMS Yeast Res 9:1123–1136. https://doi.org/10.1111/j.1567-1364.2009.00537.x
doi: 10.1111/j.1567-1364.2009.00537.x
pubmed: 19566685
Blank LM, Lehmbeck F, Sauer U (2005) Metabolic-flux and network analysis in fourteen hemiascomycetous yeasts. FEMS Yeast Res 5:545–558. https://doi.org/10.1016/j.femsyr.2004.09.008
doi: 10.1016/j.femsyr.2004.09.008
pubmed: 15780654
Boer H, Maaheimo H, Koivula A, Penttilä M, Richard P (2010) Identification in Agrobacterium tumefaciens of the D-galacturonic acid dehydrogenase gene. Appl Microbiol Biotechnol 86:901–909. https://doi.org/10.1007/s00253-009-2333-9
doi: 10.1007/s00253-009-2333-9
pubmed: 19921179
Brockman IM, Prather KLJ (2015) Dynamic metabolic engineering: New strategies for developing responsive cell factories. Biotechnol J 10:1360–1369. https://doi.org/10.1002/biot.201400422
doi: 10.1002/biot.201400422
pubmed: 25868062
pmcid: 4629492
Cheah LC, Stark T, Adamson LSR, Abidin RS, Lau YH, Sainsbury F, Vickers CE (2021) Artificial self-assembling nanocompartment for organizing metabolic pathways in yeast. ACS Synth Biol 10:3251–3263. https://doi.org/10.1021/acssynbio.1c00045
doi: 10.1021/acssynbio.1c00045
pubmed: 34591448
pmcid: 8689640
Chen N, Wang J, Zhao Y, Deng Y (2018) Metabolic engineering of Saccharomyces cerevisiae for efficient production of glucaric acid at high titer. Microb Cell Fact 17:1–11. https://doi.org/10.1186/s12934-018-0914-y
doi: 10.1186/s12934-018-0914-y
pubmed: 29306327
pmcid: 5756420
Chen L-Z, Huang S-L, Hou J, Guo X-P, Wang F-S, Sheng J-Z (2020) Cell-based and cell-free biocatalysis for the production of D-glucaric acid. Biotechnol Biofuels 13:203. https://doi.org/10.1186/s13068-020-01847-0
doi: 10.1186/s13068-020-01847-0
pubmed: 33303009
pmcid: 7731778
Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P (1992) Multifunctional yeast high-copy-number shuttle vectors. Gene 110:119–122. https://doi.org/10.1016/0378-1119(92)90454-w
doi: 10.1016/0378-1119(92)90454-w
pubmed: 1544568
Ciriacy M, Breitenbach I (1979) Physiological effects of seven different blocks in glycolysis in Saccharomyces cerevisiae. J Bacteriol 139:152–160
doi: 10.1128/jb.139.1.152-160.1979
pubmed: 378952
pmcid: 216840
de Koning W, van Dam K (1992) A method for the determination of changes of glycolytic metabolites in yeast on a subsecond time scale using extraction at neutral pH. Anal Biochem 204:118–123
doi: 10.1016/0003-2697(92)90149-2
pubmed: 1514678
Doong SJ, Gupta A, Prather KLJ (2018) Layered dynamic regulation for improving metabolic pathway productivity in Escherichia coli. PNAS 115:2964–2969. https://doi.org/10.1073/pnas.1716920115
doi: 10.1073/pnas.1716920115
pubmed: 29507236
pmcid: 5866568
Dueber JE, Wu GC, Malmirchegini GR, Moon TS, Petzold CJ, Ullal AV, Prather KL, Keasling JD (2009) Synthetic protein scaffolds provide modular control over metabolic flux. Nat Biotechnol 27:753–759. https://doi.org/10.1038/nbt.1557
doi: 10.1038/nbt.1557
pubmed: 19648908
Fang H, Deng Y, Pan Y, Li C, Yu L (2022) Distributive and collaborative push-and-pull in an artificial microbial consortium for improved consolidated bioprocessing. AIChE J 68:e17844. https://doi.org/10.1002/AIC.17844
doi: 10.1002/AIC.17844
Fang H, Zhao C, Li C, Song Y, Yu L, Song X, Wu J, Yang L (2023) Direct consolidated bioprocessing for D-glucaric acid production from lignocellulose under subcritical water pretreatment. J Chem Eng 454:140339. https://doi.org/10.1016/J.CEJ.2022.140339
doi: 10.1016/J.CEJ.2022.140339
Fiaux J, Cakar ZP, Sonderegger M, Wuthrich K, Szyperski T, Sauer U (2003) Metabolic-flux profiling of the yeasts Saccharomyces cerevisiae and Pichia stipitis. Eukaryot Cell 2:170–180. https://doi.org/10.1128/ec.2.1.170-180.2003
doi: 10.1128/ec.2.1.170-180.2003
pubmed: 12582134
pmcid: 141173
Gancedo JM, Lagunas R (1973) Contribution of the pentose-phosphate pathway to glucose metabolism in Saccharomyces cerevisiae: a critical analysis on the use of labelled glucose. Plant Sci Lett 1:193–200
doi: 10.1016/0304-4211(73)90044-8
Gancedo C, Serrano R (1989) Energy yielding metabolism. In: Rose AH, Harrison JS (eds) The yeasts. Academic press, Cambridge, pp 205–259
Gietz RD, Sugino A (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74:527–534
doi: 10.1016/0378-1119(88)90185-0
pubmed: 3073106
Gueldener U, Heinisch J, Koehler GJ, Voss D, Hegemann JH (2002) A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res 30:e23. https://doi.org/10.1093/NAR/30.6.E23
doi: 10.1093/NAR/30.6.E23
pubmed: 11884642
pmcid: 101367
Guo L, Qi M, Gao C, Ye C, Hu G, Song W, Wu J, Liu L, Chen X (2022) Engineering microbial cell viability for enhancing chemical production by second codon engineering. Metab Eng 73:235–246. https://doi.org/10.1016/J.YMBEN.2022.08.008
doi: 10.1016/J.YMBEN.2022.08.008
pubmed: 35987432
Gupta A, Hicks MA, Manchester SP, Prather KLJ (2016) Porting the synthetic D-glucaric acid pathway from Escherichia coli to Saccharomyces cerevisiae. Biotechnol J 11:1201–1208. https://doi.org/10.1002/biot.201500563
doi: 10.1002/biot.201500563
pubmed: 27312887
Gupta A, Reizman IMB, Reisch CR, Prather KLJ (2017) Dynamic regulation of metabolic flux in engineered bacteria using a pathway-independent quorum-sensing circuit. Nat Biotechnol 35:273–279. https://doi.org/10.1038/nbt.3796
doi: 10.1038/nbt.3796
pubmed: 28191902
pmcid: 5340623
Henry SA, Gaspar ML, Jesch SA (2014) The response to inositol: regulation of glycerolipid metabolism and stress response signaling in yeast. Chem Phys Lipids 180:23–43. https://doi.org/10.1016/J.CHEMPHYSLIP.2013.12.013
doi: 10.1016/J.CHEMPHYSLIP.2013.12.013
pubmed: 24418527
Heux S, Cadiere A, Dequin S (2008) Glucose utilization of strains lacking PGI1 and expressing a transhydrogenase suggests differences in the pentose phosphate capacity among Saccharomyces cerevisiae strains. FEMS Yeast Res 8:217–224. https://doi.org/10.1111/J.1567-1364.2007.00330.X
doi: 10.1111/J.1567-1364.2007.00330.X
pubmed: 18036177
Hou J, Gao C, Guo L, Nielsen J, Ding Q, Tang W, Hu G, Chen X, Liu L (2020) Rewiring carbon flux in Escherichia coli using a bifunctional molecular switch. Metab Eng 61:47–57. https://doi.org/10.1016/J.YMBEN.2020.05.004
doi: 10.1016/J.YMBEN.2020.05.004
pubmed: 32416271
Lee CC, Kibblewhite RE, Paavola CD, Orts WJ, Wagschal K (2016) Production of glucaric acid from hemicellulose substrate by rosettasome enzyme assemblies. Mol Biotechnol 58:489–496. https://doi.org/10.1007/s12033-016-9945-y
doi: 10.1007/s12033-016-9945-y
pubmed: 27198564
Li C, Lin X, Ling X, Li S, Fang H (2021) Consolidated bioprocessing of lignocellulose for production of glucaric acid by an artificial microbial consortium. Biotechnol Biofuels 14:1–16. https://doi.org/10.1186/S13068-021-01961-7
doi: 10.1186/S13068-021-01961-7
Lien OG (1959) Determination of gluconolactone, galactonolactone and their free acids by the hydroxamate method. Anal Chem 31:1363–1366
doi: 10.1021/ac60152a035
Liu Y, Gong X, Wang C, Du G, Chen J, Kang Z (2016) Production of glucaric acid from myo-inositol in engineered Pichia pastoris. Enzyme Microb 91:8–16. https://doi.org/10.1016/j.enzmictec.2016.05.009
doi: 10.1016/j.enzmictec.2016.05.009
Maaheimo H, Fiaux J, Cakar ZP, Bailey JE, Sauer U, Szyperski T (2001) Central carbon metabolism of Saccharomyces cerevisiae explored by biosynthetic fractional
doi: 10.1046/j.1432-1327.2001.02126.x
pubmed: 11298766
Maitra PK (1971) Glucose and fructose metabolism in a phosphoglucoseisomeraseless mutant of Saccharomyces cerevisiae. J Bacteriol 107:759–769
doi: 10.1128/jb.107.3.759-769.1971
pubmed: 5095288
pmcid: 246998
Marques WL, Anderson LA, Sandoval L, Hicks MA, Prather KLJ (2020) Sequence-based bioprospecting of myo-inositol oxygenase (Miox) reveals new homologues that increase glucaric acid production in Saccharomyces cerevisiae. Enzyme Microb 140:109623. https://doi.org/10.1016/J.ENZMICTEC.2020.109623
doi: 10.1016/J.ENZMICTEC.2020.109623
Moon TS, Yoon SH, Lanza AM, Roy-Mayhew JD, Prather KL (2009) Production of glucaric acid from a synthetic pathway in recombinant Escherichia coli. AEM 75:589–595. https://doi.org/10.1128/AEM.00973-08
doi: 10.1128/AEM.00973-08
Moon TS, Dueber JE, Shiue E, Prather KL (2010) Use of modular, synthetic scaffolds for improved production of glucaric acid in engineered E. coli. Metab Eng 12:298–305. https://doi.org/10.1016/j.ymben.2010.01.003
doi: 10.1016/j.ymben.2010.01.003
pubmed: 20117231
Nidelet T, Brial P, Camarasa C, Dequin S (2016) Diversity of flux distribution in central carbon metabolism of S. cerevisiae strains from diverse environments. Microb Cell Fact 15:1–13. https://doi.org/10.1186/S12934-016-0456-0
doi: 10.1186/S12934-016-0456-0
Nygård Y, Toivari MH, Penttilä M, Ruohonen L, Wiebe MG (2011) Bioconversion of D-xylose to D-xylonate with Kluyveromyces lactis. Metab Eng 13:383–391. https://doi.org/10.1016/j.ymben.2011.04.001
doi: 10.1016/j.ymben.2011.04.001
pubmed: 21515401
Petroll K, Care A, Bergquist PL, Sunna A (2020) A novel framework for the cell-free enzymatic production of glucaric acid. Metab Eng 57:162–173. https://doi.org/10.1016/j.ymben.2019.11.003
doi: 10.1016/j.ymben.2019.11.003
pubmed: 31726216
Qu YN, Yan HJ, Guo Q, Li JL, Ruan YC, Yue XZ, Zheng WX, Tan TW, Fan LH (2018) Biosynthesis of D-glucaric acid from sucrose with routed carbon distribution in metabolically engineered Escherichia coli. Metab Eng 47:393–400. https://doi.org/10.1016/j.ymben.2018.04.020
doi: 10.1016/j.ymben.2018.04.020
pubmed: 29715517
Raman S, Rogers JK, Taylor ND, Church GM (2014) Evolution-guided optimization of biosynthetic pathways. PNAS 111:17803–17808. https://doi.org/10.1073/pnas.1409523111
doi: 10.1073/pnas.1409523111
pubmed: 25453111
pmcid: 4273373
Reizman IMB, Stenger AR, Reisch CR, Gupta A, Connors NC, Prather KLJ (2015) Improvement of glucaric acid production in E. coli via dynamic control of metabolic fluxes. Metab Eng Commun 2:109–116. https://doi.org/10.1016/J.METENO.2015.09.002
doi: 10.1016/J.METENO.2015.09.002
pubmed: 26478859
pmcid: 4606470
Rogers JK, Church GM (2016) Genetically encoded sensors enable real-time observation of metabolite production. PNAS 113:2388–2393. https://doi.org/10.1073/pnas.1600375113
doi: 10.1073/pnas.1600375113
pubmed: 26858408
pmcid: 4780645
Sakuta R, Nakamura N (2019) Production of hexaric acids from biomass. International J Mol Sci 20:3660. https://doi.org/10.3390/IJMS20153660
doi: 10.3390/IJMS20153660
Salusjärvi L, Toivari M, Vehkomäki M-L, Koivistoinen O, Mojzita D, Niemelä K, Penttilä M, Ruohonen L (2017) Production of ethylene glycol or glycolic acid from D-xylose in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 101:8151–8163. https://doi.org/10.1007/s00253-017-8547-3
doi: 10.1007/s00253-017-8547-3
pubmed: 29038973
Sherman F, Fink G, Hicks JB (1983) Methods in yeast genetics: A laboratory manual. Cold Springs Harbor Laboratory, Cold Springs Harbor
Shiue E, Prather KLJ (2014) Improving D-glucaric acid production from myo-inositol in E. coli by increasing MIOX stability and myo-inositol transport. Metab Eng 22:22–31. https://doi.org/10.1016/j.ymben.2013.12.002
doi: 10.1016/j.ymben.2013.12.002
pubmed: 24333274
Shiue E, Brockman IM, Prather KLJ (2015) Improving product yields on D-glucose in Escherichia coli via knockout of pgi and zwf and feeding of supplemental carbon sources. Biotechnol Bioeng 112:579–587. https://doi.org/10.1002/BIT.25470
doi: 10.1002/BIT.25470
pubmed: 25258165
Su HH, Guo ZW, Wu XL, Xu P, Li N, Zong MH, Lou WY (2019) Efficient bioconversion of sucrose to high-value-added glucaric acid by in vitro metabolic engineering. Chemsuschem 12:2278–2285. https://doi.org/10.1002/cssc.201900185
doi: 10.1002/cssc.201900185
pubmed: 30791217
Su HH, Peng F, Ou XY, Zeng YJ, Zong MH, Lou WY (2020) Combinatorial synthetic pathway fine-tuning and cofactor regeneration for metabolic engineering of Escherichia coli significantly improve production of D-glucaric acid. N Biotechnol 59:51–58. https://doi.org/10.1016/j.nbt.2020.03.004
doi: 10.1016/j.nbt.2020.03.004
pubmed: 32693027
Toivari MH, Maaheimo H, Penttilä M, Ruohonen L (2010a) Enhancing the flux of D-glucose to the pentose phosphate pathway in Saccharomyces cerevisiae for the production of D-ribose and ribitol. Appl Microbiol Biotechnol 85:731–739. https://doi.org/10.1007/s00253-009-2184-4
doi: 10.1007/s00253-009-2184-4
pubmed: 19711072
Toivari MH, Ruohonen L, Richard P, Penttilä M, Wiebe MG (2010b) Saccharomyces cerevisiae engineered to produce D-xylonate. Appl Microbiol Biotechnol 88:751–760. https://doi.org/10.1007/s00253-010-2787-9
doi: 10.1007/s00253-010-2787-9
pubmed: 20680264
van Strien N, Rautiainen S, Asikainen M, Thomas DA, Linnekoski J, Niemelä K, Harlin A (2020) A unique pathway to platform chemicals: aldaric acids as stable intermediates for the synthesis of furandicarboxylic acid esters. Green Chem 22:8271–8277. https://doi.org/10.1039/d0gc02293d
doi: 10.1039/d0gc02293d
Verho R, Richard P, Jonson PH, Sundqvist L, Londesborough J, Penttilä M (2002) Identification of the first fungal NADPH-GAPDH from Kluyveromyces lactis. Biochem 41:13833–13838. https://doi.org/10.1021/bi0265325
doi: 10.1021/bi0265325
Verma BK, Mannan AA, Zhang F, Oyarzún DA (2022) Trade-offs in biosensor optimization for dynamic pathway engineering. ACS Synth Biol 11:228–240. https://doi.org/10.1021/ACSSYNBIO.1C00391
doi: 10.1021/ACSSYNBIO.1C00391
pubmed: 34968029
Vinopal RT, Hillman JD, Schulman H, Reznikoff WS, Fraenkel DG (1975) New phosphoglucose isomerase mutants of Escherichia coli. J Bacteriol 122:1172–1174
doi: 10.1128/jb.122.3.1172-1174.1975
pubmed: 1097391
pmcid: 246173
Ye C, Bandara WMMS, Greenberg ML (2013) Regulation of inositol metabolism is fine-tuned by inositol pyrophosphates in Saccharomyces cerevisiae. JBC 288:24898–24908. https://doi.org/10.1074/jbc.M113.493353
doi: 10.1074/jbc.M113.493353
Yoon SH, Moon TS, Iranpour P, Lanza AM, Prather KJ (2009) Cloning and characterization of uronate dehydrogenases from two pseudomonads and Agrobacterium tumefaciens strain C58. J Bacteriol 191:1565–1573. https://doi.org/10.1128/jb.00586-08
doi: 10.1128/jb.00586-08
pubmed: 19060141
Zhang X, Xu C, Liu YL, Wang J, Zhao YY, Deng Y (2020) Enhancement of glucaric acid production in Saccharomyces cerevisiae by expressing Vitreoscilla hemoglobin. Biotechnol Lett 42:2169–2178. https://doi.org/10.1007/s10529-020-02966-2
doi: 10.1007/s10529-020-02966-2
pubmed: 32691185
Zhang Q, Wan Z, Yu IKM, Tsang DCW (2021) Sustainable production of high-value gluconic acid and glucaric acid through oxidation of biomass-derived glucose: a critical review. J Clean Prod 312:127745. https://doi.org/10.1016/J.JCLEPRO.2021.127745
doi: 10.1016/J.JCLEPRO.2021.127745
Zhao Y, Li J, Su R, Liu Y, Wang J, Deng Y (2021) Effect of magnesium ions on glucaric acid production in the engineered Saccharomyces cerevisiae. J Biotechnol 332:61–71. https://doi.org/10.1016/J.JBIOTEC.2021.03.020
doi: 10.1016/J.JBIOTEC.2021.03.020
pubmed: 33812897
Zhao Y, Zuo F, Shu Q, Yang X, Deng Y (2023) Efficient production of glucaric acid by engineered Saccharomyces cerevisiae. AEM. https://doi.org/10.1128/aem.00535-23
doi: 10.1128/aem.00535-23