Stirring the hydrogen and butanol production from Enset fiber via simultaneous saccharification and fermentation (SSF) process

Abstract

Enset fiber is a promising feedstock for biofuel production with the potential to reduce carbon emissions and improve the sustainability of the energy system. This study aimed to maximize hydrogen and butanol production from Enset fiber through simultaneous saccharification and fermentation (SSF) process in bottles as well as in bioreactor. The SSF process in bottles resulted in a higher butanol concentration of 11.36 g/L with a yield of 0.23 g/g and a productivity of 0.16 g/(L h) at the optimal process parameters of 5% (w/v) substrate loading, 16 FPU/g cellulase loading, and 100 rpm agitation speed from pretreated Enset fiber. Moreover, a comparable result to the bottle experiment was observed in the bioreactor with pH-uncontrolled SSF process, although with a decreased in butanol productivity to 0.095 g/(L h). However, using the pre-hydrolysis simultaneous saccharification and fermentation (PSSF) process in the bioreactor with a 7% (w/v) substrate loading led to the highest butanol concentration of 12.84 g/L with a productivity of 0.104 g/(L h). Furthermore, optimizing the SSF process parameters to favor hydrogen resulted in an increased hydrogen yield of 198.27 mL/g-Enset fiber at atmospheric pressure, an initial pH of 8.0, and 37 °C. In general, stirring the SSF process to shift the product ratio to either hydrogen or butanol was possible by adjusting temperature and pressure. At 37 °C and atmospheric pressure, the process resulted in an e-mol yield of 12% for hydrogen and 38% for butanol. Alternatively, at 30 °C and 0.55 bar overpressure, the process achieved a yield of 6% e-mol of hydrogen and 48% e-mol of butanol. This is the first study to produce hydrogen and butanol from Enset fiber using the SSF process and contributes to the development of a circular bioeconomy.

Graphical Abstract

References

[1] AhmedSF, RafaN, MofijurM, BadruddinIA, InayatA, AliMS, FarrokO, Yunus KhanTM. Biohydrogen production from biomass sources: metabolic pathways and economic analysis. Front Energy Res, 2021, 9: 1-13

[2] AlalayahWM, KalilMS, KadhumAAH, JahimJM, AlaujNM. Hydrogen production using Clostridium saccharoperbutylacetonicum N1–4 (ATCC 13564). Int J Hydrogen Energy, 2008, 33: 7392-7396

[3] Al-ShorganiNKN, ShukorH, AbdeshahianP, Mohd NazirMY, KalilMS, HamidAA, Wan YusoffWM. Process optimization of butanol production by Clostridium saccharoperbutylacetonicum N1–4 (ATCC 13564) using palm oil mill effluent in acetone-butanol-ethanol fermentation. Biocatal Agric Biotechnol, 2015, 4: 244-249

[4] BalsanG, AstolfiV, BenazziT, MeirelesMAA, MaugeriF, Di LuccioM, Dal PráV, MossiAJ, TreichelH, MazuttiMA. Characterization of a commercial cellulase for hydrolysis of agroindustrial substrates. Bioprocess Biosyst Eng, 2012, 35: 1229-1237

[5] BorrellJS, BiswasMK, GoodwinM, BlommeG, SchwarzacherT, Heslop-HarrisonJS, WendawekAM, BerhanuA, KallowS, JanssensS, et al. . Enset in Ethiopia: a poorly characterized but resilient starch staple. Ann Bot, 2019, 123: 747-766

[6] BrosseauJD, YanJ-Y, LoKV. The relationship between hydrogen gas and butanol production by Clostridium saccharoperbutylacetonicum. Biotechnol Bioeng, 1986, 28: 305-310

[7] CebreirosF, FerrariMD, LareoC. Cellulose hydrolysis and IBE fermentation of eucalyptus sawdust for enhanced biobutanol production by Clostridium beijerinckii DSM 6423. Ind Crops Prod, 2019, 134: 50-61

[8] ChenC, WangL, XiaoG, LiuY, XiaoZ, DengQ, YaoP. Continuous acetone-butanol-ethanol (ABE) fermentation and gas production under slight pressure in a membrane bioreactor. Bioresour Technol, 2014, 163: 6-11

[9] ChengCL, LoYC, LeeKS, LeeDJ, LinCY, ChangJS. Biohydrogen production from lignocellulosic feedstock. Bioresour Technol, 2011, 102: 8514-8523

[10] ChengC, BaoT, YangST. Engineering Clostridium for improved solvent production: recent progress and perspective. Appl Microbiol Biotechnol, 2019, 103: 5549-5566

[11] Dahman Y, Syed K, Begum S, Roy P, Mohtasebi B (2019) Biofuels: their characteristics and analysis. In: Woodhead publishing series in composites science and engineering,Biomass, biopolymer-based materials, and bioenergy, Woodhead Publishing. Elsevier Ltd, Amsterdam. https://doi.org/10.1016/B978-0-08-102426-3.00014-X

[12] DongJJ, DingJC, ZhangY, MaL, XuGC, HanRZ, NiY. Simultaneous saccharification and fermentation of dilute alkaline-pretreated corn stover for enhanced butanol production by Clostridium saccharobutylicum DSM 13864. FEMS Microbiol Lett, 2016, 363: 1-6

[13] dos SantosAC, XimenesE, KimY, LadischMR. Lignin-enzyme interactions in the hydrolysis of lignocellulosic biomass. Trends Biotechnol, 2019, 37: 518-531

[14] FatehiP. Recent advancements in various steps of ethanol, butanol, and isobutanol productions from woody materials. Biotechnol Prog, 2013, 29: 297-310

[15] FengJ, ZongW, WangP, ZhangZT, GuY, DoughertyM, BorovokI, WangY. RRNPP-Type quorum-sensing systems regulate solvent formation, sporulation and cell motility in Clostridium saccharoperbutylacetonicum. Biotechnol Biofuels, 2020, 13: 1-16

[16] FerchichiM, CrabbeE, HintzW, GilGH, AlmadidyA. Influence of culture parameters on biological hydrogen production by Clostridium saccharoperbutylacetonicum ATCC 27021. World J Microbiol Biotechnol, 2005, 21: 855-862

[17] FoulquierC, RivièreA, HeulotM, Dos ReisS, PerduC, GirbalL, PinaultM, DusséauxS, YooM, SoucailleP, et al. . Molecular characterization of the missing electron pathways for butanol synthesis in Clostridium acetobutylicum. Nat Commun, 2022, 13: 1-11

[18] GoriaK, SinghHM, SinghA, KothariR, TyagiVV. Insights into biohydrogen production from algal biomass: challenges, recent advancements and future directions. Int J Hydrogen Energy, 2023

[19] GuanW, ShiS, TuM, LeeYY. Acetone-butanol-ethanol production from Kraft paper mill sludge by simultaneous saccharification and fermentation. Bioresour Technol, 2016, 200: 713-721

[20] GuoY, LiuY, GuanM, TangH, WangZ, LinL, PangH. Production of butanol from lignocellulosic biomass: recent advances, challenges, and prospects. RSC Adv, 2022, 12: 18848-18863

[21] HeCR, KuoYY, LiSY. Lignocellulosic butanol production from Napier grass using semi-simultaneous saccharification fermentation. Bioresour Technol, 2017, 231: 101-108

[22] International Energy Agency (IEA) (2022) Global CO2 emissions rebounded to their highest level in history in 2021

[23] KumarM, GoyalY, SarkarA, GayenK. Comparative economic assessment of ABE fermentation based on cellulosic and non-cellulosic feedstocks. Appl Energy, 2012, 93: 193-204

[24] Kumar RamamoorthyN, SambaviTR, RenganathanS. A study on cellulase production from a mixture of lignocellulosic wastes. Process Biochem, 2019, 83: 148-158

[25] LeeSY, ParkJH, JangSH, NielsenLK, KimJ, JungKS. Fermentative butanol production by clostridia. Biotechnol Bioeng, 2008, 101: 209-228

[26] LiD, ChenH. Biological hydrogen production from steam-exploded straw by simultaneous saccharification and fermentation. Int J Hydrogen Energy, 2007, 32: 1742-1748

[27] LiJ, ZhangY, ShiS, TuM. Effect of residual extractable lignin on acetone-butanol-ethanol production in SHF and SSF processes. Biotechnol Biofuels, 2020, 13: 1-12

[28] Md RazaliNAA, IbrahimMF, BahrinEK, Abd-AzizS. Optimisation of simultaneous saccharification and fermentation (SSF) for biobutanol production using pretreated oil palm empty fruit bunch. Molecules, 2018

[29] Michael B, Maria AT (2023) Global Climate Litigation Report: 2023 Status Review

[30] Midhun PrasadK, SomasundaramM, AnandB, ShankarR, RajkumarP. A review on pyrolysis of agro-waste and plastic waste into biofuels: shifting to bio-based economy. Bioenergy Res, 2023, 16: 1438-1466

[31] NakayamaS, BandoY, OhnishiA, KadokuraT, NakazatoA. Decreased hydrogen production leads to selective butanol production in co-cultures of Clostridium thermocellum and Clostridium saccharoperbutylacetonicum strain N1–4. J Biosci Bioeng, 2013, 115: 173-175

[32] OberoiHS, VadlaniPV, SaidaL, BansalS, HughesJD. Ethanol production from banana peels using statistically optimized simultaneous saccharification and fermentation process. Waste Manag, 2011, 31: 1576-1584

[33] ÖhgrenK, BuraR, SaddlerJ, ZacchiG. Effect of hemicellulose and lignin removal on enzymatic hydrolysis of steam pretreated corn stover. Bioresour Technol, 2007, 98: 2503-2510

[34] OlofssonK, BertilssonM, LidénG. A short review on SSF – an interesting process option for ethanol production from lignocellulosic feedstocks. Biotechnol Biofuels, 2008, 14: 1-14

[35] PrattoB, ChandgudeV, de SousaR, CruzAJG, BankarS. Biobutanol production from sugarcane straw: defining optimal biomass loading for improved ABE fermentation. Ind Crops Prod, 2020

[36] QiG, HuangD, WangJ, ShenY, GaoX. Enhanced butanol production from ammonium sulfite pretreated wheat straw by separate hydrolysis and fermentation and simultaneous saccharification and fermentation. Sustain Energy Technol Assessments, 2019, 36: 100549

[37] QureshiN, SinghV, LiuS, EzejiTC, SahaBC, CottaMA. Process integration for simultaneous saccharification, fermentation, and recovery (SSFR): Production of butanol from corn stover using Clostridium beijerinckii P260. Bioresour Technol, 2014, 154: 222-228

[38] RajagopalanG, HeJ, YangKL. One-pot fermentation of agricultural residues to produce butanol and hydrogen by Clostridium strain BOH3. Renew Energy, 2016, 85: 1127-1134

[39] RajakJ. A preliminary review on impact of climate change and our environment with reference to global warming. Int J Environ Sci, 2021, 10: 11-14

[40] SallehMSM, IbrahimMF, RoslanAM, Abd-AzizS. Improved biobutanol production in 2-L simultaneous saccharification and fermentation with delayed yeast extract feeding and in-situ recovery. Sci Rep, 2019, 9: 1-9

[41] SarkarB, YaserD. Enhanced biobutanol production using novel clostridial fusants in simultaneous saccharifi cation and fermentation of green renewable agriculture residues. Biofuels Bioprod Biorefining, 2014, 8: 743

[42] SeidN, GriesheimerP, NeumannA. Investigating the processing potential of ethiopian agricultural residue enset/ensete ventricosum for biobutanol production. Bioengineering, 2022, 9: 1-14

[43] SeidN, OchsenreitherK, NeumannA. Caproate production from Enset fiber in one-pot two-step fermentation using anaerobic fungi (Neocallimastix cameroonii strain G341) and Clostridium kluyveri DSM 555. Microb Cell Fact, 2023

[44] SinghV, SinghH, DasD. Optimization of the medium composition for the improvement of hydrogen and butanol production using Clostridium saccharoperbutylacetonicum DSM 14923. Int J Hydrogen Energy, 2019, 44: 26905-26919

[45] SinghV, YadavS, SenR, DasD. Concomitant hydrogen and butanol production via co-digestion of organic wastewater and nitrogenous residues. Int J Hydrogen Energy, 2020, 45: 24477-24490

[46] Sluiter A, Hames B, Hyman D, Payne C, Ruiz R, Scarlata C, Sluiter J, Templeton D, Wolfe J (2008) Determination of total solids in biomass and total dissolved solids in liquid process samples

[47] SoniBK, DasK, GhoseTK. Inhibitory factors involved in acetone-butanol fermentation by Clostridium saccharoperbutylacetonicum. Curr Microbiol, 1987, 16: 61-67

[48] SteinUH, Abbasi-HosseiniM, KainJ, FuchsW, BochmannG. Influence of gas-release strategies on the production of biohydrogen and biobutanol in ABE fermentation. Biofuels, 2022, 13: 9-15

[49] VallesA, Álvarez-HornosFJ, Martínez-SoriaV, MarzalP, GabaldónC. Comparison of simultaneous saccharification and fermentation and separate hydrolysis and fermentation processes for butanol production from rice straw. Fuel, 2020

[50] Vamsi KrishnaK, BharathiN, George ShijuS, Alagesan PaariK, MalaviyaA. An updated review on advancement in fermentative production strategies for biobutanol using Clostridium spp, 2022BerlinSpringer

[51] WangYB, GaoC, ZhengZ, LiuFM, ZangJY, MiaoJL. Immobilization of cold-active cellulase from antarctic bacterium and its use for kelp cellulose ethanol fermentation. BioResources, 2015, 10: 1757-1772

[52] WangP, ChenYM, WangY, LeeYY, ZongW, TaylorS, McDonaldT, WangY. Towards comprehensive lignocellulosic biomass utilization for bioenergy production: efficient biobutanol production from acetic acid pretreated switchgrass with Clostridium saccharoperbutylacetonicum N1–4. Appl Energy, 2019, 236: 551-559

[53] WeissND, FelbyC, ThygesenLG. Enzymatic hydrolysis is limited by biomass-water interactions at high-solids: improved performance through substrate modifications 09 engineering 0904 chemical engineering 09 engineering 0915 interdisciplinary engineering. Biotechnol Biofuels, 2019, 12: 1-13

[54] WingrenA, GalbeM, ZacchiG. Techno-economic evaluation of producing ethanol from softwood: comparison of SSF and SHF and identification of bottlenecks. Biotechnol Prog, 2003, 19: 1109-1117

[55] WuH, WangC, ChenP, HeAY, XingFX, KongXP, JiangM. Effects of pH and ferrous iron on the coproduction of butanol and hydrogen by Clostridium beijerinckii IB4. Int J Hydrogen Energy, 2017, 42: 6547-6555

[56] WuY, WangZ, MaX, XueC. High temperature simultaneous saccharification and fermentation of corn stover for efficient butanol production by a thermotolerant Clostridium acetobutylicum. Process Biochem, 2021, 100: 20-25

[57] YadavS, SinghV, MahataC, DasD. Optimization for simultaneous enhancement of biobutanol and biohydrogen production. Int J Hydrogen Energy, 2021, 46: 3726-3741

[58] YangX, TuM, XieR, AdhikariS, TongZ. A comparison of three pH control methods for revealing effects of undissociated butyric acid on specific butanol production rate in batch fermentation of Clostridium acetobutylicum. AMB Express, 2013, 3: 1-8

[59] YaoD, DongS, WangP, ChenT, WangJ, YueZB, WangY. Robustness of Clostridium saccharoperbutylacetonicum for acetone-butanol-ethanol production: effects of lignocellulosic sugars and inhibitors. Fuel, 2017, 208: 549-557

[60] YerushalmiL, VoleskyB, SzczesnyT. Effect of increased hydrogen partial pressure on the acetone-butanol fermentation by Clostridium acetobutylicum. Appl Microbiol Biotechnol, 1985, 22: 103-107

[61] ZhaoT, TashiroY, SonomotoK. Smart fermentation engineering for butanol production: designed biomass and consolidated bioprocessing systems. Appl Microbiol Biotechnol, 2019, 103: 9359-9371

[62] ZhengJ, TashiroY, WangQ, SonomotoK. Recent advances to improve fermentative butanol production: genetic engineering and fermentation technology. J Biosci Bioeng, 2015, 119: 1-9

Funding

German Academic Exchange Service(DAAD-EECBP Homegrown Ph.D. Scholarship Program 2019)

Karlsruhe Institute of Technology(APC was funded by the Karlsruhe Institute of Technology (KIT) Publication Fund)

Karlsruher Institut für Technologie (KIT) (4220)