Abstract
Background: Xylitol, a five-carbon polyalcohol, is used in the food and pharmaceutical industries and as a building block in the synthesis of high-value chemicals. It can be sustainably produced from renewable sources through xylose assimilating microbe fermentation.
Results: We screened microbial strains for xylitol production and identified Wickerhamomyces anomalus Z1 as a key xylitol producer. Utilizing lignocellulosic biomass hydrolysates for xylitol production poses challenges due to microbial sensitivity to inhibitors from biomass pre-treatment. In this study, an adaptive laboratory evolution (ALE) of W. anomalus Z1 was performed by culturing the yeast in a mineral medium supplemented with gradual increases of sugarcane bagasse hemicellulosic hydrolysate (SCHH) obtained by intensified steam explosion pretreatment. The performance of the adapted yeast, named Wickerhamomyces anomalus ALE, was assessed in comparison to the wild-type strain regarding its capacity to produce xylitol using SCHH. The evolved yeast reached a xylitol yield of 0.11 g xylitol/g xylose whereas the wild-type strain could not produce xylitol. Removing acetic acid from SCHH enhanced W. anomalus ALE performance, with optimal results at 75% hydrolyzed hemicellulose, yielding 0.44 g xylitol/g xylose and 13.41 g/L xylitol.
Conclusions: This study demonstrates the potential of W. anomalus ALE in successfully valorizing the hemicellulosic fraction of sugarcane bagasse for sustainable xylitol production.
References
Prabhu, A.A.; Bosakornranut, E.; Amraoui, Y.; et al. Enhanced xylitol production using non-detoxified xylose rich pre-hydrolysate from sugarcane bagasse by newly isolated Pichia fermentans. Biotechnol Biofuels 2020;13:209. https://doi.org/10.1186/s13068-020-01845-2 PMid: 33375948
de Albuquerque, T.L.; Gomes, S.D.L.; Marques, J.E.; et al. Xylitol production from cashew apple bagasse by Kluyveromyces marxianus CCA510. Catal Today 2015;255:33–40. https://doi.org/10.1016/j.cattod.2014.10.054
Morais Junior, W.G.; Pacheco, T.F.; Trichez, D.; et al. Xylitol production on sugarcane biomass hydrolysate by newly identified Candida tropicalis JA2 strain. Yeast 2019;36(5):349–361. ttps://doi.org/10.1002/yea.3394 PMid: 30997699
Khatri, P.; Pandit, A.B. Systematic review of life cycle assessments applied to sugarcane bagasse utilization alternatives. Biomass Bioenergy 2022;158:106365. https://doi.org/10.1016/j.biombioe.2022.106365
Nasution, M.H.; Lelinasari, S.; Kelana, M.G.S. A review of sugarcane bagasse pretreatment for bioethanol production. IOP Conference Series: Earth and Environmental Science 2022;963:012014. https://doi.org/10.1088/1755-1315/963/1/012014
Agwa, I.S.; Zeyad, A.M.; Tayeh, B.A.; et al. A comprehensive review on the use of sugarcane bagasse ash as a supplementary cementitious material to produce eco-friendly concretes. Mater Today Proc 2022;65:688–696. https://doi.org/10.1016/j.matpr.2022.03.264
Rehman, S.; Murtaza, M.A.; Mushtaq, Z. Xylitol as sweetener. In: Merillon, JM., Ramawat, K., editors. Sweeteners. Reference Series in Phytochemistry; Springer, Cham, 2016; pp. 1–21. https://doi.org/10.1007/978-3-319-26478-3_30-1
Hernández-Pérez, A.F.; de Arruda, P.V.; Sene, L.; et al. Xylitol bioproduction: State-of-the-art, industrial paradigm shift, and opportunities for integrated biorefineries. Crit Rev Biotechnol 2019;39(7):924–943. https://doi.org/10.1080/07388551.2019.1640658 PMid: 31311338
Tiefenbacher, K.F. Technology of main ingredients—Sweeteners and lipids. In: Wafer and Waffle; Academic Press, Elsevier, 2017; pp. 123–225. https://doi.org/10.1016/B978-0-12-809438-9.00003-X
Da Silva, S.S.; Chandel, A.K. D-Xylitol: Fermentative Production, Application and Commercialization; Springer-Verlag Berlin Heidelberg, 2012; 348 p. ISBN 9783642318870. https://doi.org/10.1007/978-3-642-31887-0
Mäkinen, K.K. Sugar alcohol sweeteners as alternatives to sugar with special consideration of xylitol. Medical Principles and Practice 2011;20(4):303–320. https://doi.org/10.1159/000324534 PMid: 21576989
Ahuja, V.; Macho, M.; Ewe, D.; et al. Biological and pharmacological potential of xylitol: A molecular insight of unique metabolism. Foods 2020;9(11):1592. https://doi.org/10.3390/foods9111592 PMid: 33147854
Queiroz, S.S.; Jofre, F.M.; Mussatto, S.I.; et al. Scaling up xylitol bioproduction: Challenges to achieve a profitable bioprocess. Renewable and Sustainable Energy Reviews 2022;154:111789. https://doi.org/10.1016/j.rser.2021.111789
Kaur, S.; Guleria, P.; Yadav, S.K. Evaluation of fermentative xylitol production potential of adapted strains of Meyerozyma caribbica and Candida tropicalis from rice straw hemicellulosic hydrolysate. Fermentation 2023;9(2):181. https://doi.org/10.3390/fermentation9020181
Werpy, T.; Petersen, G. Top value added chemicals from biomass volume i-results of screening for potential candidates from sugars and synthesis gas; U.S. Technical Report, Department of Energy Office of Scientific and Technical Information 2004:15008859. https://doi.org/10.2172/15008859 PMid: 15054238
Sooch, B.S.; Lugani, Y. Role of microbes in the synthesis of industrial products from lignocellulosic materials. In: Singh, N.K., Chattopadhyay, A., Lichtfouse, E., editors; Sustainable Agriculture Reviews 60: Microbial Processes in Agriculture; Springer Nature Switzerland: Cham, 2023;60:415–458. https://doi.org/10.1007/978-3-031-24181-9_16
Dasgupta, D.; Bandhu, S.; Adhikari, D.K.; et al. Challenges and prospects of xylitol production with whole cell bio-catalysis: A review. Microbiol Res 2017;197:9–21, https://doi.org/10.1016/j.micres.2016.12.012 PMid: 28219529
Goli, J.K.; Hameeda, B. Production of xylitol and ethanol from acid and enzymatic hydrolysates of Typha latifolia by Candida tropicalis JFH5 and Saccharomyces cerevisiae VS3. Biomass Convers Biorefin 2023;13:9741-9751. https://doi.org/10.1007/s13399-021-01868-1
Umai, D.; Kayalvizhi, R.; Kumar, V.; et al. Xylitol: Bioproduction and applications-A review. Frontiers in Sustainability 2022;3:826190. https://doi.org/10.3389/frsus.2022.826190
Jeffries T. Utilization of xylose by bacteria, yeasts, and fungi. In: Fiechter A, Jeffries T, editors. Pentoses and Lienin. Berlin, Boston: De Gruyter; 1983. p. 1-32. https://doi.org/10.1515/9783112620809-002 PMid: 6437152
Sampaio, F.C.; Silveira WB da; Chaves-Alves, V.M.; et al. Screening of filamentous fungi for production of xylitol from D-xylose. Brazilian Journal of Microbiology 2003;34(4):325–328. https://doi.org/10.1590/S1517-83822003000400007
Lugani, Y.; Sooch, B.S. Fermentative production of xylitol from a newly isolated xylose reductase producing Pseudomonas putida BSX-46. LWT 2020;134:109988. https://doi.org/10.1016/j.lwt.2020.109988
Antunes, F.A.F.; dos Santos, J.C.; da Cunha, M.A.A.; et al. Biotechnological production of xylitol from biomass. In: Fang, Z., Smith, Jr., R., Qi, X. editors. Production of platform chemicals from sustainable resources. Biofuels and Biorefineries, Springer: Singapore, 2017; pp. 311–342. https://doi.org/10.1007/978-981-10-4172-3_10
Bonfiglio, F.; Cagno, M.; Yamakawa, C.K.; et al. Production of xylitol and carotenoids from switchgrass and Eucalyptus globulus hydrolysates obtained by intensified steam explosion pretreatment. Ind Crops Prod 2021;170:113800. https://doi.org/10.1016/j.indcrop.2021.113800
Bonfiglio, F.; Cagno, M.; Rey, F.; et al. Pretreatment of switchgrass by steam explosion in a semi-continuous pre-pilot reactor. Biomass Bioenergy 2019;121:41-47. https://doi.org/10.1016/j.biombioe.2018.12.013
Wang, X.; Khushk, I.; Xiao, Y.; et al. Tolerance improvement of Corynebacterium glutamicum on lignocellulose derived inhibitors by adaptive evolution. Appl Microbiol Biotechnol 2018;102:377–388. https://doi.org/10.1007/s00253-017-8627-4 PMid: 29151160
Portnoy, V.A.; Bezdan, D.; Zengler, K. Adaptive laboratory evolution-harnessing the power of biology for metabolic engineering. Curr Opin Biotechnol 2011;22(4):590–594. https://doi.org/10.1016/j.copbio.2011.03.007 PMid: 21497080
Jönsson, L.J.; Martín, C. Pretreatment of lignocellulose: Formation of inhibitory by-products and strategies for minimizing their effects. Bioresour Technol 2016;199:103–112. https://doi.org/10.1016/j.biortech.2015.10.009 PMid: 26482946
Sarkar, P.; Mukherjee, M.; Goswami, G.; et al. Adaptive laboratory evolution induced novel mutations in Zymomonas mobilis ATCC ZW658: A potential platform for co-utilization of glucose and xylose. J Ind Microbiol Biotechnol 2020;47(3):329–341. https://doi.org/10.1007/s10295-020-02270-y PMid: 32152759
Rodriguez, P.; Magallanes-Noguera, C.; Menéndez, P.; et al. A study of Raphanus sativus and its endophytes as carbonyl group bioreducing agents. Biocatal Biotransformation 2015;33(2): 121–129. https://doi.org/10.3109/10242422.2015.1053471
Marconi, F.; Umpiérrez, M.L.; Gonzalez, D.; et al. Endophytic Biocatalysts with enoate reductase activity isolated from Mentha pulegium. World J Microbiol Biotechnol 2018;34:50. https://doi.org/10.1007/s11274-018-2434-7 PMid: 29550961
Botto, E.; Gioia, L.; Menéndez, M.P.; et al. Pseudozyma sp. isolation from eucalyptus leaves and its hydrolytic activity over xylan. Biocatal Agric Biotechnol 2019;21:101282. https://doi.org/10.1016/j.bcab.2019.101282
Rodríguez, P.; Sierra, W.; Rodríguez, S.; et al. Biotransformation of 1,8-cineole, the Main Product of Eucalyptus Oils. Electronic Journal of Biotechnology 2006;9:232–236. https://doi.org/10.2225/vol9-issue3-fulltext-28
Giorgi, V.; Chaves, M.; Menendez, P.; et al. Bioprospecting of whole-cell biocatalysts for cholesterol biotransformation. World J Microbiol Biotechnol, 2019;35:12. https://doi.org/10.1007/s11274-018-2586-5 PMid: 30604276
Rodríguez, P.; Reyes, B.; Barton, M.; et al. Stereoselective biotransformation of ?-alkyl-?-keto esters by endophytic bacteria and yeast. J Mol Catal B Enzym 2011;71(3-4):90–94. https://doi.org/10.1016/j.molcatb.2011.04.003
Rodriguez, P.; Gonzalez, D.; Rodríguez Giordano, S. Endophytic microorganisms: A source of potentially useful biocatalysts. J Mol Catal B Enzym 2016;133(S1):S569–S581. https://doi.org/10.1016/j.molcatb.2017.02.013
Ballesteros, L.F.; Teixeira, J.A.; Mussatto, S.I. Selection of the solvent and extraction conditions for maximum recovery of antioxidant phenolic compounds from coffee silverskin. Food Bioproc Tech 2014;7:1322–1332. https://doi.org/10.1007/s11947-013-1115-7
Domingues, R.; Bondar, M.; Palolo, I.; et al. Xylose metabolism in bacteria—opportunities and challenges towards efficient lignocellulosic biomass?based biorefineries. Applied Sciences 2021;11(17):8112. https://doi.org/10.3390/app11178112
Ahuja, V., Bhatt, A.K., Mehta, S. et al. Xylitol production by Pseudomonas gessardii VXlt-16 from sugarcane bagasse hydrolysate and cost analysis. Bioprocess Biosyst Eng 2022;45:1019–1031. https://doi.org/10.1007/s00449-022-02721-z
Espinoza-Acosta, J.L. Biotechnological production of xylitol from agricultural waste. Biotecnia 2020;22(1):126–134. https://doi.org/10.18633/biotecnia.v22i1.1160
Carneiro, C.V.G.C.; Silva, F.C. de P.; Almeida, J.R.M. Xylitol production: Identification and comparison of new producing yeasts. Microorganisms 2019;7(11):484. https://doi.org/10.3390/microorganisms7110484 PMid: 31652879
Kurtzman, C.P. Wickerhamomyces Kurtzman, Robnett & Basehoar-Powers (2008). In: Kurtzman, CP, Fell JW, Boekhout T, editors. The Yeasts; Elsevier, 2011;2:899–917. https://doi.org/10.1016/B978-0-444-52149-1.00080-X
Sehnem, N.T.; Hickert, L.R.; da Cunha-Pereira, F.; et al. Bioconversion of soybean and rice hull hydrolysates into ethanol and xylitol by furaldehyde-tolerant strains of Saccharomyces cerevisiae, Wickerhamomyces anomalus, and their cofermentations. Biomass Convers Biorefin 2017;7:199–206. https://doi.org/10.1007/s13399-016-0224-8
Walker, G.M. Pichia anomala: Cell physiology and biotechnology relative to other yeasts. Antonie van Leeuwenhoek 2011;99:25–34. https://doi.org/10.1007/s10482-010-9491-8 PMid: 20706871
Sundh, I.; Melin, P. Safety and regulation of yeasts used for biocontrol or biopreservation in the food or feed chain. Antonie van Leeuwenhoek 2011;99:113–119. https://doi.org/10.1007/s10482-010-9528-z PMid: 21086043
Cheng, K.K.; Cai, B.Y.; Zhang, J.A.; et al. Sugarcane bagasse hemicellulose hydrolysate for ethanol production by acid recovery process. Biochem Eng J 2008;38:105–109, https://doi.org/10.1016/j.bej.2007.07.012
do Espírito Santo, M.C.; Cardoso, E.B.; Guimaraes, F.E.G.; et al. Multifaceted characterization of sugarcane bagasse under different steam explosion severity conditions leading to distinct enzymatic hydrolysis yields. Ind Crops Prod 2019;139:111542. https://doi.org/10.1016/j.indcrop.2019.111542
Carvalho, A.F.A.; Marcondes, W.F.; de Oliva Neto, P.; et al. The potential of tailoring the conditions of steam explosion to produce xylo-oligosaccharides from sugarcane bagasse. Bioresour Technol 2018;250:221–229, https://doi.org/10.1016/j.biortech.2017.11.041 PMid: 29174899
Zhang, L.; Peng, W.; Wang, F.; et al. Fractionation and quantitative structural analysis of lignin from a lignocellulosic biorefinery process by gradient acid precipitation. Fuel 2022;309:122153. https://doi.org/10.1016/j.fuel.2021.122153
Morales, P.; Gentina, J.C.; Aroca, G.; et al. Development of an acetic acid tolerant Spathaspora passalidarum strain through evolutionary engineering with resistance to inhibitors compounds of autohydrolysate of Eucalyptus globulus. Ind Crops Prod 2017;106:5–11. https://doi.org/10.1016/j.indcrop.2016.12.023
Vajzovic, A.; Bura, R.; Kohlmeier, K.; et al. Novel endophytic yeast Rhodotorula mucilaginosa strain PTD3 II: Production of xylitol and ethanol in the presence of inhibitors. J Ind Microbiol Biotechnol 2012;39(10):1453–1463. https://doi.org/10.1007/s10295-012-1154-5 PMid: 22711018
Bellido, C.; Bolado, S.; Coca, M.; et al. Effect of inhibitors formed during wheat straw pretreatment on ethanol fermentation by Pichia stipitis. Bioresour Technol 2011;102(23):10868–10874. https://doi.org/10.1016/j.biortech.2011.08.128 PMid: 21983414
Björling, T.; Lindman, B. Evaluation of xylose-fermenting yeasts for ethanol production from spent sulfite liquor. Enzyme Microb Technol 1989;11(4):240–246. https://doi.org/10.1016/0141-0229(89)90099-9
Bonatto, C.; Venturin, B.; Mayer, D.A.; et al. Experimental data and modelling of 2G ethanol production by Wickerhamomyces sp. UFFS-CE-3.1.2. Renew Energy 2020;145:2445–2450. https://doi.org/10.1016/j.renene.2019.08.010
Casey, E.; Sedlak, M.; Ho, N.W.Y.; et al. Effect of acetic acid and pH on the cofermentation of glucose and xylose to ethanol by a genetically engineered strain of Saccharomyces cerevisiae. FEMS Yeast Res 2010;10(4):385–393. https://doi.org/10.1111/j.1567-1364.2010.00623.x PMid: 20402796
Biazi, L.E.; Santos, S.C.; Kaupert Neto, A.A.; et al. Adaptation strategy to increase the tolerance of Scheffersomyces stipitis NRRL Y-7124 to inhibitors of sugarcane bagasse hemicellulosic hydrolysate through comparative studies of proteomics and fermentation. Bioenergy Res 2022;15:479–492, https://doi.org/10.1007/s12155-021-10267-3
Martín, C.; Marcet, M.; Almazán, O.; et al. Adaptation of a recombinant xylose-utilizing Saccharomyces cerevisiae strain to a sugarcane bagasse hydrolysate with high content of fermentation inhibitors. Bioresour Technol 2007;98(7):1767–1773. https://doi.org/10.1016/j.biortech.2006.07.021 PMid: 1693445
Mussatto, S.I.; Roberto, I.C. Establishment of the optimum initial xylose concentration and nutritional supplementation of brewer’s spent grain hydrolysate for xylitol production by Candida guilliermondii. Process Biochemistry 2008;43(5):540–546. https://doi.org/10.1016/j.procbio.2008.01.013
Giovati, L.; Ciociola, T.; Simone, T.; et al. Wickerhamomyces yeast killer toxins’ medical applications. Toxins 2021;13(9):655. https://doi.org/10.3390/toxins13090655 PMid: 34564659
Padilla, B.; Gil, J.V.; Manzanares, P. Challenges of the non-conventional yeast Wickerhamomyces anomalus in winemaking. Fermentation 2018;4(3):68. https://doi.org/10.3390/fermentation4030068
Zhou, N.; Semumu, T.; Gamero, A. Non-conventional yeasts as alternatives in modern baking for improved performance and aroma enhancement. Fermentation 2021;7(3):102. https://doi.org/10.3390/fermentation7030102
Passoth, V.; Olstorpe, M.; Schnürer, J. Past, present and future research directions with Pichia anomala. Antonie van Leeuwenhoek 2011;99:121–125. https://doi.org/10.1007/s10482-010-9508-3 PMid: 20924674
Sehnem, N.T.; Machado, Â.S.; Matte, C.R.; et al. Second-generation ethanol production by Wickerhamomyces anomalus strain adapted to furfural, 5-hydroxymethylfurfural (HMF), and high osmotic pressure. An Acad Bras Cienc 2020;92(S2):e20181030. https://doi.org/10.1590/0001-3765202020181030 PMid: 33084752
Prakash, G.; Varma, A.J.; Prabhune, A.; et al. Microbial production of xylitol from D-xylose and sugarcane bagasse hemicellulose using newly isolated thermotolerant yeast Debaryomyces hansenii. Bioresour Technol 2011;102(3):3304–3308. https://doi.org/10.1016/j.biortech.2010.10.074 PMid: 21067918
Raj, K.; Krishnan, C. Improved co-production of ethanol and xylitol from low-temperature aqueous ammonia pretreated sugarcane bagasse using two-stage high solids enzymatic hydrolysis and Candida tropicalis. Renew Energy 2020;153:392–403, https://doi.org/10.1016/j.renene.2020.02.042
Vaz de Arruda, P.; dos Santos, J.C.; Rodrigues, RLB; et al. Scale up of xylitol production from sugarcane bagasse hemicellulosic hydrolysate by Candida guilliermondii FTI 20037. Journal of Industrial and Engineering Chemistry 2017;47:297–302. https://doi.org/10.1016/j.jiec.2016.11.046
Vallejos, M.E.; Chade, M.; Mereles, E.B.; et al. Strategies of detoxification and fermentation for biotechnological production of xylitol from sugarcane bagasse. Ind Crops Prod 2016;91:161–169. https://doi.org/10.1016/j.indcrop.2016.07.007
Rodrigues, R.C.L.B.; Felipe, M.G.A.; Roberto, I.C.; et al. Batch xylitol production by Candida guilliermondii FTI 20037 from sugarcane bagasse hemicellulosic hydrolyzate at controlled pH values. Bioprocess Biosyst Eng 2003;26:103–107. https://doi.org/10.1007/s00449-003-0332-2 PMid: 14624353
Palladino, F.; Rodrigues, R.C.L.B.; da Silva, S.P.; et al. Strategy to reduce acetic acid in sugarcane bagasse hemicellulose hydrolysate concomitantly with xylitol production by the promising yeast Cyberlindnera xylosilytica in a bioreactor. Biotechnol Lett 2023;45:263–272, https://doi.org/10.1007/s10529-022-03337-9 PMid: 36586052

This work is licensed under a Creative Commons Attribution-ShareAlike 4.0 International License.
Copyright (c) 2024 Electronic Journal of Biotechnology
