Abstract
The coproduction of polymalic acid (PMA) and liamocins, two important metabolites secreted by Aureobasidium pullulans, from two waste by-products from the xylitol and gluconate industries was investigated in shake flasks and fermentors, confirming that waste xylose mother liquor (WXML) could be utilized as an economical feedstock without any pretreatment. Gluconate could strengthen carbon flux and NADPH supply for the synergetic biosynthesis of PMA and liamocins. High PMA and liamocin titers of 82.9 ± 2.1 and 28.3 ± 2.7 g/L, respectively, were obtained from the coupled WXML and waste gluconate mother liquor (WGML) in batch fermentation, with yields of 0.84 and 0.25 g/g, respectively. These results are comparable to those obtained from renewable feedstocks. Economic assessment of the process revealed that PMA and liamocins could be coproduced from two by-products at costs of $1.48/kg or $0.67/kg (with liamocins credit), offering an economic and sustainable process for the application of waste by-products.
Similar content being viewed by others
References
Slepecky RA, Starmer WT (2009) Phenotypic plasticity in fungi: a review with observations on Aureobasidium pullulans. Mycologia 101(6):823–832. https://doi.org/10.3852/08-197
Prasongsuk S, Lotrakul P, Ali I, Bankeeree W, Punnapayak H (2018) The current status of Aureobasidium pullulans in biotechnology. Folia Microbiol 63(2):129–140. https://doi.org/10.1007/s12223-017-0561-4
Chi Z, Liu G-L, Liu C-G, Chi Z-M (2016) Poly(beta-L-malic acid) (PMLA) from Aureobasidium spp. and its current proceedings. Appl Microbiol Biotechnol 100(9):3841–3851. https://doi.org/10.1007/s00253-016-7404-0
Zou X, Cheng C, Feng J, Song X, Lin M, Yang S-T (2019) Biosynthesis of polymalic acid in fermentation: advances and prospects for industrial application. Crit Rev Biotechnol 39(3):408–421. https://doi.org/10.1080/07388551.2019.1571008
Qiao Y, Wang C, Liu B, Peng Y, Meng H, Yang T, Zhou Q, Guo S, Wu H (2019) Enhanced endocytic and pH-sensitive poly(malic acid) micelles for antitumor drug delivery. J Biomed Nanotechnol 15:28–41. https://doi.org/10.1166/jbn.2019.2673
Israel LL, Braubach O, Galstyan A, Chiechi A, Shatalova ES, Grodzinski Z, Ding H, Black KL, Ljubimova JY, Holler E (2019) A combination of tri-leucine and angiopep-2 drives a polyanionic polymalic acid nanodrug platform across the blood-brain barrier. ACS Nano 13:1253–1271. https://doi.org/10.1021/acsnano.8b06437
Zou X, Zhou Y, Yang S-T (2013) Production of polymalic acid and malic acid by Aureobasidium pullulans fermentation and acid hydrolysis. Biotechnol Bioeng 110(8):2105–2113. https://doi.org/10.1002/bit.24876
Price NPJ, Manitchotpisit P, Vermillion KE, Bowman MJ, Leathers TD (2013) Structural characterization of novel extracellular liamocins (mannitol oils) produced by Aureobasidium pullulans strain NRRL 50380. Carbohydr Res 370:24–32. https://doi.org/10.1016/j.carres.2013.01.014
Leathers TD, Price NPJ, Bischoff KM, Manitchotpisit P, Skory CD (2015) Production of novel types of antibacterial liamocins by diverse strains of Aureobasidium pullulans grown on different culture media. Biotechnol Lett 37(10):2075–2081. https://doi.org/10.1007/s10529-015-1892-3
Kim J-S, Lee I-K, Yun B-S (2018) Pullusurfactans A-E, new biosurfactants produced by Aureobasidium pullulans A11211–4–57 from a fleabane, Erigeron annus (L.) pers. J Antibiot 71(11):920–926. https://doi.org/10.1038/s41429-018-0089-0
Manitchotpisit P, Watanapoksin R, Price NPJ, Bischoff KM, Tayeh M, Teeraworawit S et al (2014) Aureobasidium pullulans as a source of liamocins (heavy oils) with anticancer activity. World J Microbiol Biotechnol 30(8):2199–2204. https://doi.org/10.1007/s11274-014-1639-7
Bischoff KM, Brockmeier SL, Skory CD, Leathers TD, Price NPJ, Manitchotpisit P et al (2018) Susceptibility of Streptococcus suis to liamocins from Aureobasidium pullulans. Biocatal Agric Biotechnol 15:291–294. https://doi.org/10.1016/j.bcab.2018.06.025
Bischoff KM, Leathers TD, Price NPJ, Manitchotpisit P (2015) Liamocin oil from Aureobasidium pullulans has antibacterial activity with specificity for species of Streptococcus. J Antibiot 68(10):642–645. https://doi.org/10.1038/ja.2015.39
Leathers TD, Price NPJ, Manitchotpisit P, Bischoff KM (2016) Production of anti-streptococcal liamocins from agricultural biomass by Aureobasidium pullulans. World J Microbiol Biotechnol 32(12):199. https://doi.org/10.1007/s11274-016-2158-5
Zan Z, Zou X (2013) Efficient production of polymalic acid from raw sweet potato hydrolysate with immobilized cells of Aureobasidium pullulans CCTCC M2012223 in aerobic fibrous bed bioreactor. J Chem Technol Biotechnol 88(10):1822–1827. https://doi.org/10.1002/jctb.4033
Cheng C, Zhou Y, Lin M, Wei P, Yang S-T (2017) Polymalic acid fermentation by Aureobasidium pullulans for malic acid production from soybean hull and soy molasses: Fermentation kinetics and economic analysis. Bioresour Technol 223:166–174. https://doi.org/10.1016/j.biortech.2016.10.042
Wei P, Cheng C, Lin M, Zhou Y, Yang S-T (2017) Production of poly(malic acid) from sugarcane juice in fermentation by Aureobasidium pullulans: Kinetics and process economics. Bioresour Technol 224:581–589. https://doi.org/10.1016/j.biortech.2016.11.003
Zou X, Wang Y, Tu G, Zan Z, Wu X (2015) Adaptation and transcriptome analysis of Aureobasidium pullulans in corncob hydrolysate for increased inhibitor tolerance to malic acid production. PLoS ONE 10(3):e0121416. https://doi.org/10.1371/journal.pone.0121416
Feng J, Li T, Zhang X, Chen J, Zhao T, Zou X (2019) Efficient production of polymalic acid from xylose mother liquor, an environmental waste from the xylitol industry, by a T-DNA-based mutant of Aureobasidium pullulans. Appl Microbiol Biotechnol 103(16):6519–6527. https://doi.org/10.1007/s00253-019-09974-x
Wang HH, Pan JC, Wang J, Wang N, Zhang J, Li Q et al (2014) Succinic acid production from xylose mother liquor by recombinant Escherichia coli strain. Biotechnol Biotechnol Equip 28(6):1042–1049. https://doi.org/10.1080/13102818.2014.952501
Liu XL, Lin LJ, Xu XY, Zhang H, Wu LT, Zhu P et al (2018) Two-step economical welan gum production by Sphingomonas sp. HT-1 from sugar industrial by-products. Carbohydr Polym 181:412–418. https://doi.org/10.1016/j.carbpol.2017.09.033
Garay LA, Sitepu IR, Cajka T, Xu J, Teh HE, German JB et al (2018) Extracellular fungal polyol lipids: A new class of potential high value lipids. Biotechnol Adv 36(2):397–414. https://doi.org/10.1016/j.biotechadv.2018.01.003
Li HQ, Li TF, Zuo H, Xiao SY, Guo MJ, Jiang M et al (2016) A novel rhodamine-based fluorescent pH probe for high-throughput screening of high-yield polymalic acid strains from random mutant libraries. RSC Adv 6(97):94756–94762. https://doi.org/10.1039/c6ra20394a
Liu YY, Chi Z, Wang ZP, Liu GL, Chi ZM (2014) Heavy oils, principally long-chain n-alkanes secreted by Aureobasidium pullulans var. melanogenum strain P5 isolated from mangrove system. J Ind Microbiol Biotechnol 41(9):1329–1337. https://doi.org/10.1007/s10295-014-1484-6
Ichihara K, Fukubayashi Y (2010) Preparation of fatty acid methyl esters for gas-liquid chromatography. J Lipid Res 51(3):635–640. https://doi.org/10.1194/jlr.D001065
Tang RR, Chi Z, Jiang H, Liu GL, Xue SJ, Hu Z et al (2018) Overexpression of a pyruvate carboxylase gene enhances extracellular liamocin and intracellular lipid biosynthesis by Aureobasidium melanogenum M39. Process Biochem 69:64–74. https://doi.org/10.1016/j.procbio.2018.03.008
Wang Y, Song X, Zhang Y, Wang B, Zou X (2016) Effects of nitrogen availability on polymalic acid biosynthesis in the yeast-like fungus Aureobasidium pullulans. Microb Cell Fact 15(1):146. https://doi.org/10.1186/s12934-016-0547-y
Yang J, Yang W, Feng J, Chen J, Jiang M, Zou X (2018) Enhanced polymalic acid production from the glyoxylate shunt pathway under exogenous alcohol stress. J Biotechnol 275:24–30. https://doi.org/10.1016/j.jbiotec.2018.04.001
Feng J, Yang J, Yang W, Chen J, Jiang M, Zou X (2018) Metabolome- and genome-scale model analyses for engineering of Aureobasidium pullulans to enhance polymalic acid and malic acid production from sugarcane molasses. Biotechnol Biofuels 11:94. https://doi.org/10.1186/s13068-018-1099-7
Luepongpattana S, Thaniyavarn J, Morikawa M (2017) Production of massoia lactone by Aureobasidium pullulans YTP6-14 isolated from the Gulf of Thailand and its fragrant biosurfactant properties. J Appl Microbiol 123(6):1488–1497. https://doi.org/10.1111/jam.13598
Sun XM, Ren LJ, Zhao QY, Ji XJ (1864) Huang H (2019) Enhancement of lipid accumulation in microalgae by metabolic engineering. Biochim Biophys Acta Mol Cell Biol Lipids 4:552–566. https://doi.org/10.1016/j.bbalip.2018.10.004
Ji XJ, Huang H (2019) Engineering Microbes to Produce Polyunsaturated Fatty Acids. Trends Biotechnol 37(4):344–346. https://doi.org/10.1016/j.tibtech.2018.10.002
Hao G, Chen H, Gu Z, Zhang H, Chen W, Chen YQ (2016) Metabolic engineering of Mortierella alpina for enhanced arachidonic acid production through the NADPH-supplying strategy. Appl Environ Microbiol 82(11):3280–3288. https://doi.org/10.1128/AEM.00572-16
Zou X, Yang J, Tian X, Guo M, Li Z, Li Y (2016) Production of polymalic acid and malic acid from xylose and corncob hydrolysate by a novel Aureobasidium pullulans YJ 6–11 strain. Process Biochem 51(1):16–23. https://doi.org/10.1016/j.procbio.2015.11.018
Xia J, Xu J, Liu X, Xu J, Wang X, Li X (2017) Economic co-production of poly(malic acid) and pullulan from Jerusalem artichoke tuber by Aureobasidium pullulans HA-4D. BMC Biotechnol 17(1):20. https://doi.org/10.1186/s12896-017-0340-y
Yegin S, Saha BC, Kennedy GJ, Leathers TD (2019) Valorization of egg shell as a detoxifying and buffering agent for efficient polymalic acid production by Aureobasidium pullulans NRRL Y-2311-1 from barley straw hydrolysate. Bioresour Technol 278:130–137. https://doi.org/10.1016/j.biortech.2018.12.119
Zeng W, Zhang B, Li M, Ding S, Chen G, Liang Z (2019) Development and benefit evaluation of fermentation strategies for poly(malic acid) production from malt syrup by Aureobasidium melanogenum GXZ-6. Bioresour Technol 274:479–487. https://doi.org/10.1016/j.biortech.2018.12.027
Leathers TD, Manitchotpisit P (2013) Production of poly(beta-L-malic acid) (PMA) from agricultural biomass substrates by Aureobasidium pullulans. Biotechnol Lett 35(1):83–89. https://doi.org/10.1007/s10529-012-1045-x
Saur KM, Brumhard O, Scholz K, Hayen H, Tiso T (2019) A pH shift induces high-titer liamocin production in Aureobasidium pullulans. Appl Microbiol Biotechnol 103(12):4741–4752. https://doi.org/10.1007/s00253-019-09677-3
Guo J, Huang SY, Chen YF, Guo XW, Xiao DG (2018) Discovering the role of the apolipoprotein gene and the genes in the putative pullulan biosynthesis pathway on the synthesis of pullulan, heavy oil and melanin in Aureobasidium pullulans. World J Microbiol Biotechnol 34(1):8. https://doi.org/10.1007/s11274-017-2398-z
Xin FH, Zhang Y, Xue SJ, Chi Z, Liu GL, Hu Z et al (2017) Heavy oils (mainly alkanes) over-production from inulin by Aureobasidium melanogenum 9–1 and its transformant 88 carrying an inulinase gene. Renew Energy 105:561–568. https://doi.org/10.1016/j.renene.2017.01.004
Manitchotpisit P, Price NPJ, Leathers TD, Punnapayak H (2011) Heavy oils produced by Aureobasidium pullulans. Biotechnol Lett 33(6):1151–1157. https://doi.org/10.1007/s10529-011-0548-1
Acknowledgements
This study was supported in part by grants from the National Natural Science Foundation of China (Grant No. 31871783 and 31571816), Fundamental Research Funds for the Central Universities (XDJK2018AC002), Chongqing Social and People's Livelihood Guarantee Special Program (cstc2016shmszx80075), and National High Technology Research and Development Program of China (863 Program) (2015AA021005).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
No potential conflict of interest was reported by the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Li, T., Yang, W., Xu, X. et al. Coproduction of polymalic acid and liamocins from two waste by-products from the xylitol and gluconate industries by Aureobasidium pullulans. Bioprocess Biosyst Eng 44, 1965–1974 (2021). https://doi.org/10.1007/s00449-021-02578-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00449-021-02578-8