Paper mulberry fruit juice: a novel biomass resource for bioethanol production

Abstract

By way of broadening the use of diverse sustainable bioethanol feedstocks, the potentials of Paper mulberry fruit juice (PMFJ), as a non-food, sugar-based substrate, were evaluated for fuel ethanol production. The suitability of PMFJ was proven, as maximum ethanol concentration (56.4 g/L) and yield (0.39 g/g) were achieved within half a day of the start of fermentation, corresponding to very high ethanol productivity of 4.7 g/L/hr. The established potentials were further optimally maximized through the response surface methodology (RSM). At the optimal temperature of 30 °C, yeast concentration of 0.55 g/L, and pH of 5, ethanol concentration, productivity, and yield obtained were 73.69 g/L, 4.61 g/L/hr, and 0.48 g/g, respectively. Under these ideal conditions, diverse metal salts were afterward screened for their effects on PMFJ fermentation. Based on a two-level fractional factorial design, nutrient addition had no positive impact on ethanol production. Thus, under the optimal process conditions, and without any external nutrient supplementation, bioethanol from PMFJ compared favorably with typical sugar-based energy crops, highlighting its resourcefulness as a high-value biomass resource for fuel ethanol production.

Keywords

1G feedstock / Ethanol conversion / Response surface methodology / Optimization / Nutrient screening

References

[1] Adigbli DM, Anning AK, Adomako JK, Fosu-mensah BY. Effects of Broussonetia papyrifera invasion and land use on vegetation characteristics in a tropical forest of Ghana. J for Res, 2018

[2] Anning AK, Gyamfi B, Effah AT. Broussonetia papyrifera controls nutrient return to soil to facilitate its invasion in a tropical forest of Ghana. J Plant Ecol, 2018, 11: 909-918.

[3] Authur R, Hayes D, Li M, Wang X, Yang Y, Zhang W (2017) China’s new nationwide E10 ethanol mandate and its global implications. https://www.extension.iastate.edu/agdm/articles/others/Li/Nov17.html. Accessed 10 Apr 2021

[4] Bahrami ME, Honarvar M, Ansari K, Jamshidi B. Measurement of quality parameters of sugar beet juices using near-infrared spectroscopy and chemometrics. J Food Eng, 2020, 271.

[5] Barcelos CA, Maeda RN, Santa Anna LMM, Pereira N. Sweet sorghum as a whole-crop feedstock for ethanol production. Biomass Bioenergy, 2016, 94: 46-56.

[6] Bhadana B, Chauhan M. Bioethanol production using saccharomyces cerevisiae with different perspectives: substrates, growth variables, inhibitor reduction and immobilization. Fermentation, 2016, 5: 2-5.

[7] Cao W, Liu R. Screening and optimization of trace elements supplement in sweet sorghum juice for ethanol production. Biomass Bioenergy, 2013, 50: 45-51.

[8] Chen X, Kuhn E, Jennings EW, Nelson R, Tao L, Zhang M, Tucker MP. DMR (deacetylation and mechanical refining) processing of corn stover achieves high monomeric sugar concentrations (230 g L−1) during enzymatic hydrolysis and high ethanol concentrations (> 10% v/v) during fermentation without hydrolysate purification or concentration. Energy Environ Sci, 2016, 9: 1237-1245.

[9] Chen J, Tang C, Yue Y, Qiao W, Hong J, Kitaoka T, Yang Z. Highly translucent all wood plastics via heterogeneous esterification in ionic liquid/dimethyl sulfoxide. Ind Crops Prod, 2017, 108: 286-294.

[10] Cheng J. Cheng J. Biological process for ethanol production. Biomass to renewable energy processes, 2018, 2, Boca Raton: Taylor & Francis, 144-190.

[11] Choosung P, Utto W, Boonyaritthongchai P, Wasusri T, Wongs-Aree C. Ethanol vapor releasing sachet reduces decay and improves aroma attributes in mulberry fruit. Food Packag Shelf Life, 2019, 22.

[12] Díaz-Nava LE, Montes-Garcia N, Domínguez JM, Aguilar-Uscanga MG. Effect of carbon sources on the growth and ethanol production of native yeast Pichia kudriavzevii ITV-S42 isolated from sweet sorghum juice. Bioprocess Biosyst Eng, 2017, 40: 1069-1077.

[13] Ding Y-M, Hu Y, Yu B-T, Mo X-C, Mo J-C. Laboratory evaluation of differential attraction of Culex pipiens pallens to fruit-based sugar baits. Acta Trop, 2016, 163: 20-25.

[14] Dodić S, Popov S, Dodić J, Ranković J, Zavargo Z, Jevtić Mučibabić R. Bioethanol production from thick juice as intermediate of sugar beet processing. Biomass Bioenergy, 2009, 33: 822-827.

[15] Dular P. Bioethanol production from rotten fruit. Int J Res Appl Sci Eng Technol, 2019, 7: 1555-1560.

[16] Eardley J, Timson DJ. Yeast cellular stress: impacts on bioethanol production. Fermentation, 2020, 6: 109.

[17] Endoh R, Horiyama M, Ohkuma M. D-Fructose assimilation and fermentation by yeasts belonging to saccharomycetes: rediscovery of universal phenotypes and elucidation of fructophilic behaviors in Ambrosiozyma platypodis and Cyberlindnera americana. Microorganisms, 2021, 9: 758.

[18] Garofalo P, Mastrorilli M, Ventrella D, Vonella AV, Campi P. Modelling the suitability of energy crops through a fuzzy-based system approach: The case of sugar beet in the bioethanol supply chain. Energy, 2020, 196.

[19] Giri R, Kundu BS, Diwan P, Raj K, Wati L. Ethanol production from direct sugarcane and juice by yeast. Agric Sci Dig Res J, 2013, 33: 188.

[20] Gonzalez-Lorca J, Rivera-Hutinel A, Moncada X, Lobos S, Seelenfreund D. Ancient and modern introduction of Broussonetia papyrifera ([L.] Vent.; Moraceae) into the Pacific: genetic, geographical and historical evidence. N Z J Bot, 2015, 53: 75-89.

[21] Gumienna M, Szambelan K, Jeleń H, Czarnecki Z. Evaluation of ethanol fermentation parameters for bioethanol production from sugar beet pulp and juice. J Inst Brew, 2014, 120: 543-549.

[22] Hadeel A, Hossain ABMS, Latifa K, ALNaqeb H, Abear J, Norah AH,. Bioethanol fuel production from rambutan fruit biomass as reducing agent of global warming and greenhouse gases. Afr J Biotechnol, 2011, 10: 10157-10165.

[23] Han Q, Wu Z, Huang B, Sun L, Ding C, Yuan S, Zhang Z, Chen Y, Hu C, Zhou L, Liu J, Huang Y, Liao J, Yuan M. Extraction, antioxidant and antibacterial activities of Broussonetia papyrifera fruits polysaccharides. Int J Biol Macromol, 2016, 92: 116-124.

[24] Heede R. Tracing anthropogenic carbon dioxide and methane emissions to fossil fuel and cement producers, 1854–2010. Clim Change, 2014, 122: 229-241.

[25] Hoffmann CM, Koch H-J, Märländer B (2021) Sugar beet. In: Crop physiology case histories for major crops. Elsevier, pp 634–672

[26] IEA-International Energy Agency (2020) Renewables 2020 analysis and forecast to 2025. In: Int Energy Agency. https://www.iea.org/reports/renewables-2020/transport-biofuels. Accessed 29 Mar 2021

[27] Jasman J, Prijambada ID, Hidayat C, Widianto D. Selection of yeast strains for ethanol fermentation of glucose-fructose-sucrose mixture. Indones J Biotechnol, 2015, 17: 114.

[28] Jebril J, Wang D, Rozeboom K, Tesso T. The A3 cytoplasm mediated male sterility increased biomass, soluble solids, and total sugar in sweet sorghum hybrids. Ind Crops Prod, 2021, 171.

[29] Jebril J, Wang D, Rozeboom K, Tesso T. Grain sink removal increases stalk juice yield, sugar accumulation, and biomass in sweet sorghum [Sorghum bicolor (L.) Moench]. Ind Crops Prod, 2021, 173: 114089.

[30] Kayikci Ö, Nielsen J. Glucose repression in Saccharomyces cerevisiae. FEMS Yeast Res, 2015, 15: fov068.

[31] Kelbert M, Romaní A, Coelho E, Pereira FB, Teixeira JA, Domingues L. Lignocellulosic bioethanol production with revalorization of low-cost agroindustrial by-products as nutritional supplements. Ind Crops Prod, 2015, 64: 16-24.

[32] Kielkopf CL, Bauer W, Urbatsch IL. Bradford assay for determining protein concentration. Cold Spring Harb Protoc, 2020

[33] Kim S, Seo AY, Lee TG. Functionalized cellulose to remove surfactants from cosmetic products in wastewater. Carbohydr Polym, 2020, 236.

[34] Klasson KT, Boone SA. Bioethanol fermentation of clarified sweet sorghum (Sorghum bicolor (L.) Moench) syrups sealed and stored under vegetable oil. Ind Crops Prod, 2021, 163: 113330.

[35] Kyereh B, Agyeman VK, Abebrese IK. Ecological characteristics that enhance Broussonetia papyrifera’s invasion in a semideciduous forest in Ghana. J Ecosyst, 2014, 2014: 1-6.

[36] Lee Y, Hwang KT. Changes in physicochemical properties of mulberry fruits (Morus alba L.) during ripening. Sci Hortic, 2017, 217: 189-196.

[37] Liao SX, Deng ZH, Cui K, Cui YZ, Zhang CH. Genetic diversity of Broussonetia papyrifera populations in southwest China. Genet Mol Res, 2014, 13: 7553-7563.

[38] Lin Y, Zhang W, Li C, Sakakibara K, Tanaka S, Kong H. Factors affecting ethanol fermentation using Saccharomyces cerevisiae BY4742. Biomass Bioenergy, 2012, 47: 395-401.

[39] Luo Z, Wang L, Shahbazi A. Optimization of ethanol production from sweet sorghum (Sorghum bicolor) juice using response surface methodology. Biomass Bioenergy, 2014, 67: 53-59.

[40] Maan I, Kaur A, Singh HP, Batish DR, Kohli RK. Evaluating the role of phenology in managing urban invasions: a case study of Broussonetia papyrifera. Urban for Urban Green, 2020, 48.

[41] Maan I, Kaur A, Singh HP, Batish DR, Kohli RK. Exotic avenue plantations turning foe: Invasive potential, distribution and impact of Broussonetia papyrifera in Chandigarh, India. Urban Urban Green, 2021, 59.

[42] Marzo C, Díaz AB, Caro I, Blandino A (2019) Status and perspectives in bioethanol production from sugar beet. In: Bioethanol Production from Food Crops. Elsevier, pp 61–79

[43] Matharasi A, Uma C, Sivagurunathan P, Sampathkumar P. Determination of bioethanol potential from banana waste using indigenous yeast (Saccharomyces cerevisiae. KX033583). J Pharmacogn Phytochem, 2018, 7: 2041-2047.

[44] Micic V, Jotanovic M. Bioethanol as fuel for internal combustion engines. Zastita Mater, 2015, 56: 403-408.

[45] Miller GL. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem, 1959, 31: 426-428.

[46] Mohd Azhar SH, Abdulla R, Jambo SA, Marbawi H, Gansau JA, Mohd Faik AA, Rodrigues KF. Yeasts in sustainable bioethanol production: a review. Biochem Biophys Rep, 2017, 10: 52-61.

[47] Morgan EC, Overholt WA, Sellers B (2013) Wildland weeds: paper mulberry, Broussonetia papyrifera. https://edis.ifas.ufl.edu. Accessed 20 Aug 2021

[48] Nasidi M, Agu R, Deeni Y, Walker G. Fermentation of stalk juices from different Nigerian sorghum cultivars to ethanol. Bioethanol, 2013

[49] OECD-Organisation for economic cooperation and development (2018) Tests to determine quality of fruits and vegetables and dry and dried produce. https://www.oecd.org/agriculturalfruit-vegetable/publications/guidelines_on_objective_tests_2018.pdf. Accessed 10 Aug 2021

[50] Olupot W. The potential of natural succession to restore degraded areas of a Ugandan rainforest dominated by the exotic paper mulberry Broussonetia papyrifera (L.) L’Hér. ex Vent. For Ecol Manag, 2022, 504: 119861.

[51] Palma M, Madeira SC, Mendes-Ferreira A, Sá-Correia I. Impact of assimilable nitrogen availability in glucose uptake kinetics in Saccharomyces cerevisiae during alcoholic fermentation. Microb Cell Factories, 2012, 11: 1-11.

[52] Park J-Y, Yuk HJ, Ryu HW, Lim SH, Kim KS, Park KH, Ryu YB, Lee WS. Evaluation of polyphenols from Broussonetia papyrifera as coronavirus protease inhibitors. J Enzyme Inhib Med Chem, 2017, 32: 504-512.

[53] Park J, Park C-W, Han S-Y, Kwon G-J, Kim N-H, Lee S-H. Effects of pH on nanofibrillation of TEMPO-oxidized paper mulberry bast fibers. Polymers, 2019, 11: 414.

[54] Pe J, Olivares G, Moncada X, Payacán C. Sex distribution of paper mulberry (Broussonetia papyrifera) in the Pacific. PLoS ONE, 2016

[55] Peña-Ahumada B, Saldarriaga-Córdoba M, Kardailsky O, Moncada X, Moraga M, Matisoo-Smith E, Seelenfreund D, Seelenfreund A. A tale of textiles: genetic characterization of historical paper mulberry barkcloth from Oceania. PLoS ONE, 2020, 15.

[56] Peng Y, Changhong W, Jianchang S, Chunhua Y, Minkai W, Hanyuan Y. Investigation on the flowering and fruiting characteristics and the productivity of Broussonetia papyrifera (L.) Vent. Guizhou for Sci Technol, 2010, 38: 24-27.

[57] Peng X, Liu H, Chen P, Tang F, Hu Y, Wang F, Pi Z, Zhao M, Chen N, Chen H, Zhang X, Yan X, Liu M, Fu X, Zhao G, Yao P, Wang L, Dai H, Li X, Xiong W, Xu W, Zheng H, Yu H, Shen S. A chromosome-scale genome assembly of paper mulberry (Broussonetia papyrifera) provides new insights into its forage and papermaking usage. Mol Plant, 2019, 12: 661-677.

[58] Pereira FB, Guimarães PMR, Teixeira JA, Domingues L. Optimization of low-cost medium for very high gravity ethanol fermentations by Saccharomyces cerevisiae using statistical experimental designs. Bioresour Technol, 2010, 101: 7856-7863.

[59] Pinu FR, Edwards PJB, Gardner RC, Villas-Boas SG. Nitrogen and carbon assimilation by Saccharomyces cerevisiae during Sauvignon blanc juice fermentation. FEMS Yeast Res, 2014, 14: 1206-1222.

[60] Rees EMR, Stewart GG. The effects of increased magnesium and calcium concentrations on yeast fermentation performance in high gravity worts. J Inst Brew, 1997, 103: 287-291.

[61] Rolz C, de León R, Mendizábal de Montenegro AL. Co-production of ethanol and biodiesel from sweet sorghum juice in two consecutive fermentation steps. Electron J Biotechnol, 2019, 41: 13-21.

[62] Saito K, Linquist B, Keobualapha B, Shiraiwa T, Horie T. Broussonetia papyrifera (paper mulberry): its growth, yield and potential as a fallow crop in slash-and-burn upland rice system of northern Laos. Agrofor Syst, 2009, 76: 525-532.

[63] Salari M, Sowti Khiabani M, Rezaei Mokarram R, Ghanbarzadeh B, Samadi Kafil H. Preparation and characterization of cellulose nanocrystals from bacterial cellulose produced in sugar beet molasses and cheese whey media. Int J Biol Macromol, 2019, 122: 280-288.

[64] Sewwandi SDC, Arampath PC, Silva ABG, Jayatissa R. Determination and comparative study of sugars and synthetic colorants in commercial branded fruit juice products. J Food Qual, 2020, 2020: 1-11.

[65] Silva LA, Gasparini K, Assis C, Ramos R, Kist V, Barbosa MHP, Teófilo RF, Bhering LL. Selection strategy for indication of crosses between potential sugarcane genotypes aiming at the production of bioenergy. Ind Crops Prod, 2017, 104: 62-67.

[66] Solís-Fuentes JA, Galán-Méndez F, del Hernández-Medel M, R, García-Gómez RS, Bernal-González M, Mendoza-Pérez S, Durán-Domínguez-de-Bazúa M del C,. Effectiveness of bagasse activated carbon in raw cane juice clarification. Food Biosci, 2019, 32.

[67] Somda MK, Savadogo A, Barro N, Thonart PAS. Effect of mineral salt in fermentation process using mango residues as carbon source for bioethanol production. Asian J Ind Eng, 2011, 3: 29-38.

[68] Sun J, Liu SF, Zhang CS, Yu LN, Bi J, Zhu F, Yang QL. Chemical composition and antioxidant activities of broussonetia papyrifera fruits. PLoS ONE, 2012, 7: 1-8.

[69] Thaiutsa B, Puangchit L (2001) Paper mulberry as an alternative crop of agroforestry systems in Thailand. Faculty of Forestry, Kasetsart University, Bangkok 10900, Thailand, Thailand

[70] Thaiutsa B, Puangchit L, Sommeechai M (2001) Effects of spacings on growth and yields of paper mulberry at different harvesting age. Faculty of Forestry, Kasetsart University, Bangkok 10900, Thailand, Thailand

[71] Thammasittirong SNR, Chatwachirawong P, Chamduang T, Thammasittirong A. Evaluation of ethanol production from sugar and lignocellulosic part of energy cane. Ind Crops Prod, 2017, 108: 598-603.

[72] Thangadurai D, Bhat S V., Sangeetha J, Mundaragi AC (2014) Production of Bioethanol from Muntingia calabura Fruits using Saccharomyces cervisiae and Schizosaccharomyces pombe. In: Proceedings of the International Symposium on Agriculture and Environment, University of Rahuna, Sri Lanka, 27 Nov 2014

[73] Tropea A, Wilson D, Cicero N, Potortì AG, La Torre GL, Dugo G, Richardson D, Waldron KW. Development of minimal fermentation media supplementation for ethanol production using two Saccharomyces cerevisiae strains. Nat Prod Res, 2016, 30: 1009-1016.

[74] UN-United Nations News (2020) Global perspectives Human stories. https://news.un.org/en/story/2020/09/1073052. Accessed 22 Sept 2021

[75] van Dyk JS, Li L, Barros D, Hu J, Zhang X, Tan T, Saddler J. The potential of biofuels in China. IEA Bioenergy, 2016, 39: 32.

[76] Vu T, LeBlanc J, Chou CC. Clarification of sugarcane juice by ultrafiltration membrane: Toward the direct production of refined cane sugar. J Food Eng, 2020, 264.

[77] Walker GM. Yeast physiology and biotechnology, 1998, Chichester: Wiley.

[78] Walker GM. Batt CA, Tortorello ML. Fermentation (Industrial): media for industrial fermentations. Encyclopedia of food microbiology, 2014, 2, Elsevier Ltd: Academic Press, 769-777.

[79] Walker GM, Basso TO. Mitigating stress in industrial yeasts. Fungal Biol, 2020, 124: 387-397.

[80] Walker GM, Walker RSK (2018) Enhancing yeast alcoholic fermentations. In: Advances in applied microbiology. Elsevier, pp 87–129

[81] Weinhandl K, Winkler M, Glieder A, Camattari A. Carbon source dependent promoters in yeasts. Microb Cell Factories, 2014, 13: 5.

[82] Xianjun P, Linhong T, Xiaoman W, Yucheng W, Shihua S. De Novo assembly of expressed transcripts and global transcriptomic analysis from seedlings of the paper mulberry (Broussonetia kazinoki x Broussonetia papyifera). PLoS ONE, 2014, 9.

[83] Yalley MK, Adusu D, Bunyamin A-R, Okyere I, Asare A. Natural regeneration of indigenous tree species in broussonetia papyrifera invaded sites in Pra -Anum Forest Reserve. Int J for Res, 2020, 2020.

[84] Yue M-Q, Wang Z, Dun B-Q, Han F-X, Li G-Y. Simplified methods of estimating fermentable sugar yield in sweet sorghum [Sorghum bicolor (L.) Moench] stems. Ind Crops Prod, 2021, 169: 113652.

[85] Zabed H, Faruq G, Sahu JN, Azirun MS, Hashim R, Nasrulhaq Boyce A. Bioethanol production from fermentable sugar juice. Sci World J, 2014

[86] Zhang A, Gao J, Quan J, Zhou B, Lam SK, Zhou Y, Lin E, Jiang K, Clarke LE, Zhang X, Yu S, Kyle GP, Li H, Zhou S, Gao S, Wang W, Guan Y. The implications for energy crops under China’s climate change challenges. Energy Econ, 2021, 96.

[87] Zhao XQ, Xue C, Ge XM, Yuan WJ, Wang JY, Bai FW. Impact of zinc supplementation on the improvement of ethanol tolerance and yield of self-flocculating yeast in continuous ethanol fermentation. J Biotechnol, 2009, 139: 55-60.

[88] Zicari S, Zhang R, Kaffka S (2019) Sugar beet. In: Integrated processing technologies for food and agricultural by-products. Elsevier, pp 331–351

Funding

National Key Research and Development Program of China(2020YFD1100704)