Abstract
Interest in the production of renewable chemicals from biomass has increased in the past years. Among these chemicals, carboxylic acids represent a significant part of the most desirable bio-based products. Xylonic acid is a five-carbon sugar-acid obtained from xylose oxidation that can be used in several industrial applications, including food, pharmaceutical, and construction industries. So far, the production of xylonic acid has not yet been available at an industrial scale; however, several microbial bio-based production processes are under development. This review summarizes the recent advances in pathway characterization, genetic engineering, and fermentative strategies to improve xylonic acid production by microorganisms from xylose or lignocellulosic hydrolysates. In addition, the strengths of the available microbial strains and processes and the major requirements for achieving biotechnological production of xylonic acid at a commercial scale are discussed. Efficient native and engineered microbial strains have been reported. Xylonic acid titers as high as 586 and 171 g L−1 were obtained from bacterial and yeast strains, respectively, in a laboratory medium. Furthermore, relevant academic and industrial players associated with xylonic acid production will be presented.
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References
Alkim C, Cam Y, Trichez D, Auriol C, Spina L, Vax A, Bartolo F, Besse P, François JM, Walther T (2015) Optimization of ethylene glycol production from (d)-xylose via a synthetic pathway implemented in Escherichia coli. Microb Cell Fact 14:127. https://doi.org/10.1186/s12934-015-0312-7
Almeida JR, Modig T, Petersson A, Hähn-Hägerdal B, Lidén G, Gorwa-Grauslund MF (2007) Increased tolerance and conversion of inhibitors in lignocellulosic hydrolysates by Saccharomyces cerevisiae. J Chem Technol Biotechnol 82:340–349. https://doi.org/10.1002/jctb.1676
Bañares AB, Nisola GM, Valdehuesa KNG, Lee W-K, Chung W-J (2021) Understanding D-xylonic acid accumulation: a cornerstone for better metabolic engineering approaches. Appl Microbiol Biotechnol 105:5309–5324. https://doi.org/10.1007/s00253-021-11410-y
Berghäll S, Hilditch S, Penttilä M, Richard P (2007) Identification in the mould Hypocrea jecorina of a gene encoding an NADP + : d-xylose dehydrogenase. FEMS Microbiol Lett 277:249–253. https://doi.org/10.1111/j.1574-6968.2007.00969.x
Bergmann JC, Trichez D, de Morais Junior WG, Ramos TGS, Pacheco TF, Carneiro CVGC, Honorato VM, Serra LA, Almeida JRM (2019) Biotechnological application of non-conventional yeasts for xylose valorization. In: Sibirny A (ed) Non-conventional yeasts: from basic research to application. Springer International Publishing, Cham, pp 23–74
Bertrand MG (1898) Action de la bactérie du sorbose sur le sucre de bois. Comptes Rendus des Séances de L’académie des Sciences 124–127
Bhatia SK, Jagtap SS, Bedekar AA, Bhatia RK, Patel AK, Pant D, Rajesh Banu J, Rao CV, Kim Y-G, Yang Y-H (2020) Recent developments in pretreatment technologies on lignocellulosic biomass: effect of key parameters, technological improvements, and challenges. Biores Technol 300:122724. https://doi.org/10.1016/j.biortech.2019.122724
Boer H, Andberg M, Pylkkänen R, Maaheimo H, Koivula A (2019) In vitro reconstitution and characterisation of the oxidative d-xylose pathway for production of organic acids and alcohols. AMB Expr 9:48. https://doi.org/10.1186/s13568-019-0768-7
Bondar M, da Fonseca MMR, Cesário MT (2021) Xylonic acid production from xylose by Paraburkholderia sacchari. Biochem Eng J 170:107982. https://doi.org/10.1016/j.bej.2021.107982
Braga M, Ferreira PM, Almeida JRM (2021) Screening method to prioritize relevant bio-based acids and their biochemical processes using recent patent information. Biofuels Bioprod Bioref 15:231–249. https://doi.org/10.1002/bbb.2156
Buchert J, Viikari L (1988a) The role of xylonolactone in xylonic acid production by Pseudomonas fragi. Appl Microbiol Biotechnol. https://doi.org/10.1007/BF00251763
Buchert J, Viikari L (1988b) Oxidative d-xylose metabolism of Gluconobacter oxydans. Appl Microbiol Biotechnol 29:375–379. https://doi.org/10.1007/BF00265822
Buchert J, Viikari L, Linko M, Markkanen P (1986) Production of xylonic acid by Pseudomonas fragi. Biotechnol Lett 8:541–546. https://doi.org/10.1007/BF01028079
Buchert J, Puls J, Poutanen K (1988) Comparison of Pseudomonas fragi and Gluconobacter oxydans for production of xylonic acid from hemicellulose hydrolyzates. Appl Microbiol Biotechnol 28:367–372. https://doi.org/10.1007/BF00268197
Buchert J (1990) Biotechnical oxidation of D-xylose and hemicellulose hydrolyzates by Gluconobacter oxydans: Dissertation
Cao Y, Xian M, Zou H, Zhang H (2013) Metabolic engineering of Escherichia coli for the production of Xylonate. PLoS ONE 8:e67305. https://doi.org/10.1371/journal.pone.0067305
Carneiro CVGC, de Paula E, Silva FC, Almeida JRM (2019) Xylitol production: identification and comparison of new producing yeasts. Microorganisms 7:484. https://doi.org/10.3390/microorganisms7110484
Chandel AK, Garlapati VK, Jeevan Kumar SP, Hans M, Singh AK, Kumar S (2020) The role of renewable chemicals and biofuels in building a bioeconomy. Biofuels Bioprod Bioref 14:830–844. https://doi.org/10.1002/bbb.2104
Chun BW, Dair B, Porteneuve CB, Jeknavorian AA, Cheung JH, Roberts LR (2005) Beneficiated water reducing compositions [Online]. USA: GRACE W R & CO; US2005096280A1, US7048793-B2, 2005. https://worldwide.espacenet.com/patent/search/family/028041816/publication/US2005096280A1?q=pn%3DUS2005096280A1. Accessed 10 Feb 2022
Chung B-W, Benita D, Macuch PJ, Debbie W, Charlotte P, Ara J (2006) The development of cement and concrete additive. ABAB 131:645–658. https://doi.org/10.1385/ABAB:131:1:645
Dai L, Jiang W, Zhou X, Xu Y (2020) Enhancement in xylonate production from hemicellulose pre-hydrolysate by powdered activated carbon treatment. Biores Technol 316:123944. https://doi.org/10.1016/j.biortech.2020.123944
François JM, Alkim C, Morin N (2020) Engineering microbial pathways for production of bio-based chemicals from lignocellulosic sugars: current status and perspectives. Biotechnol Biofuels 13:118. https://doi.org/10.1186/s13068-020-01744-6
Gao C, Hou J, Xu P, Guo L, Chen X, Hu G, Ye C, Edwards H, Chen J, Chen W, Liu L (2019) Programmable biomolecular switches for rewiring flux in Escherichia coli. Nat Commun 10:3751. https://doi.org/10.1038/s41467-019-11793-7
Han J, Hua X, Zhou X, Xu B, Wang H, Huang G, Xu Y (2021) A cost-practical cell-recycling process for xylonic acid bioproduction from acidic lignocellulosic hydrolysate with whole-cell catalysis of Gluconobacter oxydans. Biores Technol 333:125157. https://doi.org/10.1016/j.biortech.2021.125157
Herrera CRJ, Vieira VR, Benoliel T, Carneiro CVGC, De Marco JL, de Moraes LMP, de Almeida JRM, Torres FAG (2021) Engineering Zymomonas mobilis for the production of Xylonic Acid from sugarcane bagasse hydrolysate. Microorganisms 9:1372. https://doi.org/10.3390/microorganisms9071372
Honghui C (2020) Method for preparing calcium threonate by taking calcium xylonate as raw material [Online]. China; CN111704542A, 2020. https://worldwide.espacenet.com/patent/search/family/072545097/publication/CN111704542A?q=pn%3DCN111704542A. Accessed 16 Feb 2022
Jagtap SS, Rao CV (2018) Microbial conversion of xylose into useful bioproducts. Appl Microbiol Biotechnol 102:9015–9036. https://doi.org/10.1007/s00253-018-9294-9
Ji H, Lu X, Zong H, Zhuge B (2017) A synthetic hybrid promoter for D-xylonate production at low pH in the tolerant yeast Candida glycerinogenes. Bioengineered 8:700–706. https://doi.org/10.1080/21655979.2017.1312229
Jiemin C (2013) Fabric for jacquard scarves [Online]. China; CN202782042U, 2013 [cited 2022 Mar 22]. https://worldwide.espacenet.com/patent/search/family/047809369/publication/CN202782042U?q=pn%3DCN202782042U. Accessed 19 March 2022
Jin D, Ma J, Li Y, Jiao G, Liu K, Sun S, Zhou J, Sun R (2022) Development of the synthesis and applications of xylonic acid: a mini-review. Fuel 314:122773. https://doi.org/10.1016/j.fuel.2021.122773
Johnsen U, Schönheit P (2004) Novel xylose dehydrogenase in the halophilic archaeon Haloarcula marismortui. J Bacteriol 186:6198–6207. https://doi.org/10.1128/JB.186.18.6198-6207.2004
Jong E de, Stichnothe H, Bell G, Jørgensen H (2020) IEA Bioenergy Task 42 - Bio-Based Chemicals: a 2020 Update
Kequan C, Mengyang L, Xin W, Jialun Q, Yibo T, Jingsong H (2021) Method for producing 1,2,4-butanetriol from recombinant Escherichia coli based on one-step fermentation of cellulose [Online]. China; CN113265430A, 2021. https://worldwide.espacenet.com/patent/search/family/077228002/publication/CN113265430A?q=pn%3DCN113265430A. Accessed 19 March 2022
Lee JW, Yook S, Koh H, Rao CV, Jin Y-S (2021) Engineering xylose metabolism in yeasts to produce biofuels and chemicals. Curr Opin Biotechnol 67:15–25. https://doi.org/10.1016/j.copbio.2020.10.012
Liu H, Valdehuesa KNG, Nisola GM, Ramos KRM, Chung W-J (2012) High yield production of d-xylonic acid from d-xylose using engineered Escherichia coli. Biores Technol 115:244–248. https://doi.org/10.1016/j.biortech.2011.08.065
Lockwood LB, Nelson GEN (1946) The oxidation of pentoses by Pseudomonas. J Bacteriol 52:581–586. https://doi.org/10.1128/jb.52.5.581-586.1946
Markham RG (1990) Compositions and methods for administering therapeutically active compounds [Online]. USA; US4968716A, 1990. https://worldwide.espacenet.com/patent/search?q=pn%3DUS4968716A. Accessed 22 Mar 2022
Morais Junior WG, Pacheco TF, Trichez D, Almeida JRM, Gonçalves SB (2019) Xylitol production on sugarcane biomass hydrolysate by newly identified Candida tropicalis JA2 strain. Yeast 36:349–361. https://doi.org/10.1002/yea.3394
Moysés D, Reis V, Almeida J, Moraes L, Torres F (2016) Xylose fermentation by Saccharomyces cerevisiae: challenges and prospects. IJMS 17:207. https://doi.org/10.3390/ijms17030207
Niu W, Molefe MN, Frost JW (2003) Microbial synthesis of the energetic material precursor 1,2,4-Butanetriol. J Am Chem Soc 125:12998–12999. https://doi.org/10.1021/ja036391+
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
Nygård Y, Maaheimo H, Mojzita D, Toivari M, Wiebe M, Resnekov O, Gustavo Pesce C, Ruohonen L, Penttilä M (2014) Single cell and in vivo analyses elucidate the effect of xylC lactonase during production of D-xylonate in Saccharomyces cerevisiae. Metab Eng 25:238–247. https://doi.org/10.1016/j.ymben.2014.07.005
Pääkkönen J, Hakulinen N, Andberg M, Koivula A, Rouvinen J (2022) Three-dimensional structure of xylonolactonase from Caulobacter crescentus: a mononuclear iron enzyme of the 6-bladed β-propeller hydrolase family. Protein Sci 31:371–383. https://doi.org/10.1002/pro.4229
Paes BG, Steindorff AS, Formighieri EF, Pereira IS, Almeida JRM (2021) Physiological characterization and transcriptome analysis of Pichia pastoris reveals its response to lignocellulose-derived inhibitors. AMB Expr 11:2. https://doi.org/10.1186/s13568-020-01170-9
Pereira B, Li Z-J, De Mey M, Lim CG, Zhang H, Hoeltgen C, Stephanopoulos G (2016) Efficient utilization of pentoses for bioproduction of the renewable two-carbon compounds ethylene glycol and glycolate. Metab Eng 34:80–87. https://doi.org/10.1016/j.ymben.2015.12.004
Pezzotti F, Therisod M (2006) Enzymatic synthesis of aldonic acids. Carbohyd Res 341:2290–2292. https://doi.org/10.1016/j.carres.2006.05.023
Porro D, Branduardi P (2017) Production of organic acids by yeasts and filamentous fungi. In: Sibirny AA (ed) Biotechnology of yeasts and filamentous fungi. Springer International Publishing, Cham, pp 205–223
Qiao Y, Li C, Lu X, Zong H, Zhuge B (2021) Transporter engineering promotes the co-utilization of glucose and xylose by Candida glycerinogenes for d-xylonate production. Biochem Eng J 175:108150. https://doi.org/10.1016/j.bej.2021.108150
Ramos TGS, Justen F, Carneiro CVGC, Honorato VM, Franco PF, Vieira FS, Trichez D, Rodrigues CM, Almeida JRM (2021) Xylonic acid production by recombinant Komagataella phaffii strains engineered with newly identified xylose dehydrogenases. Bioresour Technol Rep 16:100825. https://doi.org/10.1016/j.biteb.2021.100825
Raposo RS, de Almeida MC, de Oliveira MD, da Fonseca MM, Cesário MT (2017) A Burkholderia sacchari cell factory: production of poly-3-hydroxybutyrate, xylitol and xylonic acid from xylose-rich sugar mixtures. N Biotechnol 34:12–22. https://doi.org/10.1016/j.nbt.2016.10.001
Salusjärvi L, Havukainen S, Koivistoinen O, Toivari M (2019) Biotechnological production of glycolic acid and ethylene glycol: current state and perspectives. Appl Microbiol Biotechnol 103:2525–2535. https://doi.org/10.1007/s00253-019-09640-2
Sauer M, Porro D, Mattanovich D, Branduardi P (2008) Microbial production of organic acids: expanding the markets. Trends Biotechnol 26:100–108. https://doi.org/10.1016/j.tibtech.2007.11.006
Shen Y, Zhou X, Xu Y (2020) Enhancement of Gluconobacter oxydans resistance to lignocellulosic-derived inhibitors in xylonic acid production by overexpressing Thioredoxin. Appl Biochem Biotechnol 191:1072–1083. https://doi.org/10.1007/s12010-020-03253-6
Singh OV, Kumar R (2007) Biotechnological production of gluconic acid: future implications. Appl Microbiol Biotechnol 75:713–722. https://doi.org/10.1007/s00253-007-0851-x
Stephen Dahms A (1974) 3-Deoxy-D-pentulosonic acid aldolase and its role in a new pathway of D-xylose degradation. Biochem Biophys Res Commun 60:1433–1439. https://doi.org/10.1016/0006-291X(74)90358-1
Stephens C, Christen B, Fuchs T, Sundaram V, Watanabe K, Jenal U (2007) Genetic Analysis of a Novel Pathway for d -Xylose Metabolism in Caulobacter crescentus. J Bacteriol 189:2181–2185. https://doi.org/10.1128/JB.01438-06
Su Y, Willis LB, Jeffries TW (2015) Effects of aeration on growth, ethanol and polyol accumulation by Spathaspora passalidarum NRRL Y-27907 and Scheffersomyces stipitis NRRL Y-7124. Biotechnol Bioeng 112:457–469. https://doi.org/10.1002/bit.25445
Sundar MSL, Nampoothiri KM (2022) An overview of the metabolically engineered strains and innovative processes used for the value addition of biomass derived xylose to xylitol and xylonic acid. Biores Technol 345:126548. https://doi.org/10.1016/j.biortech.2021.126548
Sundar MSL, Susmitha A, Rajan D, Hannibal S, Sasikumar K, Wendisch VF, Nampoothiri KM (2020) Heterologous expression of genes for bioconversion of xylose to xylonic acid in Corynebacterium glutamicum and optimization of the bioprocess. AMB Expr 10:68. https://doi.org/10.1186/s13568-020-01003-9
Toivari MH, Ruohonen L, Richard P, Penttilä M, Wiebe MG (2010) Saccharomyces cerevisiae engineered to produce D-xylonate. Appl Microbiol Biotechnol 88:751–760. https://doi.org/10.1007/s00253-010-2787-9
Toivari M, Nygård Y, Kumpula E-P, Vehkomäki M-L, Benčina M, Valkonen M, Maaheimo H, Andberg M, Koivula A, Ruohonen L, Penttilä M, Wiebe MG (2012a) Metabolic engineering of Saccharomyces cerevisiae for bioconversion of d-xylose to d-xylonate. Metab Eng 14:427–436. https://doi.org/10.1016/j.ymben.2012.03.002
Toivari MH, Nygård Y, Penttilä M, Ruohonen L, Wiebe MG (2012b) Microbial d-xylonate production. Appl Microbiol Biotechnol 96:1–8. https://doi.org/10.1007/s00253-012-4288-5
Toivari M, Vehkomäki M-L, Nygård Y, Penttilä M, Ruohonen L, Wiebe MG (2013) Low pH d-xylonate production with Pichia kudriavzevii. Biores Technol 133:555–562. https://doi.org/10.1016/j.biortech.2013.01.157
Trichez D, Steindorff AS, Soares CEVF, Formighieri EF, Almeida JRM (2019) Physiological and comparative genomic analysis of new isolated yeasts Spathaspora sp. JA1 and Meyerozyma caribbica JA9 reveal insights into xylitol production. FEMS Yeast Res. https://doi.org/10.1093/femsyr/foz034
Wang C, Wei D, Zhang Z, Wang D, Shi J, Kim CH, Jiang B, Han Z, Hao J (2016) Production of xylonic acid by Klebsiella pneumoniae. Appl Microbiol Biotechnol 100:10055–10063. https://doi.org/10.1007/s00253-016-7825-9
Weimberg R (1961) Pentose oxidation by Pseudomonas fragi. J Biol Chem 236:629–635
Werpy TA, Holladay JE, White JF (2004) Top value added chemicals from biomass: I. results of screening for potential candidates from sugars and synthesis gas. U. S. Dep Energy 1:76. https://doi.org/10.2172/926125
Yan J, Xu J, Cao M, Li Z, Xu C, Wang X, Yang C, Xu P, Gao C, Ma C (2018) Engineering of glycerol utilization in Gluconobacter oxydans 621H for biocatalyst preparation in a low-cost way. Microb Cell Fact 17:158. https://doi.org/10.1186/s12934-018-1001-0
Yim SS, Choi JW, Lee SH, Jeon EJ, Chung W-J, Jeong KJ (2017) Engineering of Corynebacterium glutamicum for consolidated conversion of hemicellulosic biomass into xylonic acid. Biotechnol J 12:1700040. https://doi.org/10.1002/biot.201700040
Zamora F, Bueno M, Molina I, Iribarren JI, Muñoz-Guerra S, Galbis JA (2000) Stereoregular copolyamides derived from d -Xylose and l -Arabinose. Macromolecules 33:2030–2038. https://doi.org/10.1021/ma9916436
Zhang Y, Guo S, Wang Y, Liang X, Xu P, Gao C, Ma C (2019) Production of d- Xylonate from corn cob hydrolysate by a metabolically engineered Escherichia coli Strain. ACS Sustainable Chem Eng 7:2160–2168. https://doi.org/10.1021/acssuschemeng.8b04839
Zhou X, Lü S, Xu Y, Mo Y, Yu S (2015) Improving the performance of cell biocatalysis and the productivity of xylonic acid using a compressed oxygen supply. Biochem Eng J 93:196–199. https://doi.org/10.1016/j.bej.2014.10.014
Zhou X, Zhou X, Tang X, Xu Y (2018) Process for calcium xylonate production as a concrete admixture derived from in-situ fermentation of wheat straw pre-hydrolysate. Biores Technol 261:288–293. https://doi.org/10.1016/j.biortech.2018.04.040
Zhou X, Han J, Xu Y (2019) Electrodialytic bioproduction of xylonic acid in a bioreactor of supplied-oxygen intensification by using immobilized whole-cell Gluconobacter oxydans as biocatalyst. Biores Technol 282:378–383. https://doi.org/10.1016/j.biortech.2019.03.042
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We thank CAPES and CNPq for scholarships for CVGCC and DT, respectively. CNPq, FAPDF and Embrapa for financial support.
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This work was supported by CNPq, FAPDF, and Embrapa. CVGCC and DT received scholarships from CAPES and CNPq.
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DT: Data analysis, Writing and Conceptualization. CVGCC and MB: Data analysis and Writing. JRMA: Supervision, Conceptualization, Writing—review & editing, Funding acquisition.
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J.R.M.A. is coauthor of a patent that described the engineering of Komagataella phaffii for the production of xylonic acid (BR 102018001359–9). All remaining authors declare that they have no competing interests.
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Trichez, D., Carneiro, C.V.G.C., Braga, M. et al. Recent progress in the microbial production of xylonic acid. World J Microbiol Biotechnol 38, 127 (2022). https://doi.org/10.1007/s11274-022-03313-5
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DOI: https://doi.org/10.1007/s11274-022-03313-5