Abstract
Production of succinic acid via separate enzymatic hydrolysis and fermentation (SHF) and simultaneous saccharification and fermentation (SSF) are alternatives and are environmentally friendly processes. These processes have attained considerable positions in the industry with their own share of challenges and problems. The high-value succinic acid is extensively used in chemical, food, pharmaceutical, leather and textile industries and can be efficiently produced via several methods. Previously, succinic acid production via chemical synthesis from petrochemical or refined sugar has been the focus of interest of most reviewers. However, these expensive substrates have been recently replaced by alternative sustainable raw materials such as lignocellulosic biomass, which is cheap and abundantly available. Thus, this review focuses on succinic acid production utilizing lignocellulosic material as a potential substrate for SSF and SHF. SSF is an economical single-step process which can be a substitute for SHF — a two-step process where biomass is hydrolyzed in the first step and fermented in the second step. SSF of lignocellulosic biomass under optimum temperature and pH conditions results in the controlled release of sugar and simultaneous conversion into succinic acid by specific microorganisms, reducing reaction time and costs and increasing productivity. In addition, main process parameters which influence SHF and SSF processes such as batch and fed-batch fermentation conditions using different microbial strains are discussed in detail.
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References
Agarwal L, Isar J, Dutt K, Saxena RK (2007) Statistical optimization for succinic acid production from E. coli in a cost-effective medium. Appl Biochem Biotech 142(2):158–167
Agbor VB, Cicek N, Sparling R, Berlin A, Levin DB (2011) Biomass pretreatment: fundamentals toward application. Biotechnol Adv 29(6):675–685
Andersson CA, Helmerius J, Hodge DB, Berglund K, Rova U (2009) Inhibition of succinic acid production in metabolically engineered Escherichia coli by neutralizing agent, organic acids, and osmolarity. Biotech Prog 25:116–123
Beauprez JJ, De Mey M, Soetaert WK (2010) Microbial succinic acid production: natural versus metabolic engineered producers. Process Biochem 45(7):1103–1114
Borges ER, Pereira Jr N (2011) Succinic acid production from sugarcane bagasse hemicellulose hydrolysate by Actinobacillus succinogenes. J Ind Microbiol Biotechnol 38:1001–1011
Chandra RP, Bura R, Mabee WE, Berlin A, Pan X, Saddler JN (2007) Substrate pretreatment: the key to effective enzymatic hydrolysis of lignocellulosics? Adv Biochem Eng Biotechnol vol 108:67–93
Chatterjee R, Millard CS, Champion K, Clark DP, Donnelly MI (2001) Mutation of the ptsG gene results in increased production of succinate in fermentation of glucose by Escherichia coli. Appl Environ Microbiol 67(1):148–154
Chen K, Jiang M, Wei P, Yao J, Wu H (2010) Succinic acid production from acid hydrolysate of corn fiber by Actinobacillus succinogenes. Appl Biochem Biotech 160(2):477v485
Chen K, Zhang H, Miao Y, Wei P, Chen J (2011a) Simultaneous saccharification and fermentation of acid-pretreated rapeseed meal for succinic acid production using Actinobacillus succinogenes. Enzyme Microb Technol 48(4–5):339–344. doi:10.1016/j.enzmictec.2010.12.009
Chen KQ, Li J, Ma JF, Jiang M, Wei P, Liu ZM, Ying HJ (2011b) Succinic acid production by Actinobacillus succinogenes using hydrolysates of spent yeast cells and corn fiber. Bioresource Technol 102(2):1704–1708
de la Hoz A, Diaz-Ortiz A, Moreno A (2005) Microwaves in organic synthesis. Thermal and non-thermal microwave effects. Chem Soc Rev 34(2):164–178
Demain AL, Newcomb M, Wu JD (2005) Cellulase, clostridia, and ethanol. Mol Biol Rev 69(1):124–154
Efe T, van der Wielen LAM, Straathof AJJ (2013) Techno-economic analysis of succinic acid production using adsorption from fermentation medium. Biomass Bioenerg 56:479–492
Galbe M, Zacchi G (2007) Pretreatment of lignocellulosic materials for efficient bioethanol production Adv Biochem Eng Biotechnol, pp 41–65
Garde A, Jonsson G, Schmidt AS, Ahring BK (2002) Lactic acid production from wheat straw hemicellulose hydrolysate by Lactobacillus pentosus and Lactobacillus brevis. Bioresource Technol 81(3):217–223
Glassner DA, Datta R (1992) Process for the production and purification of succinic acid. US Patents 5,143,834
Gokarn RR, Eiteman MA, Altman E (1998) Expression of pyruvate carboxylase enhances succinate production in Escherichia coli without affecting glucose uptake. Biotechnol Lett 20:795–798
Guettler MV, Jain MK, Rumler D (1996) Method for making succinic acid, bacterial variants for use in the process, and methods for obtaining variants. US Patents 5:573–931
Hamzah F, Idris A, Rashid R, Ming S (2009) Lactic acid production from microwave-alkali pre-treated empty fruit bunches fibre using Rhizopus oryzae pellet. J App Sci 9(17):3086–3091
Hamzah F, Idris A (2008) Enzymatic hydrolysis of treated palm oil empty fruit bunches fibre (EFB)using combination alkali-microwave techniques. J Biotechnol 136(Supp 1):S406
Hamzah F, Idris A, Shuan TK (2011) Preliminary study on enzymatic hydrolysis of treated oil palm (Elaeis) empty fruit bunches fibre (EFB) by using combination of cellulase and β1-4 glucosidase. Biomass Bioenerg 35(3):1055–1059
Han Y, Chen H (2008) Characterization of β-glucosidase from corn stover and its application in simultaneous saccharification and fermentation. Bioresource Technol 99(14):6081–6087
Hodge DB, Andersson C, Berglund KA, Rova U (2009) Detoxification requirements for bioconversion of softwood dilute acid hydrolyzates to succinic acid. Enzyme Microb Technol 44(5):309–316
Hofvendahl K, Hahn-Hägerdal B, Åkerberg C, Zacchi G (1999) Simultaneous enzymatic wheat starch saccharification and fermentation to lactic acid by Lactococcus lactis. Appl Microbiol Biotechnol 52(2):163–169
Hu Z, Wang Y, Wen Z (2008) Alkali (NaOH) pretreatment of switchgrass by radio frequency-based dielectric heating. Appl Biochem Biotechnol 148(1–3):71–81
Huang LP, Jin B, Lant P, Zhou J (2005) Simultaneous saccharification and fermentation of potato starch wastewater to lactic acid by Rhizopus oryzae and Rhizopus arrhizus. Biochem Eng 23:265–276
Jantama K, Haupt MJ, Svoronos SA, Zhang X, Moore JC, Shanmugam KT, Ingram LO (2008a) Combining metabolic engineering and metabolic evolution to develop nonrecombinant strains of Escherichia coli C that produce succinate and malate. Biotechnol Bioeng 99(5):1140–1153
Jantama K, Zhang X, Moore JC, Shanmugam KT, Svoronos SA, Ingram LO (2008b) Eliminating side products and increasing succinate yields in engineered strains of Escherichia coli C. Biotechnol Bioeng 101(5):881–893
John RP, Anisha GS, Nampoothiri KM, Pandey A (2009) Direct lactic acid fermentation: focus on simultaneous saccharification and lactic acid production. Biotechnol Adv 27(2):145–152
John RP, Nampoothiri KM, Pandey A (2006) Simultaneous saccharification and l-(+)-lactic acid fermentation of protease-treated wheat bran using mixed culture of lactobacilli. Biotechnol Lett 28(22):1823–1826
Jung YH, Kim IJ, Han JI, Choi IG, Kim KH (2011) Aqueous ammonia pretreatment of oil palm empty fruit bunches for ethanol production. Bioresour Technol 102(20):9806–9809
Kamm B, Kamm M, Schmidt M, Starke I, Kleinpeter E (2006) Chemical and biochemical generation of carbohydrates from lignocellulose-feedstock (Lupinus nootkatensis) — quantification of glucose. Chemosphere 62(1):97–105
Kim DY, Yim SC, Lee PC, Lee WG, Lee SY, Chang HN (2004) Batch and continuous fermentation of succinic acid from wood hydrolysate by Mannheimia succiniciproducens MBEL55E. Enzyme Microb Technol 35(6–7):648–653
Kim J, Yun S, Ounaies Z (2006) Discovery of cellulose as a smart material. Macromolecules 39(12):4202–4206
Kim S, Park JM, Seo JW, Kim CH (2012) Sequential acid-/alkali-pretreatment of empty palm fruit bunch fiber. Bioresource Technol 109:229–233
Kumar R, Singh S, Singh OV (2008) Bioconversion of lignocellulosic biomass: biochemical and molecular perspectives. J Ind Microbiol Biot 35(5):377–391
Lai L-W, Idris A (2013) Disruption of oil palm trunks and fronds by microwave-alkali pretreatment. BioResources 8(2)
Lee JW, Na D, Park JM, Lee J, Choi S, Lee SY (2012) Systems metabolic engineering of microorganisms for natural and non-natural chemicals. Nat Chem Biol 8(6):536–546
Lee PC, Lee SY, Hong SH, Chang HN (2002) Isolation and characterization of a new succinic acid producing bacterium, Mannheimia succiniciproducens MBEL55E, from bovine rumen. Appl Microbiol Biot 58(5):663–668
Lee PC, Lee SY, Chang HN (2008) Succinic acid production by Anaerobiospirillum succiniciproducens ATCC 29305 growing on galactose, galactose/glucose, and galactose/lactose. J Microbiol Biotechnol 18(11):1792–1796
Lee PC, Lee SY, Hong SH, Chang HN (2003a) Batch and continuous cultures of Mannheimia succiniciproducens MBEL55E for the production of succinic acid from whey and corn steep liquor. Bioprocess Biosyst Eng 26(1):63–67
Lee PC, Lee SY, Hong SH, Chang HN, Park SC (2003b) Biological conversion of wood hydrolysate to succinic acid by Anaerobiospirillum succiniciproducens. Biotechnol Lett 25(2):111–114
Lee PC, Lee WG, Kwon S, Lee SY, Chang HN (1999) Succinic acid production by Anaerobiospirillum succiniciproducens: effects of the H2/CO2 supply and glucose concentration. Enzyme Microb Technol 24(8–9):549–554
Lee PC, Lee WG, Lee SY, Chang HN (2001) Succinic acid production with reduced by-product formation in the fermentation of Anaerobiospirillum succiniciproducens using glycerol as a carbon source. Biotechnol Bioeng 72:41–48
Lee SJ, Song H, Lee SY (2006) Genome-based metabolic engineering of M. succiniproducens for succinic acid production. Appl Environ Microbiol 72(3):1939–1948
Li J, Zheng XY, Fang XJ, Liu SW, Chen KQ, Jiang M, Wei P, Ouyang PK (2011) A complete industrial system for economical succinic acid production by Actinobacillus succinogenes. Bioresource Technol 102(10):6147–6152
Li QA, Siles JA, Thompson IP (2010a) Succinic acid production from orange peel and wheat straw by batch fermentations of Fibrobacter succinogenes S85. Appl Microbiol Biot 88:671–678
Li Q, Yang M, Wang D, Li W, Wu Y, Zhang Y, Xing J, Su Z (2010b) Efficient conversion of crop stalk wastes into succinic acid production by Actinobacillus succinogenes. Bioresource Technol 101(9):3292–3294
Lin H, Bennett GN, San K-Y (2005) Metabolic engineering of aerobic succinate production systems in Escherichia coli to improve process productivity and achieve the maximum theoretical succinate yield. Metabolic Eng 7(2):116–127
Linko YY, Javanainen P (1996) Simultaneous liquefaction, saccharification, and lactic acid fermentation on barley starch. Enz Microb Technol 19(2):118–123
Liu YP, Zheng P, Sun ZH, Ni Y, Dong JJ, Wei P (2008a) Strategies of pH control and glucose-fed batch fermentation for production of succinic acid by Actinobacillus succinogenes CGMCC1593. J Chem Technol Biot 83(5):722–729
Liu YP, Zheng P, Sun ZH, Ni Y, Dong JJ, Zhu LL (2008b) Economical succinic acid production from cane molasses by Actinobacillus succinogenes. Bioresour Technol 99(6):1736–1742
Luo L, van der Voet E, Huppes G (2010) Biorefining of lignocellulosic feedstock – technical, economic and environmental considerations. Bioresour Technol 101(13):5023–5032
Ma JF, Jiang M, Chen KQ, Xu B, Liu SW, Wei P, Ying HJ, Chang HN, Ouyang PK (2011) Strategies for efficient repetitive production of succinate using metabolically engineered Escherichia coli. Bioprocess Biosyst Eng 34(4):411–418
Marques S, Santos JAL, Gírio FM, Roseiro JC (2008) Lactic acid production from recycled paper sludge by simultaneous saccharification and fermentation. Bioch Eng J 41(3):210–216
Medema MH, Van Raaphorst R, Takano E, Breitling R (2012) Computational tools for the synthetic design of biochemical pathways. Nat Rev Microbiol 10(3):191–202
McKinlay JB, Vieille C (2008) 13C-metabolic flux analysis of A. succinogenes fermentative metabolism at different NaHCO3 and H2 concentrations. Metab Eng 10(1):55–68
McKinlay JB, Vieille C, Zeikus JG (2007) Prospects for a bio-based succinate industry. Appl Microbiol Biot 76(4):727–740
Miura S, Arimura T, Itoda N, Dwiarti L, Feng JB, Bin CH, Okabe M (2004) Production of lactic acid from corncob. J Biosci Bioeng 97(3):153–157
Moldes AB, Alonso JL, Parajö JC (2000) Multi-step feeding systems for lactic acid production by simultaneous saccharification and fermentation of processed wood. Bioproc Eng 22(2):175–180
Mosier N, Wyman C, Dale B, Elander R, Lee Y, Holtzapple M, Ladisch M (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Bioresour Technol 96(6):673–686
Nghiem NP (1997) Production of succinic acid by Anaerobiospirillum succiniciproducens. Appl Biochem Biotech 63–65(1–3):565–576
Okino S, Inui M, Yukawa H (2005) Production of organic acids by Corynebacterium glutamicum under oxygen deprivation. Appl Microbiol Biot 68(4):475–480
Okino S, Noburyu R, Suda M, Jojima T, Inui M, Yukawa H (2008) An efficient succinic acid production process in a metabolically engineered Corynebacterium glutamicum strain. Appl Microbiol Biot 81(3):459–464
Park EY, Anh PN, Okuda N (2004) Bioconversion of waste office paper to l-(+)-lactic acid by the filamentous fungus Rhizopus oryzae. Bioresource technol 93(1):77–83
Raab AM, Gebhardt G, Bolotina N, Weuster-Botz D, Lang C (2010) Metabolic engineering of Saccharomyces cerevisiae for the biotechnological production of succinic acid. Metab Eng 12:518–525
Rajaram S, Varma A (1990) Production and characterization of xylanase from Bacillus thermoalkalophilus grown on agricultural wastes. Appl Microbiol Biotechnol 34:141–144
Rose JKC, Bennett AB (1999) Cooperative disassembly of the cellulose–xyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. Trends Plant 4(5):176–183
Samuelov NS, Datta R, Jain MK, Zeikus JG (1999) Whey fermentation by Anaerobiospirillum succiniciproducens for production of a succinate-based animal feed additive. Appl Environ Microbiol 65(5):2260–2263
Sánchez AM, Bennett GN, San KY (2005) Novel pathway engineering design of the anaerobic central metabolic pathway in Escherichia coli to increase succinate yield and productivity. Metab Eng 7(3):229–239
Song H, Huh YS, Lee SY, Hong WH, Hong YK (2007) Recovery of succinic acid produced by fermentation of a metabolically engineered Mannheimia succiniciproducens strain. J Biotechnol 132(4):445–452
Song H, Jang SH, Park JM, Lee SY (2008) Modeling of batch fermentation kinetics for succinic acid production by Mannheimia succiniciproducens. Biochem Eng J 40(1):107–115
Song H, Lee SY (2006) Production of succinic acid by bacterial fermentation. Enzyme Microb Technol 39(3):352–361
Stols L, Donnelly MI (1997) Production of succinic acid through overexpression of NAD(+)-dependent malic enzyme in an Escherichia coli mutant. Appl Environ Microbiol 63(7):2695–2701
Van Dyk JS, Pletschke BI (2012) A review of lignocellulose bioconversion using enzymatic hydrolysis and synergistic cooperation between enzymes—factors affecting enzymes, conversion and synergy. Biotechnol Adv 30(6):1458–1480
Vemuri GN, Eiteman MA, Altman E (2002) Effects of growth mode and pyruvate carboxylase on succinic acid production by metabolically engineered strains of Escherichia coli. Appl Environ Microbiol 68(4):1715–1727
Venkatesh KV (1997) Simultaneous saccharification and fermentation of cellulose to lactic acid. Bioresource Technol 62(3):91–98
Wang D, Li QA, Yang MH, Zhang YJ, Su ZG, Xing JM (2011) Efficient production of succinic acid from corn stalk hydrolysates by a recombinant Escherichia coli with ptsG mutation. Process Biochem 46:365–371
Willke T, Vorlop KD (2004) Industrial bioconversion of renewable resources as an alternative to conventional chemistry. App Microbiol Biotechnol 66(2):131–142
Xu Q, Singh A, Himmel ME (2009) Perspectives and new directions for the production of bioethanol using consolidated bioprocessing of lignocellulose. Curr Opin Biotechnol 20(3):364–371
Yáñez R, Moldes AB, Alonso JL, Parajó JC (2003) Production of d-(−)-lactic acid from cellulose by simultaneous saccharification and fermentation using Lactobacillus coryniformis subsp. torquens. Biotechnol lett 25(14):1161–1164
Zeikus JG (1980) Chemical and fuel production by anaerobic bacteria. Annu Rev Microbiol 34:423–464
Zeikus JG, Jain MK, Elankovan P (1999) Biotechnology of succinic acid production and markets for derived industrial products. Appl Microbiol Biotechnol 51(5):545–552
Zhang X, Jantama K, Moore JC, Jarboe LR, Shanmugam KT, Ingram LO (2009) Metabolic evolution of energy-conserving pathways for succinate production in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 106(48):20180–20185. doi:10.1073/pnas.0905396106
Zhang ZY, Jin B, Kelly JM (2007) Production of lactic acid from renewable materials by Rhizopus fungi. Biochem Eng J 35(3):251–263
Zheng P, Dong JJ, Sun ZH, Ni Y, Fang L (2009) Fermentative production of succinic acid from straw hydrolysate by Actinobacillus succinogenes. Bioresource Technol 100(8):2425–2429
Zheng P, Fang L, Xu Y, Dong JJ, Ni Y, Sun ZH (2010) Succinic acid production from corn stover by simultaneous saccharification and fermentation using Actinobacillus succinogenes. Bioresource Technol 101(20):7889–7894
Zhu S, Wu Y, Yu Z, Liao J, Zhang Y (2005) Pretreatment by microwave/alkali of rice straw and its enzymic hydrolysis. Process Biochem 40(9):3082–3086
Zhu S, Wu Y, Yu Z, Wang C, Yu F, Jin S, Ding Y, Ra C, Liao J, Zhang Y (2006) Comparison of three microwave/chemical pretreatment processes for enzymatic hydrolysis of rice straw. Biosyst Eng 93(3):279–283
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Akhtar, J., Idris, A. & Abd. Aziz, R. Recent advances in production of succinic acid from lignocellulosic biomass. Appl Microbiol Biotechnol 98, 987–1000 (2014). https://doi.org/10.1007/s00253-013-5319-6
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DOI: https://doi.org/10.1007/s00253-013-5319-6