Abstract
Due to growing consumer preference towards natural ingredients in food products, the production of flavors by microbial biotransformation of agrowastes provides an eco-friendly, cost-effective and sustainable pathway for biovanillin production. In the present study, biovanillin was produced by microbial biotransformation of ferulic acid (FA) using Streptomyces sp. ssr-198. The strain was able to grow in glucose medium supplemented with 1 g/L FA and produce 20.91 ± 1.11 mg/L vanillin within 96 h, along with 5.78 ± 0.13 mg/L vanillic acid in 144 h. Estimation of enzymes involved in FA degradation detected maximum feruloyl-CoA synthetase activity (1.21 ± 0.03 U/mg protein) at 96 h and maximum vanillin dehydrogenase activity (0.31 ± 0.008 U/mg protein) at 168 h, with small amounts of ferulic acid esterase activity (0.13 ± 0.002 U/mg protein) in the fermentation medium. Further, the glucose deficient production medium supplemented with 3 g/L of ferulic acid when inoculated with Streptomyces sp. ssr-198 (6% wet weight) produced maximum vanillin (685 ± 20.11 mg/L) within 72 h at 37 °C under agitation (150 rpm) and declined thereafter. Furthermore, in a one-pot experiment, wherein crude ferulic acid esterase (700 IU/g of substrate) from Enterococcus lactis SR1 was added into 10% w/v wheat bran (natural source of ferulic acid) based medium and was inoculated with 1% w/v of Streptomyces sp. ssr-198 resulted in maximum vanillin production (1.02 ± 0.02 mg/g of substrate) within 60 h of incubation. The study provides an insight into synergistic effect of using FAE of E. lactis SR1 and Streptomyces sp. ssr-198 for bioproduction of biovanillin using agro residues.
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References
Abdelkafi S, Sayadi S, Ali Gam ZB, Casalot L, Labat M (2016) Bioconversion of ferulic acid to vanillic acid by Halomonas elongate isolated from table-olive fermentation. FEMS Microbiol Lett 262(1):115–120. https://doi.org/10.1111/j.1574-6968.2006.00381.x
Ahmed Laskar A, Younus H (2019) Aldehyde toxicity and metabolism: the role of aldehyde dehydrogenases in detoxification, drug resistance and carcinogenesis. Drug Metab Rev 51(1):42–64. https://doi.org/10.1080/03602532.2018.1555587
Asabjeu AC, Noubissie E, Carly DZS, Ali A (2020) Optimization of the enzymatic hydrolysis of cellulose of Triplochiton scleroxylan sawdust in view of the production of bioethanol. Scientific African 8:e00438. https://doi.org/10.1016/j.sciaf.2020.e00438
Banerjee G, Chattopadhyay P (2018) Vanillin biotechnology: the perspectives and future. J Sci Food Agric 99(2):499–506. https://doi.org/10.1002/jsfa.9303
Boz H (2016) Ferulic acid in cereals: a review. Czech Journal of Food Sciences 33(1):1–7. https://doi.org/10.17221/401/2014-cjfs
Brink DP, Ravi K, Lidén G, Gorwa-Grauslund MF (2019) Mapping the diversity of microbial lignin catabolism: experiences from the eLignin database. Appl Microbiol Biotechnol 103:3979–4002. https://doi.org/10.1007/s00253-019-09692-4
Calisti C, Ficca AG, Barghini P, Ruzzi M (2008) Regulation of ferulic catabolic genes in Pseudomonas fluorescens BF13: involvement of a MarR family regulator. Appl Microbiol Biotechnol 80(3):475–483. https://doi.org/10.1007/s00253-008-1557-4
Chakraborty D, Kaur B, Obulisamy K, Sevam A, Wong JWC (2017) Agrowaste to vanillin conversion by a natural Pediococcus acidilactici strain BD16. Environmental Technol 38(13–14):1823–1834. https://doi.org/10.1080/09593330.2016.1237556
Chattopadhyay P, Banerjee G, Sen SK (2018) Cleaner production of vanillin through biotransformation of ferulic acid esters from agroresidue by Streptomyces sannanensis. J Cleaner Production 182:272–279. https://doi.org/10.1016/j.jclepro.2018.02.043
Chen P, Yan L, Wu Z, Li S, Bai Z, Yan X (2016) A microbial transformation using Bacillus subtilis B7-S to produce natural vanillin from ferulic acid. Scientific Reports. 6(1). https://doi.org/10.1038/srep20400
Di Gioia D, Luziatelli F, Negroni A, Ficca AG, Fava F, Ruzzi M (2011) Metabolic engineering of Pseudomonas fluorescens for the production of vanillin from ferulic acid. J Biotechnol 156(4):309–316. https://doi.org/10.1016/j.jbiotec.2011.08.014
Erten H, Tanguler H, Cabaroglu T, Canbas A (2006) The influence of inoculum level on fermentation and flavour compounds of white wines made from cv. Emir. J Inst Brew 112(3):232–236. https://doi.org/10.1002/j.2050-0416.2006.tb00718.x
Galadima AI, Salleh MM, Hussin H, Chong CS, Yahya A, Mohamad SE (2019) Biovanillin: production concepts and prevention of side product formation. Biomass Conversion Biorefinery 10(2):589–609. https://doi.org/10.1007/s13399-019-00418-0
Gallage NJ, Møller BL (2015) Vanillin-Bioconversion and bioengineering of the most popular plant flavor and its de novo biosynthesis in the Vanilla orchid. Mol Plant 8(1):40–57. https://doi.org/10.1016/j.molp.2014.11.008
Ghosh S, Sachan A, Sen SK, Mitra A (2006) Microbial transformation of ferulic acid to vanillic acid by Streptomyces sannanensis MTCC 6637. J Ind Microbiol Biotechnol 34(2):131–138. https://doi.org/10.1007/s10295-006-0177-1
Graf N, Altenbuchner J (2013) Genetic engineering of Pseudomonas putida KT2440 for rapid and high-yield production of vanillin from ferulic acid. Appl Microbiol Biotechnol 98(1):137–149. https://doi.org/10.1007/s00253-013-5303-1
Gunnarsson N, Palmqvist EA (2006) Influence of pH and carbon source on the production of vanillin from ferulic acid by Streptomyces setonii ATCC 39116. Developments Food Sci 23:73–76. https://doi.org/10.1016/S0167-4501(06)80018-X
Hua D, Ma C, Song L, Lin S, Zhang Z, Deng Z, Xu P (2007) Enhanced vanillin production from ferulic acid using adsorbent resin. Appl Microbiol Biotechnol 74(4):783–790. https://doi.org/10.1007/s00253-006-0735-5
Kaur B, Chakraborty D, Kumar B (2013) Phenolic biotransformations during conversion of ferulic acid to vanillin by lactic acid bacteria. BioMed Res Int 2013:1–6. https://doi.org/10.1155/2013/590359
Knusten JS, Liberatore MW (2009) Rheology of high-solids biomass slurries for biorefinery applications. J Rheol 53(4):877–892. https://doi.org/10.1122/1.3143878
Luziatelli F, Brunetti L, Ficca AG, Ruzzi M (2019) Maximizing the efficiency of vanillin production by biocatalyst enhancement and process optimization. Front Bioeng Biotechnol. https://doi.org/10.3389/fbioe.2019.00279
Margesin R, Voggler G, Wagner AO, Zhang D, Poyntner, (2021) Biodegradation of lignin monomers and bioconversion of ferulic acid to vanillic acid by Paraburkholderia aromaticivorans AR20-38 isolated from Alpine forest soil. Appl Microbiol Biotechnol 105:2967–2977. https://doi.org/10.1007/s00253-021-11215-z
Nurika I, Suhartini S, Azizah N, Barker GC (2020) Extraction of vanillin following bioconversion of rice straw and its optimization by Response Surface Methodology. Molecules 25(24):6031. https://doi.org/10.3390/molecules25246031
Parke D, Ornston LN (2003) Hydroxycinnamate (hca) catabolic genes from Acinetobacter sp. strain ADP1 are repressed by HcaR and are induced by hydroxycinnamoyl-Coenzyme A thioesters. Appl Environ Microbiol. 69(9):5398–409. https://doi.org/10.1128/aem.69.9.5398-5409.2003
Plaggenborg R, Overhage J, Loos A, Archer JAC, Lessard P, Sinskey AJ (2006) Potential of Rhodococcus strains for biotechnological vanillin production from ferulic acid and eugenol. Appl Microbiol Biotechnol 72(4):745–755. https://doi.org/10.1007/s00253-005-0302-5
Rejani CT, Radhakrishnan S (2020) Microbial conversion of vanillin from ferulic acid extracted from raw coir pith. Natural Product Res 19:1–9. https://doi.org/10.1080/14786419.2020.1849194
Sharma A, Sharma A, Singh J, Sharma P, Tomar GS, Singh S, et al (2020) A biorefinery approach for the production of ferulic acid from agroresidues through ferulic acid esterase of lactic acid bacteria. 3 Biotech. 10(8). https://doi.org/10.1007/s13205-020-02360-9
Singh S, Pranaw K, Singh B, Tiwari R, Nain L (2014) Production, optimization and evaluation of multicomponent holocellulase produced by Streptomyces sp. ssr-198. J Taiwan Inst Chem Eng 45(5):2379–2386. https://doi.org/10.1016/j.jtice.2014.07.014
Singh S, Tiwari R, Renuse S, Pranaw K, Nain L (2015) Proteomic analysis of Streptomyces sp. ssr-198 grown on paddy straw. J Basic Microbiol 55(6):790–797. https://doi.org/10.1002/jobm.201400639
Su R, Ni K, Wang T, Yang X, Zhang J, Liu Y (2019) Effects of ferulic acid esterase-producing Lactobacillus fermentum and cellulase additives on the fermentation quality and microbial community of alfalfa silage. PeerJ 7:e7712. https://doi.org/10.7717/peerj.7712
Taira J, Toyoshima R, Ameku N, Iguchi A, Tamaki Y (2018) Vanillin production by biotransformation of phenolic compounds in fungus. Aspergillus Luchuensis AMB Expr 8:40. https://doi.org/10.1186/s13568-018-0569-4
Tang PL, Hassan O (2020) Bioconversion of ferulic acid attained from pineapple peels and pineapple crown leaves into vanillic acid and vanillin by Aspergillus niger I-472. BMC Chem 14:7. https://doi.org/10.1186/s13065-020-0663-y
Tchuidjang TT, Noubissie E, Ali A (2021) Optimization of the pre-treatment of white sawdust (Triplochiton scleroxylon) by the organosolv process for the production of bioethanol. Oil Gas Sci. tehnol. 76 (23) https://doi.org/10.2516/ogst/2021004
Watanabe M, Yoshida E, Fukada H, Inoue H, Tokura M, Ishikawa K (2015) Characterization of a feruloyl esterase B from Talaromyces cellulolyticus. Biosci Biotechnol Biochem 79(11):1845–1851. https://doi.org/10.1080/09168451.2015.1058700
Wu D, Cai G, Li X, Li B, Lu J (2018) Cloning and expression of ferulic acid esterase gene and its effect on wort filterability. Biotech Lett 40(4):711–717. https://doi.org/10.1007/s10529-018-2511-x
Xie Y, Guo J, Li W, Wu Z, Yu Z (2021) Effects of ferulic acid esterase-producing Lactic Acid Bacteria and storage temperature on the fermentation quality, in vitro digestibility and phenolic acid extraction, yields of Sorghum (Sorghum bicolor L.) silage. Microorganisms 9(1):114. https://doi.org/10.3390/microorganisms9010114
Xu Z, Kong J, Zhang S, Wang T, Liu X (2020) Comparison of enzyme secretion and ferulic acid production by Escherichia coli expressing different Lactobacillus Feruloyl Esterases. Front Microbiol. https://doi.org/10.3389/fmicb.2020.568716
Yan L, Chen P, Zhang S, Li S, Yan X, Wang N (2016) Biotransformation of ferulic acid to vanillin in the packed bed-stirred fermentors. Scientific Reports 6(1). https://doi.org/10.1038/srep34644
Yang W, Tang H, Ni J, Wu Q, Hua D, Tao F (2013) Characterization of two Streptomyces enzymes that convert ferulic acid to vanillin. PLoS ONE 8(6):e67339. https://doi.org/10.1371/journal.pone.0067339
Zamzuri NA, Abd-Aziz S (2012) Biovanillin from agro wastes as an alternative food flavour. J Sci Food Agric 93(3):429–438. https://doi.org/10.1002/jsfa.5962
Acknowledgements
Abha Sharma acknowledges the fellowship received from the Department of Science and Technology (File No. LS/700/2016) under WoS-A scheme. All the authors thank ICAR-IARI, New Delhi for providing essential facilities for the research work.
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Sharma, A., Singh, J., Sharma, P. et al. One-pot microbial bioconversion of wheat bran ferulic acid to biovanillin. 3 Biotech 11, 462 (2021). https://doi.org/10.1007/s13205-021-03006-0
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DOI: https://doi.org/10.1007/s13205-021-03006-0