Abstract
An empty oil-palm fruit bunch (EFB) has been proposed as an alternative lignocellulose with potential to produce bio-succinate. However, studies of succinate production from EFB were sparse. Succinate concentrations and yield reported in published literatures were still low. To be more attractive, the utilization of EFB for bio-succinate at high concentrations and yields was demonstrated in this study. EFB was thermochemically pretreated employing diluted H2SO4, 121 °C for 30 min. After pretreatment, detoxification of EFB black-liquor hemicellulosic hydrolysate exploiting 0.5%(w/v) activated carbon could remove 92.04% furfural and 100% HMF derived from degraded sugars and fatty acids in EFB. Removals of 76.4% acetate and 95.80% phenols from the activated carbon-treated hydrolysate were further achieved by vacuum distillation. The 70%(v/v) detoxified hydrolysate showed the least inhibitory effect on succinate production at the level of 54.8 ± 1.5 g/L by Escherichia coli KJ12201-14 T. Alternatively, 70 g/L acid-pretreated EFB cellulosic solid was hydrolyzed with minimized cellulase and β-glucosidase at a ratio of 15FPU:10CBU/g to release fermentable sugars at 94.02% recovery to produce 32.3 ± 1.6 g/L succinate. A combined fraction of 50%(v/v) detoxified EFB hydrolysate and 70 g/L cellulosic EFB solid was additionally utilized to produce succinate at 72.5 ± 0.8 g/L with a yield of 0.83 ± 0.02 g/g. These concentration and yield attained were highest than those of previous literatures. Our fermentation differs from published reports in the application of low inorganic-salts medium (0.9 g/L) without supplementation of any rich nutrients. These may reduce costs of medium, purification, energy consumption, and waste disposal. Our developed process may be an economically feasible option for future industrial succinate production.
Similar content being viewed by others
Data availability
Not applicable.
References
Oliverira DM, Mota TR, Ferrarese-Filho O, dos Santos WD (2021) Sustainable production of succinic acid and 3-hydroxypropionic acid from renewable feedstocks. In: Chandel AK, Fernando S (eds) Production of Top 12 Biochemicals Selected by USDOE from Renewable Resources, 1st edn. Elsevier, Cambridge, USA, pp 367–386
Chundawat SPS, Beckham GT, Himmel ME, Dale BE (2011) Deconstruction of lignocellulosic biomass to fuels and chemicals. Annu Rev Chem Biomol Eng 2:121–145
Zheng P, Dong JJ, Sun ZH, Ni Y, Fang L (2009) Fermentative production of succinic acid from straw hydrolysate by Actinobacillus succinogenes. Bioresour Technol 100:2425–2429
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
Li Q, Yang M, Wang D, Li W, Wu Y, Zhang Y, Xing J, Su Z (2010) Efficient conversion of corn stalk wastes into succinic acid production by Actinobacillus succinogenes. Bioresour Technol 101:3292–3294
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. Bioresour Technol 101:7889–7894
Li J, Zheng XY, Fang XI, Liu SW, Chen KQ, Jiang M, Wei P, Ouyang PK (2011) A complete industrial system for economical succinic acid production by Actinobacillus succinogenes. Bioresour Technol 102:6147–6152
Li QA, Siles JA (2010) Thompson IP Succinic acid production from orange peel and wheat straw by batch fermentations of Fibrobacter succinogenes S85. Appl Microbiol Biotechnol 88:671–678
Borges ER, Pereira N (2011) Succinic acid production from sugarcane bagasse hemicellulose hydrolysate by Actinobacillus succinogenes. J Ind Microbiol Biotechnol 38:1001–1011
Chen P, Tao S, Zheng P (2016) Efficient and repeated production of succinic acid by turning sugarcane bagasse into sugar and support. Bioresour Technol 211:406–413
Chen C, Ding S, Wang D, Li Z, Ye Q (2014) Simultaneous saccharification and fermentation of cassava to succininc acid by Escherichia coli NZN111. Bioresour Technol 163:100–105
Hijosa-Valsero M, Paniagua-García AI, Díez-Antolínez R (2022) Assessment of vine shoots and surplus grape must for succinic acid bioproduction. Appl Microbiol Biotechnol 106:4977–4994
Lee JS, Lin CJ, Lee WC, Teng HY, Chuang MH (2002) Production of succinic acid through the fermentation of Actinobacillus succinogenes on the hydrolysate of Napier grass. Biotechnol Biofuels Bioprod 15(1):9. https://doi.org/10.1186/s13068-022-02106-0
Sawisit A, Jampatesh S, Jantama SS, Jantama K (2018) Optimization of sodium hydroxide pretreatment and enzyme loading for efficient hydrolysis of rice straw to improve succinate production by metabolically engineered Escherichia coli KJ122 under simultaneous saccharification and fermentation. Bioresour Technol 260:348–356
Kresnowati M, Mardawati E, Setiadi T (2015) Production of xylitol from oil palm empty fruits bunch: a case study on biorefinery concept. Mod Appl Sci 9:206–213
Akhtar J, Idris A (2017) A Oil palm empty fruit bunches a promising substrate for succinic acid production via simultaneous saccharification and fermentation. Renew Energy 114:917–923
Luthfi AA, Jahim JM, Harun S, Tan JP, Manaf SFA, Shah SSM (2018) Kinetics of the bioproduction of succinic acid by Actinobacillus succinogenes from oil palm lignocellulosic hydrolysate in bioreactor. BioRes 13:8279–8294
Khunnonkwao P, Jantanma SS, Kanchanatawee S, Jantama K (2018) Re-engineering Escherichia coli KJ122 to enhance the utilization of xylose and xylose/glucose mixture for efficient succinate production in mineral salt medium. Appl Microbiol Biotechnol 102:127–141
Chaleewong T, Khunnonkwao P, Puchongkawarin C, Jantama K (2022) Kinetic modeling of succinate production from glucose and xylose by metabolically engineered Escherichia coli KJ12201. Biochem Eng J 185:108487. https://doi.org/10.1016/j.bej.2022.108487
Utrilla J, Tah AV, Martinez BT, Gosset G, Martinez A (2016) Production of D-lactate from sugarcane bagasse and corn stover hydrolysates using metabolic engineered Escherichia coli strains. Bioresour Technol 220:208–214
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagent. Am J Enol Vitic 16:144–158
Alvira P, Tomas-Pejo E, Ballesters M, Negro MJ (2010) Pretreatment technologies for an efficient bioethanol production process based on enzymatic hydrolysis: a review. Bioresour Technol 101:4851–4861
Kim S, Park JM, Seo JW, Kim CH (2012) Sequential acid-/alkali pretreatment of empty palm fruit bunch fiber. Bioresour Technol 109:229–233
Siramon P, Punsuvon V, Vaithanomsat P (2018) Production of bioethanol from oil palm empty fruit bunch via acid impregnation-steam explosion pretreatment. Waste Biomass Valor 9:1407–1414
do Nascimento BF, de Araujo CMB, do Nascimento AC, da Silva FLH, de Melo DJN, Jaguaribe EF, Lima Cavalcanti JVF, da Motta Sobrinho MA (2021) Detoxification of sisal bagasse hydrolysate using activated carbon produced from the gasification of acai waste. J Hazard Mater 409:124494
Preechakun T, Pongchaiphol S, Raita M, Champreda V, Laosiripojana N (2022) Detoxification of hemicellulose-enriched hydrolysate from sugarcane bagasse by activated carbon and macroporous adsorption resin. Biomass Conv Bioref. https://doi.org/10.1007/s13399-022-03596-6
Han J, Xu B, Wang H, Huang G, Zhang X, Xu Y (2022) Purification of acidic lignocellulose hydrolysate using anion-exchange resin: multicomponent adsorption, kinetic and thermodynamic study. Bioresour Technol 351:126979. https://doi.org/10.1016/j.biortech.2022.126979
Jin T, Xing X, Xie Y, Sun Y, Bian S, Liu L, Chen G, Wang X, Yu X, Su Y (2023) Evaluation of preparation and detoxification of hemicellulose hydrolysate for improved xylitol production from quinoa straw. Int J Mol Sci 24:516. https://doi.org/10.3390/ijms24010516
Zhang Y, Li M, Wang Y, Ji X, Zhang L, Hou L (2015) Simultaneous concentration and detoxification of lignocellulosic hydrolysates by vacuum membrane distillation coupled with adsorption. Bioresour Technol 197:276–283
Zhu J, Yong Q, Xu Y, Yu S (2011) Detoxification of corn stover pre-hydrolysate by trialkylamine extraction to improve the ethanol production with Pichia stipitis CBS 5776. Bioresour Technol 102:663–1668
Avci A, Saha BC, Dien BS, Kennedy GJ, Cotta MA (2013) Response surface optimization of corn stover pre-treatment using dilute phosphoric acid for enzymatic hydrolysis and ethanol production. Bioresour Technol 130:603–612
Jampatesh S, Sawisit A, Wong N, Jantama SS, Jantama K (2019) Evaluation of inhibitory effect and feasible utilization of diluted-acid-pretreated rice straw on succinate production by metabolically engineered Escherichia coli AS1600a. Bioresour Technol 273:93–102
Liu R, Liang L, Li F, Wu M, Chen K, Ma J, Jiang M, Wei P, Ouyang P (2013) Efficient succinic acid production from lignocellulosic biomass by simultaneous utilization of glucose and xylose in engineered Escherichia coli. Bioresour Technol 149:84–91
Ventorino V, Robertiello A, Cimini D, Argenzio O, Schiraldi C, Montella S, Faraco V, Ambrosanio A, Viscardi S, Pepe O (2017) Bio-based succinate production from Arundo donax hydrolysate with the new natural succinic acid-producing strain Basfia succiniciproducens BPP7. BioEnergy Res: 488–498.
Salvachúa D, Mohagheghi A, Smith H, Bradfield MFA, Nicol W, Black BA, Biddy WJ, Dowe N, Beckham GT (2016) Succinic acid production on xylose-enriched biorefinery streams by Actinobacillus succinogenes in batch fermentation. Biotechnol Biofuels 9. https://doi.org/10.1186/s13068-016-0425-1.
Pateraki C, Ladakis D, Stragier L, Verstraete W, Kookos I, Papanikolaou S, Koutinas A (2016) Pretreatment of spent sulphite liquor via ultrafiltration and nanofiltration for bio-based succinic acid production. J Biotechnol 233:95–105
Akhtar J, Hassan N, Idris A, Ngadiman NHA (2019) Optimization of simultaneous saccharification and fermentation process conditions for the production of succinic acid from oil palm empty fruit bunches. J Wood Chem Technol 40:136–145
Bu J, Yan X, Wang YT, Zhu SM, Zhu MJ (2019) Co-production of high-gravity bioethanol and succinic acid from potassium peroxymonosulfate and deacetylation sequentially pretreated sugarcane bagasse by simultaneous saccharification and co-fermentation. Energy Convers Manag 186:131–139
Menon V, Rao M (2012) Trends in bioconversion of lignocellulose: biofuels, platform chemicals and biorefinery concept. Prog Energy Combust Sci 38:522–550
Castro E, Nieves IS, Mullinnix MT, Sagues WJ, Hoffman RW, Fernandez-Sandoval MT, Tian Z, Rockwood DL, Tamang B, Ingram LO (2014) Optimization of dilute-phosphoric-acid steam pretreatment of Eucalyptus benthamii for biofuel production. Appl Energy 125:76–83
Lu J, Lv Y, Jiang Y, Wu M, Xu B, Zhang W, Zhou J, Dong W, Xin F, Jiang M (2020) Consolidated bioprocessing of hemicellulose-enriched lignocellulose to succinic acid through a microbial cocultivation system. ACS Sustainable Chem Eng 8:9035–9045
Zheng Z, Chen T, Zhao M, Wang Z, Zhao X (2012) Engineering Escherichia coli for succinate production from hemicellulose via consolidated bioprocessing. Microb Cell Fact 11:37
Alcantara J, Mondala A, Hughey L, Shields S (2017) Direct succinic acid production from minimally pretreated biomass using sequential solid-state fermentation with mixed fungal cultures. Fermentation 3(3):30
Filippi K, Georgaka N, Alexandri M, Papapostolou H, Koutinas A (2021) Valorisation of grape stalks and pomace for the production of bio-based succinic acid by Actinobacillus succinogenes. Ind Crops Prod 168:113578
Alexandri M, Schneider R, Papapostolou H, Ladakis D, Koutinas A, Venus J (2019) Restructuring the conventional sugar beet industry into a novel biorefnery: fractionation and bioconversion of sugar beet pulp into succinic acid and value-added coproducts. ACS Sustain Chem Eng 7:6569–6579
Efthymiou MN, Pateraki C, Papapostolou H, Lin CSK, Koutinas A (2021) Restructuring the sunfower-based biodiesel industry into a circular bio-economy business model converting sunfower meal and crude glycerol into succinic acid and value-added co-products. Biomass Bioenergy 155:106265
Ferone M, Raganati F, Ercole A, Olivieri G, Salatino P, Marzocchella A (2018) Continuous succinic acid fermentation by Actinobacillus succinogenes in a packed-bed bioflm reactor. Biotechnol Biofuels 11:138
Jantama K (2022) Technology toward biochemicals precursors and bioplastic production. In: Thongchul N, Kokossis A, Assabumrungrat S (eds) A-Z of biorefinery: a comprehensive view, 1st edn. Elsevier, Cambridge, USA, pp 265–341
Sorokina KN, Samoylova YV, Gromov NV, Ogorodnikova OL, Parmon VN (2020) Production of biodiesel and succinic acid from the biomass of the microalga Micractinium sp. IC-44. Bioresour Tech 317:124026. https://doi.org/10.1016/j.biortech.2020.124026
Knoshaug EP, Mohagheghi A, Nagle NJ, Stickel JJ, Dong T, Karp EM, Kruger JS, Brandner DG, Manker LP, Rorrer NA, Hyman DA, Christensen ED, Pienkos PT (2018) Demonstration of parallel algal processing: production of renewable diesel blendstock and a high-value chemical intermediate. Green Chem 20:457–468
Chiang YY, Nagarajan D, Lo YC, Chen CY, Ng IS, Chang CH, Lee DJ, Chang JS (2021) Succinic acid fermentation with immobilized Actinobacillus succinogenes using hydrolysate of carbohydrate-rich microalgal biomass. Bioresour Technology 342:126014. https://doi.org/10.1016/j.biortech.2021.126014
Chen K, Jiang M, Wei P, Yao J, Wu H (2010) Succinic acid production from acid hydrolysate of corn fiber by Actinobacillus succinogenes using hydrolysates. Appl Biochem Biotechnol 160:477–485
Chen KQ, Li J, Ma JF, Jiang M, Wei P, Liu ZM (2011) Succinic acid production by Actinobacillus succinogenes using hydrolysates of spent yeast cells and corn fiber. Bioresour Technol 102:1704–1708
Dorado MP, Lin SKC, Koutinas A, Du C, Wang R, Webb C (2009) Cereal-based biorefinery development: utilization of wheat milling by-products for the production of succinic acid. J Biotechnol 143:51–59
Shen N, Zhang H, Qin Y, Wang Q, Zhu J, Li Y, Jiang MG, Huang R (2018) Efficient production of succinic acid from duckweed (Landoltia punctata) hydrolysate by Actinobacillus succinogenes GXAS137. Bioresour Technol 250:35–42
Acknowledgements
All authors thank Suksomboon Palm Oil Co., Ltd. (Thailand) to provide an oil palm empty fruit bunch (EFB) waste used throughout this study.
Funding
This work was financially supported by (i) the Suranaree University of Technology (SUT), (ii) the Thailand Science Research and Innovation (TSRI), and (iii) the National Science Research and Innovation Fund (NSRF) (project code 90464) under the full-time researcher fellowship (Grant No.61/10/2562), and (iv) the Agricultural Research Development Agency (ARDA) (CRP6305030530).
Author information
Authors and Affiliations
Contributions
KJ conceived, designed, and suggested methodology and research plan, supervised, and performed project administration and funding acquisition. PK investigated experiments, provided methodology, and wrote an original draft of the manuscript. CP, SI, and SK helped in investigating experiments. KJ also analyzed and validated data and edited, reviewed, and finalized the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Ethical approval
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Khunnonkwao, P., Phosiran, C., In, S. et al. Valorization of empty oil-palm fruit bunch waste for an efficient improvement of succinic acid production by metabolically engineered Escherichia coli. Biomass Conv. Bioref. (2023). https://doi.org/10.1007/s13399-023-03888-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13399-023-03888-5