Microbial production of L-malate from renewable non-food feedstocks

doi:10.1016/j.cjche.2020.10.017

Abstract

Abstract: L-malate is an intermediate of the tricarboxylic acid cycle which is naturally occurred in various microorganisms, and it has been widely applied in polymer, beverage and food, textile, agricultural and pharmaceutical industries. Driven by the pursuit of a sustainable economy, microbial production of L-malate has received much attention in last decades. In this review, we focus on the utilization of wastes and/or byproducts as feedstocks for the microbial production of L-malate. Firstly, we present the recent developments on the natural or engineered metabolic pathways that dedicate to the biosynthesis of L-malate, and also provide a comprehensive discussions on developing high-efficient producers. Then, the recent achievements in microbial production of L-malate from various carbon sources were concluded and discussed. Furthermore, some abundant non-food feedstocks which have been used for microbial production of other chemicals were reviewed, as they may be potential candidate feedstock for L-malate production in future. Finally, we outlined the major challenges and proposed further improvements for the production of L-malate.

Key words: L-malate, Renewable feedstock, Microbial fermentation, Bioeconomy, C4 dicarboxylic acid

摘要： L-malate is an intermediate of the tricarboxylic acid cycle which is naturally occurred in various microorganisms, and it has been widely applied in polymer, beverage and food, textile, agricultural and pharmaceutical industries. Driven by the pursuit of a sustainable economy, microbial production of L-malate has received much attention in last decades. In this review, we focus on the utilization of wastes and/or byproducts as feedstocks for the microbial production of L-malate. Firstly, we present the recent developments on the natural or engineered metabolic pathways that dedicate to the biosynthesis of L-malate, and also provide a comprehensive discussions on developing high-efficient producers. Then, the recent achievements in microbial production of L-malate from various carbon sources were concluded and discussed. Furthermore, some abundant non-food feedstocks which have been used for microbial production of other chemicals were reviewed, as they may be potential candidate feedstock for L-malate production in future. Finally, we outlined the major challenges and proposed further improvements for the production of L-malate.

关键词: L-malate, Renewable feedstock, Microbial fermentation, Bioeconomy, C4 dicarboxylic acid

Youming Jiang, Xiaohan Ye, Tianwen Zheng, Weiliang Dong, Fengxue Xin, Jiangfeng Ma, Min Jiang. Microbial production of L-malate from renewable non-food feedstocks[J]. Chinese Journal of Chemical Engineering, 2021, 29(2): 105-111.

Youming Jiang, Xiaohan Ye, Tianwen Zheng, Weiliang Dong, Fengxue Xin, Jiangfeng Ma, Min Jiang. Microbial production of L-malate from renewable non-food feedstocks[J]. 中国化学工程学报, 2021, 29(2): 105-111.

References

[1] Z. Chi, Z.P. Wang, G.Y. Wang, I. Khan, Z.M. Chi, Microbial biosynthesis and secretion of L-malic acid and its applications, Crit. Rev. Biotechnol. 36 (2016) 99–107.
[2] X. Yin, J.H. Li, H.D. Shin, G.C. Du, L. Liu, J. Chen, Metabolic engineering in the biotechnological production of organic acids in the tricarboxylic acid cycle of microorganisms: advances and prospects, Biotechnol. Adv. 33 (2015) 830–841.
[3] T. Werpy, G. Petersen, Top value added chemicals from biomass: I. results of screening for potential candidates from sugars and synthesis gas. United States: N. p., 2004, https://doi.org/10.2172/15008859.
[4] M. Sauer, D. Porro, D. Mattanovich, P. Branduardi, Malic acid production from renewables, Trends Biotechnol. 26 (2008) 100–108.
[5] A. Kövilein, C. Kubisch, L.Y. Cai, K. Ochsenreither, Malic acid production from renewables: a review, J. Chem. Technol. Biot. 95 (2020) 513–526.
[6] S. Somasundaram, G.T. Eom, S.H. Hong, Efficient malate production in Escherichia coli using a synthetic scaffold protein complex, Appl. Biochem. Biotechnol. 184 (2017) 1308–1318.
[7] I. Goldberg, J.S. Rokem, O. Pines, Organic acids: old metabolites, new themes, J. Chem. Technol. Biot. 81 (2006) 1601–1611.
[8] R.A. Sheldon, Green chemistry and resource efficiency: towards a green economy, Green Chem. 18 (2016) 3180–3183.
[9] S. Choi, C.W. Song, J.H. Shin, S.Y. Lee, Biorefineries for the production of top building block chemicals and their derivatives, Metab. Eng. 28 (2015) 223–239.
[10] S. Alonso, M. Rendueles, M. Diaz, Microbial production of specialty organic acids from renewable and waste materials, Crit. Rev. Biotechnol. 35 (2015) 497–513.
[11] Y.J. Liu, J. Zhang, G.Z. Cui, Q. Cui, Current progress of targetron technology: development, improvement and application in metabolic engineering, Biotechnol. J. 10 (2015) 855–865.
[12] J. Liu, J. Li, H.D. Shin, L. Liu, G. Du, J. Chen, Protein and metabolic engineering for the production of organic acids, Bioresour. Technol. 239 (2017) 412–421.
[13] E. Battat, Y. Peleg, A. Bercovitz, J.S. Rokem, I. Goldberg, Optimization of Lmalate production by Aspergillus flavus in a stirred fermentor, Biotechnol. Bioeng. 37 (1991) 1108–1116.
[14] Z.P. Wang, G.Y. Wang, I. Khan, Z.M. Chi, High-level production of calcium malate from glucose by Penicillium sclerotiorum K302, Bioresour. Technol. 143 (2013) 674–677.
[15] I. Khan, K. Nazir, Z.P. Wang, G.L. Liu, Z.M. Chi, Calcium malate overproduction by Penicillium viticola 152 using the medium containing corn steep liquor, Appl. Microbiol. Biotechnol. 98 (2014) 1539–1546.
[16] R.M. Zelle, E. Hulster, W.A. Winden, P. Waard, C. Dijkema, A.A. Winkler, J.M. Geertman, J.P. Dijken, J.T. Pronk, A.J. Maris, Malate production by Saccharomyces cerevisiae: engineering of pyruvate carboxylation, oxaloacetate reduction, and malate export, Appl. Environ. Microbiol. 74 (2008) 2766–2777.
[17] S.H. Brown, L. Bashkirova, R. Berka, T. Chandler, T. Doty, K. McCall, M. McCulloch, S. McFarland, S. Thompson, D. Yaver, A. Berry, Metabolic engineering of Aspergillus oryzae NRRL 3488 for increased production of Lmalate, Appl. Microbiol. Biotechnol. 97 (2013) 8903–8912.
[18] J. Liu, Z. Xie, H.D. Shin, J. Li, G. Du, J. Chen, L. Liu, Rewiring the reductive tricarboxylic acid pathway and L-malate transport pathway of Aspergillus oryzae for overproduction of L-malate, J. Biotechnol. 253 (2017) 1–9.
[19] J.J. Liu, J.H. Li, Y.F. Liu, H.D. Shin, R. Ledesma-Amaro, G.C. Du, J. Chen, L. Liu, Synergistic rewiring of carbon metabolism and redox metabolism in cytoplasm and mitochondria of Aspergillus oryzae for increased L-malate production, ACS Synth. Biol. 7 (2018) 2139–2147.
[20] X. Chen, G. Xu, N. Xu, W. Zou, P. Zhu, L. Liu, J. Chen, Metabolic engineering of Torulopsis glabrata for malate production, Metab. Eng. 19 (2013) 10–16.
[21] X. Chen, Y. Wang, X. Dong, G. Hu, L. Liu, Engineering rTCA pathway and C4-dicarboxylate transporter for L-malate production, Appl. Microbiol. Biotechnol. 101 (2017) 4041–4052.
[22] S.Y. Moon, S.H. Hong, T.Y. Kim, S.Y. Lee, Metabolic engineering of Escherichia coli for the production of malate, Biochem. Eng. J. 40 (2008) 312–320.
[23] X. Zhang, X. Wang, K.T. Shanmugam, L.O. Ingram, L-malate production by metabolically engineered Escherichia coli, Appl. Environ. Microbiol. 77 (2011) 427–434.
[24] L. Mu, J. Wen, Engineered Bacillus subtilis 168 produces L-malate by heterologous biosynthesis pathway construction and lactate dehydrogenase deletion, World J. Microbiol. Biotechnol. 29 (2013) 33–41.
[25] H. Negoro, A. Kotaka, K. Matsumura, H. Tsutsumi, Y. Hata, Enhancement of malate-production and increase in sensitivity to dimethyl succinate by mutation of the VID24 gene in Saccharomyces cerevisiae, J. Biosci. Bioeng. 121 (2016) 665–671.
[26] I. Martinez, H. Gao, G.N. Bennett, K.Y. San, High yield production of four-carbon dicarboxylic acids by metabolically engineered Escherichia coli, J. Ind. Microbiol. Biotechnol. 45 (2018) 53–60.
[27] X. Dong, X. Chen, Y. Qian, Y. Wang, L. Wang, W. Qiao, L. Liu, Metabolic engineering of Escherichia coli W3110 to produce L-malate, Biotechnol. Bioeng. 114 (2017) 656–664.
[28] C. Gao, S. Wang, G. Hu, L. Guo, X. Chen, P. Xu, L. Liu, Engineering Escherichia coli for malate production by integrating modular pathway characterization with CRISPRi-guided multiplexed metabolic tuning, Biotechnol. Bioeng. 115 (2018) 661–672.
[29] X. Zou, Y. Zhou, S.T. Yang, Production of polymalate and malate by Aureobasidium pullulans fermentation and acid hydrolysis, Biotechnol. Bioeng. 110 (2013) 2105–2113.
[30] T. Zambanini, E. Sarikaya, W. Kleineberg, J.M. Buescher, G. Meurer, N. Wierckx, L.M. Blank, Efficient malate production from glycerol with Ustilago trichophora TZ1, Biotechnol. Biofuels 9 (2016) 67.
[31] K. Ochsenreither, C. Fischer, A. Neumann, C. Syldatk, Process characterization and influence of alternative carbon sources and carbon-to-nitrogen ratio on organic acid production by Aspergillus oryzae DSM1863, Appl. Microbiol. Biotechnol. 98 (2014) 5449–5460.
[32] J. Iyyappan, G. Baskar, B. Bharathiraja, R. Saravanathamizhan, Malic acid production from biodiesel derived crude glycerol using morphologically controlled Aspergillus Niger in batch fermentation, Bioresour. Technol. 269 (2018) 393–399.
[33] T.P. West, Malate production from thin stillage by Aspergillus species, Biotechnol. Lett. 33 (2011) 2463–2467.
[34] C. Cheng, Y. Zhou, M. Lin, P. Wei, S.T. Yang, Polymalate fermentation by Aureobasidium pullulans for malate production from soybean hull and soy molasses: fermentation kinetics and economic analysis, Bioresour. Technol. 223 (2017) 166–174.
[35] Y. Deng, Y. Mao, X. Zhang, Metabolic engineering of a laboratory-evolved Thermobifida fusca muC strain for malate production on cellulose and minimal treated lignocellulosic biomass, Biotechnol. Prog. 32 (2016) 14–20.
[36] X. Zou, J. Yang, X. Tian, M.J. Guo, Z.H. Li, Y.Z. Li, Production of polymalate and malate from xylose and corncob hydrolysate by a novel Aureobasidium pullulans YJ 6–11 strain, Process Biochem. 51 (2016) 16–23.
[37] X.J. Li, Y. Liu, Y. Yang, H. Zhang, H.L. Wang, Y. Wu, M. Zhang, T. Sun, J.S. Cheng, X.F. Wu, L.J. Pan, S.T. Jiang, H.W. Wu, High levels of malate production by the bioconversion of corn straw hydrolyte using an isolated Rhizopus delemar strain, Biotechnol. Biopro. 19 (2014) 478–492.
[38] S. Dörsam, J. Fesseler, O. Gorte, T. Hahn, S. Zibek, C. Syldatk, K. Ochsenreither, Sustainable carbon sources for microbial organic acid production with filamentous fungi, Biotechnol. Biofuels 10 (2017) 242.
[39] N. Vivek, R. Sindhu, A. Madhavan, A.J. Anju, E. Castro, V. Faraco, A. Pandey, P. Binod, Recent advances in the production of value added chemicals and lipids utilizing biodiesel industry generated crude glycerol as a substrate-Metabolic aspects, challenges and possibilities: An overview, Bioresour. Technol. 239 (2017) 507–517.
[40] C. Li, K.L. Lesnik, H. Liu, Microbial conversion of waste glycerol from biodiesel production into value-added products, Energies 6 (2013) 4739–4768.
[41] P. Anand, R.K. Saxena, A comparative study of solvent-assisted pretreatment of biodiesel derived crude glycerol on growth and 1,3-propanediol production from Citrobacter freundii, N. Biotechnol. 29 (2012) 199–205.
[42] M. Saini, Z.W. Wang, C.J. Chiang, Y.P. Chao, Metabolic engineering of Escherichia coli for production of n-butanol from crude glycerol, Biotechnol. Biofuels 10 (2017) 173.
[43] J.M. Clomburg, R. Gonzalez, Anaerobic fermentation of glycerol: a platform for renewable fuels and chemicals, Trends Biotechnol. 31 (2013) 20–28.
[44] Z. Cui, C. Gao, J. Li, J. Hou, C.S.K. Lin, Q. Qi, Engineering of unconventional yeast Yarrowia lipolytica for efficient succinic acid production from glycerol at low pH, Metab. Eng. 42 (2017) 126–133.
[45] F. Xin, C. Wang, W. Dong, W. Zhang, H. Wu, J. Ma, M. Jiang, Comprehensive investigations of biobutanol production by a non-acetone and 1,3-propanediol generating Clostridium strain from glycerol and polysaccharides, Biotechnol. Biofuels 9 (2016) 220.
[46] Q. Li, H. Wu, Z. Li, Q. Ye, Enhanced succinate production from glycerol by engineered Escherichia coli strains, Bioresour. Technol. 218 (2016) 217–223.
[47] N. Li, B. Zhang, Z. Wang, Y.J. Tang, T. Chen, X. Zhao, Engineering Escherichia coli for fumaric acid production from glycerol, Bioresour. Technol. 174 (2014) 81–87.
[48] F. Yang, M.A. Hanna, R. Sun, Value-added uses for crude glycerol–a byproduct of biodiesel production, Biotechnol. Biofuels 5 (2012) 13.
[49] T. Zambanini, H.H. Tehrani, E. Geiser, C.K. Sonntag, J.M. Buescher, G. Meurer, N. Wierckx, L.M. Blank, Metabolic engineering of Ustilago trichophora TZ1 for improved malic acid production, Metab. Eng. Commun. 4 (2017) 12–21.
[50] T.P. West, Fungal biotransformation of crude glycerol into malic acid, Z. Naturforsch. C 70 (2015) 165–167.
[51] N. Sarkar, S.K. Ghosh, S. Bannerjee, K. Aikat, Bioethanol production from agricultural wastes: an overview, Renew. Energy 37 (2012) 19–27.
[52] M.J. Taherzadeh, K. Karimi, Acid-based hydrolysis processes for ethanol from lignocellulosic materials: a review, BioResources 2 (2007) 472–499.
[53] Y. Kim, R. Hendrickson, N.S. Mosier, M.R. Ladisch, B. Bals, V. Balan, B.E. Dale, B. S. Dien, M.A. Cotta, Effect of compositional variability of distillers’ grains on cellulosic ethanol production, Bioresour. Technol. 101 (2010) 5385–5393.
[54] Y. Kim, N.S. Mosier, R. Hendrickson, T. Ezeji, H. Blaschek, B. Dien, M. Cotta, B. Dale, M.R. Ladisch, Composition of corn dry-grind ethanol by-products: DDGS, wet cake, and thin stillage, Bioresour. Technol. 99 (2008) 5165–5176.
[55] T.P. West, Microbial production of malic acid from biofuel-related coproducts and biomass, Fermentation 3 (2017) 14.
[56] F. Fao, Online Statistical Service, Food and Agriculture Organization of the United Nations, 2012, http://www.fao.org/faostat/en/#data.
[57] P. Lakshmanan, R.J. Geijskes, K.S. Aitken, C.L.P. Grof, G.D. Bonnett, G.R. Smith, Sugarcane biotechnology: the challenges and opportunities, Vitro Cell. Dev-PL 41 (2005) 345–363.
[58] M.B. Doelle, H.W. Doelle, Sugar-cane molasses fermentation by Zymomonas mobilis, Appl. Microbiol. Biot. 33 (1990) 31–35.
[59] J.F. Ma, F. Li, R.M. Liu, L.Y. Liang, Y.L. Ji, C. Wei, M. Jiang, H.H. Jia, P.K. Ouyang, Succinic acid production from sucrose and molasses by metabolically engineered E. coli using a cell surface display system, Biochem. Eng. J. 91 (2014) 240–249.
[60] J. Feng, J. Yang, W. Yang, J. Chen, M. Jiang, X. Zou, Metabolome-and genomescale model analyses for engineering of Aureobasidium pullulans to enhance polymalate and malate production from sugarcane molasses, Biotechnol. Biofuels 11 (2018) 94.
[61] F.W. Bai, W.A. Anderson, M. Moo-Young, Ethanol fermentation technologies from sugar and starch feedstocks, Biotechnol. Adv. 26 (2008) 89–105.
[62] M. Talacuece, F. Justino, R. Rodrigues, M. Flores, J. Nascimento, E. Santos, Modeling of soybean under present and future climates in Mozambique, Climate 4 (2016) 31.
[63] J. Dong, Y. Du, Y. Zhou, S.T. Yang, Butanol production from soybean hull and soy molasses by acetone-butanol-ethanol fermentation, ACS Symposium Series 1178 (2014) 25–41.
[64] M.L. Zhang, Y.T. Fan, Y. Xing, C.M. Pan, G.S. Zhang, J.J. Lay, Enhanced biohydrogen production from cornstalk wastes with acidification pretreatment by mixed anaerobic cultures, Biomass Bioenerg. 31 (2007) 250–254.
[65] V. Menon, M. Rao, Trends in bioconversion of lignocellulose: Biofuels, platform chemicals & biorefinery concept, Prog. Energ. Combust. 38 (2012) 522–550.
[66] V.B. Agbor, N. Cicek, R. Sparling, A. Berlin, D.B. Levin, Biomass pretreatment: fundamentals toward application, Biotechnol. Adv. 29 (2011) 675–685.
[67] J.K. Saini, R. Saini, L. Tewari, Lignocellulosic agriculture wastes as biomass feedstocks for second-generation bioethanol production: concepts and recent developments, 3 Biotech. 5 (2015) 337–353.
[68] Y. Li, B. Huang, H. Wu, Z. Li, Q. Ye, Y.P. Zhang, Production of succinate from acetate by metabolically engineered Escherichia coli, ACS Synth. Biol. 5 (2016) 1299–1307.
[69] P. Zheng, L. Fang, Y. Xu, J.J. Dong, Y. Ni, Z.H. Sun, Succinic acid production from corn stover by simultaneous saccharification and fermentation using Actinobacillus succinogenes, Bioresour. Technol. 101 (2010) 7889–7894.
[70] S. Sokhansanj, A. Turhollow, J. Cushman, J. Cundiff, Engineering aspects of collecting corn stover for bioenergy, Biomass Bioenerg. 23 (2002) 347–355.
[71] M.T. Agler, B.A. Wrenn, S.H. Zinder, L.T. Angenent, Waste to bioproduct conversion with undefined mixed cultures: the carboxylate platform, Trends Biotechnol. 29 (2011) 70–78.
[72] M.E. Himmel, S.Y. Ding, D.K. Johnson, W.S. Adney, M.R. Nimlos, J.W. Brady, T.D. Foust, Biomass recalcitrance: engineering plants and enzymes for biofuels production, Science 315 (2007) 804–807.
[73] X. Zou, Y. Wang, G. Tu, Z. Zan, X. Wu, Adaptation and transcriptome analysis of Aureobasidium pullulans in corncob hydrolysate for increased inhibitor tolerance to malate production, PLoS One 10 (3) (2015) e0121416.
[74] A.R. Prazeres, F. Carvalho, J. Rivas, Cheese whey management: a review, J. Environ. Manage. 110 (2012) 48–68.
[75] R. Moreno, A. Escapa, J. Cara, B. Carracedo, X. Gómez, A two-stage process for hydrogen production from cheese whey: integration of dark fermentation and biocatalyzed electrolysis, Int. J. Hydrogen Energ. 40 (2015) 168–175.
[76] L. Jiang, H. Cui, L. Zhu, Y. Hu, X. Xu, S. Li, H. Huang, Enhanced propionic acid production from whey lactose with immobilized Propionibacterium acidipropionici and the role of trehalose synthesis in acid tolerance, Green Chem. 17 (2015) 250–259.
[77] Y.H. Seo, M. Sung, J.I. Han, Lactulose production from cheese whey using recyclable catalyst ammonium carbonate, Food Chem. 197 (2016) 664–669.
[78] A. Matsushika, H. Inoue, T. Kodaki, S. Sawayama, Ethanol production from xylose in engineered Saccharomyces cerevisiae strains: current state and perspectives, Appl. Microbiol. Biot. 84 (2009) 37–53.
[79] R. Ravindran, A.K. Jaiswal, Exploitation of food industry waste for high-value products, Trends Biotechnol. 34 (2016) 58–69.
[80] N. Soltani, A. Bahrami, M.I. Pech-Canul, L.A. González, Review on the physicochemical treatments of rice husk for production of advanced materials, Chem. Eng. J. 264 (2015) 899–935.
[81] G. Wang, L. Tan, Z.Y. Sun, Z.X. Gou, Y.Q. Tang, K. Kida, Production of bioethanol from rice straw by simultaneous saccharification and fermentation of whole pretreated slurry using Saccharomyces cerevisiae KF-7, Environ. Prog. Sustain. 34 (2015) 582–588.
[82] A. Abraham, A.K. Mathew, R. Sindhu, A. Pandey, P. Binod, Potential of rice straw for bio-refining: an overview, Bioresour. Technol. 215 (2016) 29–36.
[83] X. Chen, Y. Zhang, Y. Gu, Z. Liu, Z. Shen, H. Chu, X. Zhou, Enhancing methane production from rice straw by extrusion pretreatment, Appl. Energ. 122 (2014) 34–41.
[84] M. Hogan, J. Otterstedt, R. Morin, J. Wilde, Biomass for heat and poweropportunity and economics, European Climate Foundation, Södra, Sveaskog, Vattenfall, report, The Hague, 2010.
[85] A.A. Koutinas, A. Vlysidis, D. Pleissner, N. Kopsahelis, I. Lopez Garcia, I.K. Kookos, S. Papanikolaou, T.H. Kwan, C.S. Lin, Valorization of industrial waste and by-product streams via fermentation for the production of chemicals and biopolymers, Chem. Soc. Rev. 43 (2014) 2587–2627.
[86] J. Rodríguez-López, A.J. Sánchez, D.M. Gómez, A. Romaní, J.C. Parajó, Fermentative production of fumaric acid from Eucalyptus globulus wood hydrolyzates, J. Chem. Technol. Biot. 87 (2012) 1036–1040.
[87] D.Y. Kim, S.C. Yim, P.C. Lee, W.G. Lee, S.Y. Lee, H.N. Chang, Batch and continuous fermentation of succinic acid from wood hydrolysate by Mannheimia succiniciproducens MBEL55E, Enzyme Microb. Tech. 35 (2004) 648–653.
[88] A. Demirbas, Waste management, waste resource facilities and waste conversion processes, Energ. Convers. Manage. 52 (2011) 1280–1287.
[89] S. Banerjee, S. Mudliar, R. Sen, B. Giri, D. Satpute, T. Chakrabarti, R.A. Pandey, Commercializing lignocellulosic bioethanol: technology bottlenecks and possible remedies, Biofuel Bioprod. Bior. 4 (2010) 77–93.
[90] C.A. Cardona, J.A. Quintero, I.C. Paz, Production of bioethanol from sugarcane bagasse: Status and perspectives, Bioresour. Technol. 101 (2010) 4754–4766.
[91] R.M. Liu, L.Y. Liang, W.J. Cao, M.K. Wu, K.Q. Chen, J.F. Ma, M. Jiang, P. Wei, P.K. Ouyang, Succinate production by metabolically engineered Escherichia coli using sugarcane bagasse hydrolysate as the carbon source, Bioresour. Technol. 135 (2013) 574–577.