Abstract
Objectives
The aim of the present work was to perform the co-culture between Trichoderma longibrachiatum LMBC 172, a mesophilic fungus, with Thermothelomyces thermophilus LMBC 162, a thermophilic fungus, by submerged fermentation in a bioreactor.
Results
There was an increase in protein production, reaching the value of 35.60 ± 3.76 µg/ml at 72 h. An increase in the amount of proteins of 27.5% in relation to the isolated cultivation of T. longibrachiatum and 19.7% in comparison when T. thermophilus was isolated and cultivated. After that, the saccharification profile of three varieties of sugarcane (sugarcane in natura, culms of sugarcane SP80-3280, and culms of Energy cane) submitted in two pretreatments (autohydrolysis and chemical) was performed. The (e) chemical pretreatment was the better in generating of fermentable sugars from sugarcane bagasse and culms of Energy cane, while with the autohydrolysis pretreatment was obtained the better values to culms of SP80-3280 sugarcane. The sugars found were glucose, xylose, arabinose, and cellobiose.
Conclusion
These results suggest that the co-culture between these microorganisms has the potential to produce an enzymatic cocktail with high performance in the hydrolysis of materials from the sugar-alcohol industry.
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References
Aghbashlo M, Khounani Z, Hosseinzadeh-Bandbafha H, Gupta VK, Amiri H, Lam SS, Morosuk T, Tabatabaei M (2021) Exergoenvironmental analysis of bioenergy systems: a comprehensive review. Renew Sust Energ Rev 149:111399. https://doi.org/10.1016/j.rser.2021.111399
Al Arni S (2018) Extraction and isolation methods for lignin separation from sugarcane bagasse: a review. Ind Crops Prod 115:330–339. https://doi.org/10.1016/j.indcrop.2018.02.012
Aono AH, Pimenta RJG, Garcia ALB, Correr FH, Hosaka GK, Carrasco MM, Cardoso-Silva CB, Mancini MC, Sforça DA, dos Santos LB, Nagai JS, Pinto LR, Landell MGA, Carneiro MS, Balsalobre TW, Quiles MG, Pereira WA, Margarido GRA, de Souza AP (2021) The wild sugarcane and sorghum kinomes: insights into expansion, diversification, and expression patterns. Front Plant Sci. https://doi.org/10.3389/fpls.2021.668623
Balabanova L, Seitkalieva A, Yugay Y, Rusapetova T, Slepchenko L, Podvolotskaya A, Yatsunskaya M, Vasyutkina E, Son O, Tekutyeva L, Shkryl Y (2022) Engineered fungus Thermothelomyces thermophilus producing plant storage proteins. J Fungi 8:119. https://doi.org/10.3390/jof8020119
Bechara R, Gomez A, Saint-Antonin V, Schweitzer JM, Maréchal F, Ensinos A (2018) Review of design works for the conversion of sugarcane to first and second-generation ethanol and electricity. Renew Sust Energ Rev 91:152–164. https://doi.org/10.1016/j.rser.2018.02.020
Bordonal RDO, Carvalho JLN, Lal R, de Figueiredo EB, de Oliveira BG, La Scala JN (2018) Sustainability of sugarcane production in Brazil. Rev Agron Sustain Dev 38:1–23. https://doi.org/10.1007/s13593-018-0490-x
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Brinkman ML, da Cunha MP, Heijnen S, Wicke B, Guilhoto JJM, Walter A, Faiij APC, van der Hilst F (2018) Interregional assessment of socio-economic effects of sugarcane ethanol production in Brazil. Renew Sust Energ Rev 88:347–362. https://doi.org/10.1016/j.rser.2018.02.014
Brück SA, Contato AG, Gamboa-Trujillo P, Oliveira TB, Cereia M, Polizeli MLTM (2022) Prospection of psychrotrophic filamentous fungi isolated from the high andean paramo region of northern ecuador: enzymatic activity and molecular identification. Microorganisms 10:282. https://doi.org/10.3390/microorganisms10020282
Buckeridge MS, Grandis A, Tavares EQP (2019) Disassembling the glycomic code of sugarcane cell walls to improve second-generation bioethanol production. In: Ray R, Ramachandran R (eds) Bioethanol Production from Food Crops, 1st edn. Elsevier, Amsterdam
Cardoso TF, Watanabe MD, Souza A, Chagas MF, Cavalett O, Morais ER, Nogueira LAH, Leal LRV, Braunbeck OA, Cortez LAB, Bonomi A (2018) Economic, environmental, and social impacts of different sugarcane production systems. Biofuel Bioprod Biorefin 12:68–82. https://doi.org/10.1002/bbb.1829
Chan-Cupul W, Heredia-Abarca G, Rodríguez-Vázquez R (2016) Atrazine degradation by fungal co-culture enzyme extracts under different soil conditions. J Environ Sci Health B 51:298–308. https://doi.org/10.1080/03601234.2015.1128742
Chandel AK, Albarelli JQ, Santos DT, Chundawat SP, Puri M, Meireles MAA (2019) Comparative analysis of key technologies for cellulosic ethanol production from Brazilian sugarcane bagasse at a commercial scale. Biofuel Bioprod Biorefin 13:994–1014. https://doi.org/10.1002/bbb.1990
Chen J, Zhang B, Luo L, Zhang F, Yi Y, Shan Y, Liu B, Zhou Y, Wang X, Lü X (2021) A review on recycling techniques for bioethanol production from lignocellulosic biomass. Renew Sust Energ Rev 149:111370. https://doi.org/10.1016/j.rser.2021.111370
Chu R, Li S, Zhu L, Yin Z, Hu D, Liu C, Mo F (2021) A review on co-cultivation of microalgae with filamentous fungi: efficient harvesting, wastewater treatment and biofuel production. Renew Sust Energ Rev 139:110689. https://doi.org/10.1016/j.rser.2020.110689
Contato AG, de Oliveira TB, Aranha GM, de Freitas EN, Vici AC, Nogueira KMV, de Lucas RC, Scarcella ASA, Buckeridge MS, Silva RN, Polizeli MLTM (2021) Prospection of fungal lignocellulolytic enzymes produced from jatoba (Hymenaea courbaril) and tamarind (Tamarindus indica) seeds: Scaling for bioreactor and saccharification profile of sugarcane bagasse. Microorganisms 9:533. https://doi.org/10.3390/microorganisms9030533
Contato AG, Vici AC, Pinheiro VE, de Oliveira TB, de Freitas EN, Aranha GM, Valvassora Junior AL, Rechia CGV, Buckeridge MS, Polizeli MLTM (2022) Comparison of Trichoderma longibrachiatum xyloglucanase production using tamarind (Tamarindus indica) and jatoba (Hymenaea courbaril) seeds: Factorial design and immobilization on ionic supports. Fermentation 8:510. https://doi.org/10.3390/fermentation8100510
de Freitas EN, Salgado JCS, Alnoch RC, Contato AG, Habermann E, Michelin M, Martínez CA, Polizeli MLTM (2021) Challenges of biomass utilization for bioenergy in a climate change scenario. Biology 10:1277. https://doi.org/10.3390/biology10121277
de Freitas EN, Khatri V, Contin DR, Oliveira TB, Contato AG, Peralta RM, dos Santos WD, Martínez CA, Saddler JN, Polizeli MLTM (2022) Climate change affects cell-wall structure and hydrolytic performance of a perennial grass as an energy crop. Biofuels Bioprod Biorefining 16:471–487. https://doi.org/10.1002/bbb.2312
de Souza AP, Leite DCC, Pattathil S, Hahn MG, Buckeridge MS (2013) Composition and structure of sugarcane cell wall polysaccharides: implications for second generation bioethanol production. Bioenergy Res 6:564–579. https://doi.org/10.1007/s12155-012-9268-1
de Souza AP, Grandis A, Leite DCC, Buckeridge MS (2014) Sugarcane as a bioenergy source: history, performance, and perspectives for second-generation bioethanol. Bioenergy Res 7:24–35. https://doi.org/10.1007/s12155-013-9366-8
Demichelis F, Laghezza M, Chiappero M, Fiore S (2020) Technical, economic and environmental assessment of bioethanol biorefinery from waste biomass. J Clean Prod 277:124111. https://doi.org/10.1016/j.jclepro.2020.124111
Devi A, Bajar S, Kour H, Kothari R, Pant D, Singh A (2022) Lignocellulosic biomass valorization for bioethanol production: a circular bioeconomy approach. Bioenergy Res 2022:1–22. https://doi.org/10.1007/s12155-022-10401-9
Farinas CS, Marconcini JM, Mattoso LHC (2018) Enzymatic conversion of sugarcane lignocellulosic biomass as a platform for the production of ethanol, enzymes and nanocellulose. J Renew Mater 6:203–216. https://doi.org/10.7569/JRM.2017.6341578
Gonçalves GR, Gandolfi OR, Bonomo RCF, Fontan RDCI, Veloso CM (2021) Synthesis of activated carbon from hydrothermally carbonized tamarind seeds for lipase immobilization: characterization and application in aroma ester synthesis. J Chem Technol Biotechnol 96:3316–3329. https://doi.org/10.1002/jctb.6884
Grassi MCB, Pereira GAG (2019) Energy-cane and RenovaBio: Brazilian vectors to boost the development of Biofuels. Ind Crops Prod 129:201–205. https://doi.org/10.1016/j.indcrop.2018.12.006
Gutiérrez AS, Eras JJC, Huisingh D, Vandecasteele C, Hens L (2018) The current potential of low-carbon economy and biomass-based electricity in Cuba. The case of sugarcane, energy cane and marabu (Dichrostachys cinerea) as biomass sources. J Clean Prod 172:2108–2122. https://doi.org/10.1016/j.jclepro.2017.11.209
Hoarau J, Caro Y, Grondin I, Petit T (2018) Sugarcane vinasse processing: toward a status shift from waste to valuable resource. A Rev J Water Process Eng 24:11–25. https://doi.org/10.1016/j.jwpe.2018.05.003
Hoffstadt K, Pohen GD, Dicke MD, Paulsen S, Krafft S, Zang JA, da Fonseca-Zang WA, Leite A, Kuperjans I (2020) Challenges and prospects of biogas from energy cane as supplement to bioethanol production. Agronomy 10:821. https://doi.org/10.3390/agronomy10060821
Intasit R, Cheirsilp B, Suyotha W, Boonsawang P (2021) Synergistic production of highly active enzymatic cocktails from lignocellulosic palm wastes by sequential solid state-submerged fermentation and co-cultivation of different filamentous fungi. Biochem Eng J 173:108086. https://doi.org/10.1016/j.bej.2021.108086
Jiménez-Barrera D, Chan-Cupul W, Fan Z, Osuna-Castro JA (2018) Fungal co-culture increases ligninolytic enzyme activities: statistical optimization using response surface methodology. Prep Biochem Biotechnol 48:787–798. https://doi.org/10.1080/10826068.2018.1509084
Karp SG, Medina JD, Letti LAJ, Woiciechowski AL, de Carvalho JC, Schmitt CC, Penha RO, Kumlehn GS, Soccol CR (2021) Bioeconomy and biofuels: the case of sugarcane ethanol in Brazil. Biofuel Bioprod Biorefin 15:899–912. https://doi.org/10.1002/bbb.2195
Khanna P, Sundari SS, Kumar NJ (1995) Production, isolation, and partial purification of xylanases from an Aspergillus sp. World J Microbiol Biotechnol 11:242–243. https://doi.org/10.1007/BF00704661
Klein BC, Chagas MF, Junqueira TL, Rezende MCAF, Cardoso TF, Cavalett O, Bonomi A (2018) Techno-economic and environmental assessment of renewable jet fuel production in integrated Brazilian sugarcane biorefineries. Appl Energy 209:290–305. https://doi.org/10.1016/j.apenergy.2017.10.079
Kumar A, Kumar V, Singh B (2021) Cellulosic and hemicellulosic fractions of sugarcane bagasse: Potential, challenges and future perspective. Int J Biol Macromol 169:564–582. https://doi.org/10.1016/j.ijbiomac.2020.12.175
Li W, Zhao L, He X (2022) Degradation potential of different lignocellulosic residues by Trichoderma longibrachiatum and Trichoderma afroharzianum under solid state fermentation. Process Biochem 112:6–17. https://doi.org/10.1016/j.procbio.2021.11.011
Lima MS, Damasio ARL, Crnkovic PM, Pinto MR, Silva AM, Silva JC, Segato F, de Lucas RC, Jorge JA, Polizeli MLTM (2016) Co-cultivation of Aspergillus nidulans recombinant strains produce an enzymatic cocktail as an alternative to alkaline sugarcane bagasse pretreatment. Front Microbiol 7:583. https://doi.org/10.3389/fmicb.2016.00583
Manouchehrinejad M, Yue Y, de Morais RAL, Souza LMO, Singh H, Mani S (2018) Densification of thermally treated energy cane and napier grass. BioEnergy Res 11:538–550. https://doi.org/10.1007/s12155-018-9921-4
Michelin M, Teixeira JA (2016) Liquid hot water pretreatment of multi feedstocks and enzymatic hydrolysis of solids obtained thereof. Bioresour Technol 216:862–869. https://doi.org/10.1016/j.biortech.2016.06.018
Pasin TM, Almeida PZ, Scarcella ASA, Infante JC, Polizeli MLTM (2020) Bioconversion of agro-industrial residues to second-generation bioethanol. In: Nanda S, Vo DVN, Sarangi PK (eds) Biorefinery of Alternative Resources: Targeting Green Fuels and Platform Chemicals. Springer Nature, Berlin
Pereira LG, Cavalett O, Bonomi A, Zhang Y, Warner E, Chum HL (2019) Comparison of biofuel life-cycle GHG emissions assessment tools: The case studies of ethanol produced from sugarcane, corn, and wheat. Renew Sust Energ Rev 110:1–12. https://doi.org/10.1016/j.rser.2019.04.043
Ramesh T, Rajalaksmi N, Dhatathrevan KS (2015) Activated carbons derived from tamarind seeds for hydrogen storage. J Energy Storage 4:89–95. https://doi.org/10.1016/j.est.2015.09.005
Ravindra K, Singh T, Mor S (2019) Emissions of air pollutants from primary crop residue burning in India and their mitigation strategies for cleaner emissions. J Clean Prod 208:261–273. https://doi.org/10.1016/j.jclepro.2018.10.031
Reid WV, Ali MK, Field CB (2020) The future of bioenergy. Glob Chang Biol 26:274–286. https://doi.org/10.1111/gcb.14883
Reis PMCL, Dariva C, Vieira GAB, Hense H (2016) Extraction and evaluation of antioxidant potential of the extracts obtained from tamarind seeds (Tamarindus indica), sweet variety. J Food Eng 173:116–123. https://doi.org/10.1016/j.jfoodeng.2015.11.00
Samuels GJ, Ismaiel A, Mulaw TB, Szakacs G, Druzhinina IS, Kubicek CP, Jaklitsch WM (2012) The Longibrachiatum Clade of Trichoderma: a revision with new species. Fungal Divers 55:77–108. https://doi.org/10.1007/s13225-012-0152-2
Scarcella ASA, Pasin TM, de Oliveira TB, de Lucas RC, Ferreira-Nozawa MS, de Freitas EN, Vici AC, Buckeridge MS, Michelin M, Polizeli MLTM (2021) Saccharification of different sugarcane bagasse varieties by enzymatic cocktails produced by Mycothermus thermophilus and Trichoderma reesei RP698 cultures in agro-industrial residues. Energy 226:120360. https://doi.org/10.1016/j.energy.2021.120360
Scarcella ASA, Pasin TM, de Lucas RC, Ferreira-Nozawa MS, Oliveira TB, Contato AG, Grandis A, Buckeridge MS, Polizeli MLTM (2023) Holocellulase production by filamentous fungi: potential in the hydrolysis of energy cane and other sugarcane varieties. Biomass Convers Biorefin 13:1163–1174. https://doi.org/10.1007/s13399-021-01304-4
Song B, Buendia-Kandia F, Yu Y, Dufour A, Wu H (2019) Importance of lignin removal in enhancing biomass hydrolysis in hot-compressed water. Bioresour Technol 288:121522. https://doi.org/10.1016/j.biortech.2019.121522
Su T, Zhao D, Khodadadi M, Len C (2020) Lignocellulosic biomass for bioethanol: Recent advances, technology trends, and barriers to industrial development. Curr Opin Green Sustain Chem 24:56–60. https://doi.org/10.1016/j.cogsc.2020.04.005
Sydney EB, de Carvalho JC, Letti LAJ, Magalhães AI Jr, Karp SG, Martinez-Burgos WJ, Candeo ES, Rodrigues C, Vandenberghe LPS, Dalmas Neto CJ, Torres LAZ, Medeiros ABP, Woiciechowski AL, Soccol CR (2021) Current developments and challenges of green technologies for the valorization of liquid, solid, and gaseous wastes from sugarcane ethanol production. J Hazard Mater 404:124059. https://doi.org/10.1016/j.jhazmat.2020.124059
UNICA. Position on 03/16/2023 [Internet]. Biweekly evaluation of the 2022/2023 crop in the center-south region. 2023 [Accessed 6 Apr. 2023]. Available at: http://www.unica.com.br/
Wang C, Yang J, Wen J, Bian J, Li M, Peng F, Sun R (2019) Structure, and distribution changes of Eucalyptus hemicelluloses during hydrothermal and alkaline pretreatments. Int J Biol Macromol 133:514–521. https://doi.org/10.1016/j.ijbiomac.2019.04.127
Yadav M, Paritosh K, Pareek N, Vivekanand V (2019) Coupled treatment of lignocellulosic agricultural residues for augmented biomethanation. J Clean Prod 213:75–88. https://doi.org/10.1016/j.jclepro.2018.12.142
Acknowledgements
We thank Mariana Cereia and Mauricio de Oliveira for technical assistance.
Funding
The authors thank Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for the doctorate grants awarded to A.G. Contato (Processes nº 2017/25862-6 and 2021/07066-3), and for the post-doctorate grant awarded to K.M.V. Nogueira (Process nº 2018/25898-3); and financial support from National Institute of Science and Technology of Bioethanol (Process FAPESP 2014/50884-5), and Process FAPESP 2018/07522-6. Conselho Nacional de Desenvolvimento Científico (CNPq), processes 465319/2014-9. M.L.T.M. Polizeli (Process 310340/2021-7), M.S. Buckeridge, and R.N. Silva are Research Fellows of CNPq.
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AGC: Methodology, Investigation, Data Curation, Formal Analysis, Writing—original draft. KMVN: Methodology, Data Curation, Formal Analysis. MSB: Funding acquisition, Conceptualization. RNS: Methodology, Data Curation, Formal Analysis. MLTMP: Funding acquisition, Conceptualization, Supervision, Writing-review & editing.
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Contato, A.G., Nogueira, K.M.V., Buckeridge, M.S. et al. Trichoderma longibrachiatum and thermothelomyces thermophilus co-culture: improvement the saccharification profile of different sugarcane bagasse varieties. Biotechnol Lett 45, 1093–1102 (2023). https://doi.org/10.1007/s10529-023-03395-7
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DOI: https://doi.org/10.1007/s10529-023-03395-7