Non-canonical D-xylose and L-arabinose metabolism via D-arabitol in the oleaginous yeast Rhodosporidium toruloides.
D-arabitol
D-xylose metabolism
L-arabinose
L-arabitol
L-ribulose
Pentose metabolism
Rhodosporidium toruloides
Rhodotorula
Xylitol
Xylulokinase
Journal
Microbial cell factories
ISSN: 1475-2859
Titre abrégé: Microb Cell Fact
Pays: England
ID NLM: 101139812
Informations de publication
Date de publication:
03 Aug 2023
03 Aug 2023
Historique:
received:
20
04
2023
accepted:
17
06
2023
medline:
7
8
2023
pubmed:
4
8
2023
entrez:
3
8
2023
Statut:
epublish
Résumé
R. toruloides is an oleaginous yeast, with diverse metabolic capacities and high tolerance for inhibitory compounds abundant in plant biomass hydrolysates. While R. toruloides grows on several pentose sugars and alcohols, further engineering of the native pathway is required for efficient conversion of biomass-derived sugars to higher value bioproducts. A previous high-throughput study inferred that R. toruloides possesses a non-canonical L-arabinose and D-xylose metabolism proceeding through D-arabitol and D-ribulose. In this study, we present a combination of genetic and metabolite data that refine and extend that model. Chiral separations definitively illustrate that D-arabitol is the enantiomer that accumulates under pentose metabolism. Deletion of putative D-arabitol-2-dehydrogenase (RTO4_9990) results in > 75% conversion of D-xylose to D-arabitol, and is growth-complemented on pentoses by heterologous xylulose kinase expression. Deletion of putative D-ribulose kinase (RTO4_14368) arrests all growth on any pentose tested. Analysis of several pentose dehydrogenase mutants elucidates a complex pathway with multiple enzymes mediating multiple different reactions in differing combinations, from which we also inferred a putative L-ribulose utilization pathway. Our results suggest that we have identified enzymes responsible for the majority of pathway flux, with additional unknown enzymes providing accessory activity at multiple steps. Further biochemical characterization of the enzymes described here will enable a more complete and quantitative understanding of R. toruloides pentose metabolism. These findings add to a growing understanding of the diversity and complexity of microbial pentose metabolism.
Identifiants
pubmed: 37537595
doi: 10.1186/s12934-023-02126-x
pii: 10.1186/s12934-023-02126-x
pmc: PMC10398940
doi:
Substances chimiques
arabitol
YFV05Y57M9
Xylose
A1TA934AKO
Arabinose
B40ROO395Z
Pentoses
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
145Subventions
Organisme : U.S. Department of Energy
ID : DE-AC02-05CH11231
Informations de copyright
© 2023. BioMed Central Ltd., part of Springer Nature.
Références
Narisetty V, Cox R, Bommareddy R, Agrawal D, Ahmad E, Pant KK, et al. Valorisation of xylose to renewable fuels and chemicals, an essential step in augmenting the commercial viability of lignocellulosic biorefineries. Sustain Energy Fuels. 2021;6:29–65.
pubmed: 35028420
pmcid: 8691124
Yang S, Vera JM, Grass J, Savvakis G, Moskvin OV, Yang Y, et al. Complete genome sequence and the expression pattern of plasmids of the model ethanologen Zymomonas mobilis ZM4 and its xylose-utilizing derivatives 8b and 2032. Biotechnol Biofuels. 2018;11:125.
pubmed: 29743953
pmcid: 5930841
Cunha JT, Soares PO, Romaní A, Thevelein JM, Domingues L. Xylose fermentation efficiency of industrial Saccharomyces cerevisiae yeast with separate or combined xylose reductase/xylitol dehydrogenase and xylose isomerase pathways. Biotechnol Biofuels. 2019;12:20.
pubmed: 30705706
pmcid: 6348659
Li H, Alper HS. Enabling xylose utilization in Yarrowia lipolytica for lipid production. Biotechnol J. 2016;11:1230–40.
pubmed: 27367454
Nora LC, Cassiano MHA, Santana ÍP, Guazzaroni M-E, Silva-Rocha R, da Silva RR. Mining novel cis-regulatory elements from the emergent host Rhodosporidium toruloides using transcriptomic data. Front Microbiol. 2022;13:1069443.
pubmed: 36687612
Nair AS, Sivakumar N. Enhanced production of biodiesel by Rhodosporidium toruloides using waste office paper hydrolysate as feedstock: optimization and characterization. Fuel. 2022;327:125174.
Shaigani P, Awad D, Redai V, Fuchs M, Haack M, Mehlmer N, et al. Oleaginous yeasts- substrate preference and lipid productivity: a view on the performance of microbial lipid producers. Microb Cell Fact. 2021;20:220.
pubmed: 34876116
pmcid: 8650408
Osorio-González CS, Saini R, Hegde K, Brar SK, Lefebvre A, Avalos-Ramírez A. Inhibitor degradation by Rhodosporidium toruloides NRRL 1588 using undetoxified wood hydrolysate as a culture media. Biomass Bioenerg. 2022;160:106419.
Saini R, Hegde K, Brar SK, Vezina P. Advanced biofuel production and road to commercialization: an insight into bioconversion potential of Rhodosporidium sp. Biomass Bioenerg. 2020;132:105439.
Osorio-González CS, Saini R, Hegde K, Brar SK, Lefebvre A, Avalos RA. Crabtree effect on rhodosporidium toruloides using wood hydrolysate as a culture media. Fermentation. 2022;9:11.
Kim D, Woo HM. Deciphering bacterial xylose metabolism and metabolic engineering of industrial microorganisms for use as efficient microbial cell factories. Appl Microbiol Biotechnol. 2018;102:9471–80.
pubmed: 30238140
Harhangi HR, Akhmanova AS, Emmens R, van der Drift C, de Laat WTAM, van Dijken JP, et al. Xylose metabolism in the anaerobic fungus Piromyces sp. strain E2 follows the bacterial pathway. Arch Microbiol. 2003;180:134–41.
pubmed: 12811467
Kim J, Coradetti ST, Kim Y-M, Gao Y, Yaegashi J, Zucker JD, et al. Multi-omics driven metabolic network reconstruction and analysis of lignocellulosic carbon utilization in Rhodosporidium toruloides. Front Bioeng Biotechnol. 2020;8:612832.
pubmed: 33585414
Jagtap SS, Rao CV. Production of D-arabitol from D-xylose by the oleaginous yeast Rhodosporidium toruloides IFO0880. Appl Microbiol Biotechnol. 2018;102:143–51.
pubmed: 29127468
Jagtap SS, Deewan A, Liu J-J, Walukiewicz HE, Yun EJ, Jin Y-S, et al. Integrating transcriptomic and metabolomic analysis of the oleaginous yeast Rhodosporidium toruloides IFO0880 during growth under different carbon sources. Appl Microbiol Biotechnol. 2021;105:7411–25.
pubmed: 34491401
Bisping B, Baumann U, Simmering R. Effects of immobilization on polyol production by Pichia farinosa. In: Immobilized Cells - Basics and Applications, Proceedings of an International Symposium organized under auspices of The Working Party on Applied Biocatalysis of the European Federation of Biotechnology Noordwijkerhout. Elsevier; 1996. p. 395–401.
Bernard EM, Christiansen KJ, Tsang SF, Kiehn TE, Armstrong D. Rate of arabinitol production by pathogenic yeast species. J Clin Microbiol. 1981;14:189–94.
pubmed: 7024306
pmcid: 271932
Yoshikawa J, Habe H, Morita T, Fukuoka T, Imura T, Iwabuchi H, et al. Production of D-arabitol from raw glycerol by Candida quercitrusa. Appl Microbiol Biotechnol. 2014;98:2947–53.
pubmed: 24352735
Diamantopoulou P, Papanikolaou S. Biotechnological production of sugar-alcohols: focus on Yarrowia lipolytica and edible/medicinal mushrooms. Process Biochem. 2023;124:113–31.
Wong B, Leeson S, Grindle S, Magee B, Brooks E, Magee PT. D-arabitol metabolism in Candida albicans: construction and analysis of mutants lacking D-arabitol dehydrogenase. J Bacteriol. 1995;177:2971–6.
pubmed: 7768790
pmcid: 176981
Egermeier M, Russmayer H, Sauer M, Marx H. Metabolic flexibility of Yarrowia lipolytica growing on glycerol. Front Microbiol. 2017;8:49.
pubmed: 28174563
pmcid: 5258708
Saha BC, Bothast RJ. Production of L-arabitol from L-arabinose by candida entomaea and Pichia guilliermondii. Appl Microbiol Biotechnol. 1996;45:299–306.
Kordowska-Wiater M, Kuzdraliński A, Czernecki T, Targoński Z, Frąc M, Oszust K. The ability of a novel strain scheffersomyces (Syn. Candida) shehatae isolated from rotten wood to produce arabitol. Pol J Microbiol. 2017;66:335–43.
pubmed: 29319532
Saha BC, Sakakibara Y, Cotta MA. Production of D-arabitol by a newly isolated Zygosaccharomyces rouxii. J Ind Microbiol Biotechnol. 2007;34:519–23.
pubmed: 17357803
Li X, Zhang Y, Zabed HM, Yun J, Zhang G, Zhao M, et al. High-level production of d-arabitol by Zygosaccharomyces rouxii from glucose: metabolic engineering and process optimization. Bioresour Technol. 2023;367:128251.
pubmed: 36334865
Blakley ER, Spencer JFT. Studies on the formation OFD -ARABITOL by osmophilic yeasts. Can J Biochem Physiol. 1962;40:1737–48.
pubmed: 13971477
Ingram JM, Wood WA. Enzymatic basis for D-ARBITOL production by Saccharomyces rouxii. J Bacteriol. 1965;89:1186–94.
pubmed: 14292984
pmcid: 277626
Zhang G, Lin Y, He P, Li L, Wang Q, Ma Y. Characterization of the sugar alcohol-producing yeast Pichia anomala. J Ind Microbiol Biotechnol. 2014;41:41–8.
pubmed: 24170383
Cheng H, Wang B, Lv J, Jiang M, Lin S, Deng Z. Xylitol production from xylose mother liquor: a novel strategy that combines the use of recombinant Bacillus subtilis and Candida maltosa. Microb Cell Fact. 2011;10:5.
pubmed: 21299871
pmcid: 3046924
Wang H, Li L, Zhang L, An J, Cheng H, Deng Z. Xylitol production from waste xylose mother liquor containing miscellaneous sugars and inhibitors: one-pot biotransformation by Candida tropicalis and recombinant Bacillus subtilis. Microb Cell Fact. 2016;15:82.
pubmed: 27184671
pmcid: 4869185
Fonseca C, Neves AR, Antunes AMM, Noronha JP, Hahn-Hägerdal B, Santos H, et al. Use of in vivo 13C nuclear magnetic resonance spectroscopy to elucidate L-arabinose metabolism in yeasts. Appl Environ Microbiol. 2008;74:1845–55.
pubmed: 18245253
pmcid: 2268326
Fonseca C, Romão R, Rodrigues de Sousa H, Hahn-Hägerdal B, Spencer-Martins I. L-Arabinose transport and catabolism in yeast. FEBS J. 2007;274:3589–600.
pubmed: 17627668
Kordowska-Wiater M. Production of arabitol by yeasts: current status and future prospects. J Appl Microbiol. 2015;119:303–14.
pubmed: 25809659
Ravikumar Y, Razack SA, Ponpandian LN, Zhang G, Yun J, Huang J, et al. Microbial hosts for production of D-arabitol: current state-of-art and future prospects. Trends Food Sci Technol. 2022;120:100–10.
Erian AM, Sauer M. Utilizing yeasts for the conversion of renewable feedstocks to sugar alcohols—a review. Bioresour Technol. 2022;346:126296.
pubmed: 34798255
Onishi H, Suzuki T. Microbial production of xylitol from glucose. Appl Microbiol. 1969;18:1031–5.
pubmed: 5370655
pmcid: 378187
Lin C-C, Hsieh P-C, Mau J-L, Teng D-F. Construction of an intergeneric fusion from Schizosaccharomyces pombe and Lentinula edodes for xylan degradation and polyol production. Enzyme Microb Technol. 2005;36:107–17.
Quarterman J, Slininger PJ, Kurtzman CP, Thompson SR, Dien BS. A survey of yeast from the Yarrowia clade for lipid production in dilute acid pretreated lignocellulosic biomass hydrolysate. Appl Microbiol Biotechnol. 2017;101:3319–34.
pubmed: 28012044
Harcus D, Dignard D, Lépine G, Askew C, Raymond M, Whiteway M, et al. Comparative xylose metabolism among the ascomycetes C. albicans, S. stipitis and S. cerevisiae. PLoS ONE. 2013;8:e80733.
pubmed: 24236198
pmcid: 3827475
Protzko RJ, Hach CA, Coradetti ST, Hackhofer MA, Magosch S, Thieme N, et al. Genomewide and enzymatic analysis reveals efficient d-galacturonic acid metabolism in the basidiomycete yeast Rhodosporidium toruloides. mSystems. 2019. https://doi.org/10.1128/mSystems.00389-19 .
doi: 10.1128/mSystems.00389-19
pubmed: 31848309
pmcid: 6918025
Yoon BH, Jeon WY, Shim WY, Kim JH. L-arabinose pathway engineering for arabitol-free xylitol production in Candida tropicalis. Biotechnol Lett. 2011;33:747–53.
pubmed: 21127946
Seiboth B, Metz B. Fungal arabinan and L-arabinose metabolism. Appl Microbiol Biotechnol. 2011;89:1665–73.
pubmed: 21212945
pmcid: 3044236
Metz B, de Vries RP, Polak S, Seidl V, Seiboth B. The Hypocrea jecorina (syn. Trichoderma reesei) lxr1 gene encodes a D-mannitol dehydrogenase and is not involved in L-arabinose catabolism. FEBS Lett. 2009;583:1309–13.
pubmed: 19303876
Metz B, Mojzita D, Herold S, Kubicek CP, Richard P, Seiboth B. A novel L-xylulose reductase essential for L-arabinose catabolism in Trichoderma reesei. Biochemistry. 2013;52:2453–60.
pubmed: 23506391
Mojzita D, Vuoristo K, Koivistoinen OM, Penttilä M, Richard P. The, “true” L-xylulose reductase of filamentous fungi identified in Aspergillus niger. FEBS Lett. 2010;584:3540–4.
pubmed: 20654618
Witteveen CFB, Weber F, Busink R, Visser J. Isolation and characterization of two xylitol dehydrogenases from Aspergillus niger. Microbiology. 1994;140:1679–85.
vanKuyk PA, de Groot MJ, Ruijter GJ, de Vries RP, Visser J. The Aspergillus niger D-xylulose kinase gene is co-expressed with genes encoding arabinan degrading enzymes, and is essential for growth on D-xylose and L-arabinose. Eur J Biochem. 2001;268:5414–23.
pubmed: 11606204
Komeda H, Yamasaki-Yashiki S, Hoshino K, Asano Y. Identification and characterization of D-xylulokinase from the D-xylose-fermenting fungus. Mucor circinelloides FEMS Microbiol Lett. 2014;360:51–61.
pubmed: 25163569
Nora LC, Wehrs M, Kim J, Cheng J-F, Tarver A, Simmons BA, et al. A toolset of constitutive promoters for metabolic engineering of Rhodosporidium toruloides. Microb Cell Fact. 2019;18:117.
pubmed: 31255171
pmcid: 6599526
Ko BS, Kim J, Kim JH. Production of xylitol from D-xylose by a xylitol dehydrogenase gene-disrupted mutant of Candida tropicalis. Appl Environ Microbiol. 2006;72:4207–13.
pubmed: 16751533
pmcid: 1489653
Böer E, Wartmann T, Schmidt S, Bode R, Gellissen G, Kunze G. Characterization of the AXDH gene and the encoded xylitol dehydrogenase from the dimorphic yeast Arxula adeninivorans. Antonie Van Leeuwenhoek. 2005;87:233–43.
pubmed: 15803389
Tran LH, Kitamoto N, Kawai K, Takamizawa K, Suzuki T. Cloning and expression of a NAD+-dependent xylitol dehydrogenase gene (xdhA) of Aspergillus oryzae. J Biosci Bioeng. 2004;97:419–22.
pubmed: 16233653
Lima LHA, do Pinheiro Amaral CG, de Moraes LMP, de Freitas SM, Torres FAG. Xylitol dehydrogenase from Candida tropicalis: molecular cloning of the gene and structural analysis of the protein. Appl Microbiol Biotechnol. 2006;73:631–9.
pubmed: 16896602
Mahmud A, Hattori K, Hongwen C, Kitamoto N, Suzuki T, Nakamura K, et al. NAD
pubmed: 23436125
Suzuki T, Tran LH, Yogo M, Idota O, Kitamoto N, Kawai K, et al. Cloning and expression of NAD+-dependent L-arabinitol 4-dehydrogenase gene (ladA) of Aspergillus oryzae. J Biosci Bioeng. 2005;100:472–4.
pubmed: 16310740
Seiboth B, Hartl L, Pail M, Kubicek CP. D-xylose metabolism in Hypocrea jecorina: loss of the xylitol dehydrogenase step can be partially compensated for by lad1-encoded L-arabinitol-4-dehydrogenase. Eukaryot Cell. 2003;2:867–75.
pubmed: 14555469
pmcid: 219359
Kim B, Sullivan RP, Zhao H. Cloning, characterization, and engineering of fungal L-arabinitol dehydrogenases. Appl Microbiol Biotechnol. 2010;87:1407–14.
pubmed: 20414651
de Vries RP, Flipphi MJ, Witteveen CF, Visser J. Characterization of an Aspergillus nidulans L-arabitol dehydrogenase mutant. FEMS Microbiol Lett. 1994;123:83–90.
pubmed: 7988903
Sullivan R, Zhao H. Cloning, characterization, and mutational analysis of a highly active and stable L-arabinitol 4-dehydrogenase from Neurospora crassa. Appl Microbiol Biotechnol. 2007;77:845–52.
pubmed: 17938906
Sukpipat W, Komeda H, Prasertsan P, Asano Y. Purification and characterization of xylitol dehydrogenase with l-arabitol dehydrogenase activity from the newly isolated pentose-fermenting yeast Meyerozyma caribbica 5XY2. J Biosci Bioeng. 2017;123:20–7.
pubmed: 27506274
Link T, Lohaus G, Heiser I, Mendgen K, Hahn M, Voegele RT. Characterization of a novel NADP(+)-dependent D-arabitol dehydrogenase from the plant pathogen Uromyces fabae. Biochem J. 2005;389(Pt 2):289–95.
pubmed: 15796718
pmcid: 1175105
Cheng H, Li Z, Jiang N, Deng Z. Cloning, purification and characterization of an NAD-Dependent D-Arabitol dehydrogenase from acetic acid bacterium. Acetobacter suboxydans Protein J. 2009;28:263–72.
pubmed: 19629658
Hallborn J, Walfridsson M, Penttilä M, Keränen S, Hahn-Hägerdal B. A short-chain dehydrogenase gene from Pichia stipitis having D-arabinitol dehydrogenase activity. Yeast. 1995;11:839–47.
pubmed: 7483848
Murray JS, Wong ML, Miyada CG, Switchenko AC, Goodman TC, Wong B. Isolation, characterization and expression of the gene that encodes D-arabinitol dehydrogenase in Candida tropicalis. Gene. 1995;155:123–8.
pubmed: 7698655
Verho R, Putkonen M, Londesborough J, Penttilä M, Richard P. A novel NADH-linked l-xylulose reductase in the l-arabinose catabolic pathway of yeast. J Biol Chem. 2004;279:14746–51.
pubmed: 14736891
Singh C, Glaab E, Linster CL. Molecular identification of D-Ribulokinase in budding yeast and mammals. J Biol Chem. 2017;292:1005–28.
pubmed: 27909055
Saini R, Osorio-Gonzalez CS, Hegde K, Kaur Brar S, Vezina P. A co-fermentation strategy with wood hydrolysate and crude glycerol to enhance the lipid accumulation in Rhodosporidium toruloides-1588. Bioresour Technol. 2022;364:127821.
pubmed: 36007764
Chen N, Xu C, Guo X, Shim H. Effects of sodium and magnesium supplement on lipid production and wastewater treatment by Rhodosporidium toruloides. Renew Energy. 2022;199:919–28.
Osorio-González CS, Saini R, Hegde K, Brar SK, Lefebvre A, Avalos RA. Carbon/nitrogen ratio as a tool to enhance the lipid production in Rhodosporidium toruloides-1588 using C5 and C6 wood hydrolysates. J Clean Prod. 2023;384:135687.
Coradetti ST, Pinel D, Geiselman GM, Ito M, Mondo SJ, Reilly MC, et al. Functional genomics of lipid metabolism in the oleaginous yeast Rhodosporidium toruloides. Elife. 2018. https://doi.org/10.7554/eLife.32110 .
doi: 10.7554/eLife.32110
pubmed: 29521624
pmcid: 5922974
Dinh HV, Suthers PF, Chan SHJ, Shen Y, Xiao T, Deewan A, et al. A comprehensive genome-scale model for Rhodosporidium toruloides IFO0880 accounting for functional genomics and phenotypic data. Metab Eng Commun. 2019;9:e00101.
pubmed: 31720216
pmcid: 6838544
Pinheiro MJ, Bonturi N, Belouah I, Miranda EA, Lahtvee P-J. Xylose metabolism and the effect of oxidative stress on lipid and carotenoid production in rhodotorula toruloides: insights for future biorefinery. Front Bioeng Biotechnol. 2020;8:1008.
pubmed: 32974324
pmcid: 7466555
Drzymała-Kapinos K, Mirończuk AM, Dobrowolski A. Lipid production from lignocellulosic biomass using an engineered Yarrowia lipolytica strain. Microb Cell Fact. 2022;21:226.
pubmed: 36307797
pmcid: 9617373
Rodriguez GM, Hussain MS, Gambill L, Gao D, Yaguchi A, Blenner M. Engineering xylose utilization in Yarrowia lipolytica by understanding its cryptic xylose pathway. Biotechnol Biofuels. 2016;9:149.
pubmed: 27446238
pmcid: 4955270
Ryu S, Trinh CT. Understanding functional roles of native pentose-specific transporters for activating dormant pentose metabolism in Yarrowia lipolytica. Appl Environ Microbiol. 2018. https://doi.org/10.1128/AEM.02146-17 .
doi: 10.1128/AEM.02146-17
pubmed: 29150499
pmcid: 5772232
Assev S, Rölla G. Evidence for presence of a xylitol phosphotransferase system in Streptococcus mutans OMZ 176. Acta Pathol Microbiol Immunol Scand B. 1984;92:89–92.
pubmed: 6730972
Hausman SZ, London J. Purification and characterization of ribitol-5-phosphate and xylitol-5-phosphate dehydrogenases from strains of Lactobacillus casei. J Bacteriol. 1987;169:1651–5.
pubmed: 3104310
pmcid: 211995
Kentache T, Milohanic E, Cao TN, Mokhtari A, Aké FM, Ma Pham QM, et al. Transport and catabolism of pentitols by listeria monocytogenes. J Mol Microbiol Biotechnol. 2016;26:369–80.
pubmed: 27553222
Povelainen M, Eneyskaya EV, Kulminskaya AA, Ivanen DR, Kalkkinen N, Neustroev KN, et al. Biochemical and genetic characterization of a novel enzyme of pentitol metabolism: D-arabitol-phosphate dehydrogenase. Biochem J. 2003;371(Pt 1):191–7.
pubmed: 12467497
pmcid: 1223252
Kuznetsova E, Proudfoot M, Gonzalez CF, Brown G, Omelchenko MV, Borozan I, et al. Genome-wide analysis of substrate specificities of the Escherichia coli haloacid dehalogenase-like phosphatase family. J Biol Chem. 2006;281:36149–61.
pubmed: 16990279
Xu Y-F, Lu W, Chen JC, Johnson SA, Gibney PA, Thomas DG, et al. Discovery and functional characterization of a yeast sugar alcohol phosphatase. ACS Chem Biol. 2018;13:3011–20.
pubmed: 30240188
pmcid: 6466636
Hult K, Veide A, Gatenbeck S. The distribution of the NADPH regenerating mannitol cycle among fungal species. Arch Microbiol. 1980;128:253–5.
pubmed: 6782999
Chroumpi T, Peng M, Aguilar-Pontes MV, Müller A, Wang M, Yan J, et al. Revisiting a “simple” fungal metabolic pathway reveals redundancy, complexity and diversity. Microb Biotechnol. 2021;14:2525–37.
pubmed: 33666344
pmcid: 8601170
Lee J-K, Koo B-S, Kim S-Y. Cloning and characterization of the xyl1 gene, encoding an NADH-preferring xylose reductase from Candida parapsilosis, and its functional expression in Candida tropicalis. Appl Environ Microbiol. 2003;69:6179–88.
pubmed: 14532079
pmcid: 201247
Verduyn C, Van Kleef R, Frank J, Schreuder H, Van Dijken JP, Scheffers WA. Properties of the NAD(P)H-dependent xylose reductase from the xylose-fermenting yeast Pichia stipitis. Biochem J. 1985;226:669–77.
pubmed: 3921014
pmcid: 1144764
Kuhn A, van Zyl C, van Tonder A, Prior BA. Purification and partial characterization of an aldo-keto reductase from Saccharomyces cerevisiae. Appl Environ Microbiol. 1995;61:1580–5.
pubmed: 7747971
pmcid: 167412
Chiang C, Knight SG. L-Arabinose metabolism by cell-free extracts of Penicillium chrysogenum. Biochim Biophys Acta. 1961;46:271–8.
pubmed: 13692999
Sakakibara Y, Saha BC. Isolation of an operon involved in xylitol metabolism from a xylitol-utilizing Pantoea ananatis mutant. J Biosci Bioeng. 2008;106:337–44.
pubmed: 19000608
Sakakibara Y, Torigoe K. Biochemical characterization of l-arabitol 2-dehydrogenase from Pantoea ananatis. J Biosci Bioeng. 2012;113:715–8.
pubmed: 22306314
Werpy T, Petersen G. Top Value Added Chemicals from Biomass: Volume I -- Results of Screening for Potential Candidates from Sugars and Synthesis Gas. US Department of Energy; 2004.
Grigoriev IV, Nikitin R, Haridas S, Kuo A, Ohm R, Otillar R, et al. MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res. 2014;42:D699-704.
pubmed: 24297253
Zhuang X, Kilian O, Monroe E, Ito M, Tran-Gymfi MB, Liu F, et al. Monoterpene production by the carotenogenic yeast Rhodosporidium toruloides. Microb Cell Fact. 2019;18:54.
pubmed: 30885220
pmcid: 6421710
Funke M, Diederichs S, Kensy F, Müller C, Büchs J. The baffled microtiter plate: increased oxygen transfer and improved online monitoring in small scale fermentations. Biotechnol Bioeng. 2009;103:1118–28.
pubmed: 19449392