Abstract
The use of several lignocellulosic and other organic wastes has been considered in literature for the production of L-asparaginases (L-ASNase); however, the use of olive mill wastewater (OMWW) has never been contemplated as culture media. OMWW is a widely available waste in the Mediterranean that needs to be treated due to its high pollutant load. In this work, OMWW is used to feed the strain Bacillus aryabhattai Ba03, which reduces the content in phenolic compounds and produces L-ASNase. A water dilution of OMWW to 25% (w/w) supplemented with 10 g/L of yeast extract at pH 8, incubated with the strain at 30 °C, was suitable for the production of 11.6 ± 0.3 U/mL extracellular L-ASNase after 2 days. In addition, the decrease of phenolic compounds together with the production of L-ASNase could be associated with the generation of aspartic acid and the expression of peroxidase activity. At the end of the bioprocess, salicylic acid was identified in the culture supernatant, assuming that chorismate metabolic pathway was followed by B. aryabhattai Ba03.
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References
Foscolou A, Critselis E, Panagiotakos D (2018) Olive oil consumption and human health: a narrative review. Maturitas 118:60–66. https://doi.org/10.1016/j.maturitas.2018.10.013
IOI International Olive Council. http://www.internationaloliveoil.org/. Accessed 28 Nov 2019
Arvanitoyannis IS, Kassaveti A, Stefanatos S (2007) Olive oil waste treatment: a comparative and critical presentation of methods, advantages & disadvantages. Crit Rev Food Sci Nutr 47:187–229. https://doi.org/10.1080/10408390600695300
Sousa DA, Costa AI, Alexandre MR, Prata JV (2019) How an environmental issue could turn into useful high-valued products: the olive mill wastewater case. Sci Total Environ 647:1097–1105. https://doi.org/10.1016/j.scitotenv.2018.08.060
Romero-García JM, Niño L, Martínez-Patiño C, Álvarez C, Castro E, Negro MJ (2014) Biorefinery based on olive biomass. State of the art and future trends. Bioresour Technol 159:421–432. https://doi.org/10.1016/j.biortech.2014.03.062
Galanakis CM (2017) Olive mill waste: recent advances for sustainable management. Elsevier
Dourou M, Kancelista A, Juszczyk P et al (2016) Bioconversion of olive mill wastewater into high-added value products. J Clean Prod 139:957–969. https://doi.org/10.1016/j.jclepro.2016.08.133
Vaidya V, Carota E, Calonzi D, Petruccioli M, D'Annibale A (2019) Production of lignin-modifying enzymes by Trametes ochracea on high-molecular weight fraction of olive mill wastewater, a byproduct of olive oil biorefinery. New Biotechnol 50:44–51. https://doi.org/10.1016/j.nbt.2019.01.007
Jallouli R, Bezzine S (2016) Lipase production by a Tunisian Fusarium solani strain cultivated on olive oil wastewater-based media and a biotreatment assay. Desalin Water Treat 57:20327–20331. https://doi.org/10.1080/19443994.2015.1111809
Malvis A, Hodaifa G, Halioui M, Seyedsalehi M, Sánchez S (2019) Integrated process for olive oil mill wastewater treatment and its revalorization through the generation of high added value algal biomass. Water Res 151:332–342. https://doi.org/10.1016/j.watres.2018.12.026
Alsafadi D, Al-Mashaqbeh O (2017) A one-stage cultivation process for the production of poly-3-(hydroxybutyrate-co-hydroxyvalerate) from olive mill wastewater by Haloferax mediterranei. New Biotechnol 34:47–53. https://doi.org/10.1016/j.nbt.2016.05.003
Lopes AM, de Oliveira-Nascimento L, Ribeiro A et al (2017) Therapeutic l-asparaginase: upstream, downstream and beyond. Crit Rev Biotechnol 37:82–99. https://doi.org/10.3109/07388551.2015.1120705
Xu F, Oruna-Concha M-J, Elmore JS (2016) The use of asparaginase to reduce acrylamide levels in cooked food. Food Chem 210:163–171. https://doi.org/10.1016/j.foodchem.2016.04.105
Shakambari G, Ashokkumar B, Varalakshmi P (2019) L-asparaginase – a promising biocatalyst for industrial and clinical applications. Biocatal Agric Biotechnol 17:213–224. https://doi.org/10.1016/j.bcab.2018.11.018
Cachumba JJM, Antunes FAF, Peres GFD, Brumano LP, Santos JC, da Silva SS (2016) Current applications and different approaches for microbial L-asparaginase production. Braz J Microbiol 47:77–85. https://doi.org/10.1016/j.bjm.2016.10.004
Singh Y, Srivastava K (2013) Statistical and evolutionary optimization for enhanced production of an antileukemic enzyme, L-asparaginase, in a protease-deficient Bacillus aryabhattai ITBHU02 isolated from the soil contaminated with hospital waste. Indian J Exp Biol 51:322–335
Miller GL (1959) Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030
Costa-Trigo I, Otero-Penedo P, Outeiriño D, Paz A, Domínguez JM (2019) Valorization of chestnut (Castanea sativa) residues: characterization of different materials and optimization of the acid-hydrolysis of chestnut burrs for the elaboration of culture broths. Waste Manag 87:472–484. https://doi.org/10.1016/j.wasman.2019.02.028
Tien M, Kirk TK (1988) Lignin peroxidase of Phanerochaete chrysosporium. Methods Enzymol 161:238–249. https://doi.org/10.1016/0076-6879(88)61025-1
Black GW, Brown NL, Perry JJB, Randall PD et al (2015) A high-throughput screening method for determining the substrate scope of nitrilases. ChemComm 51:2660. https://doi.org/10.1039/c4cc06021k
Li X, Zhang X, Xu S, Zhang H, Xu M, Yang T, Wang L, Qian H, Zhang H, Fang H, Osire T, Rao Z, Yang S (2018) Simultaneous cell disruption and semi-quantitative activity assays for high-throughput screening of thermostable L-asparaginases. Sci Rep 8:7915. https://doi.org/10.1038/s41598-018-26241-7
Ferrara MA, Bonomo Severino NM, Valente RH et al (2010) High-yield extraction of periplasmic asparaginase produced by recombinant Pichia pastoris harbouring the Saccharomyces cerevisiae ASP3 gene. Enzym Microb Technol 47:71–76. https://doi.org/10.1016/j.enzmictec.2010.05.001
Singh Y, Srivastava SK (2014) Performance improvement of Bacillus aryabhattai ITBHU02 for high-throughput production of a tumor-inhibitory L-asparaginase using a kinetic model based approach. J Chem Technol Biotechnol 89:117–127. https://doi.org/10.1002/jctb.4121
Paz A, Carballo J, Pérez MJ, Domínguez JM (2016) Bacillus aryabhattai BA03: a novel approach to the production of natural value-added compounds. World J Microbiol Biotechnol 32:. https://doi.org/10.1007/s11274-016-2113-5
Makky EA, Chun Loh Y, Karim MR (2014) Purification and partial characterization of a low molecular weight L-asparaginase produced from corn cob waste. Biocatal Agric Biotechnol 3:265–270. https://doi.org/10.1016/j.bcab.2014.07.004
Shakambari G, Sameer Kumar R, Ashokkumar B, Varalakshmi P (2017) Agro waste utilization for cost-effective production of L -asparaginase by Pseudomonas plecoglossicida RS1 with anticancer and acrylamide mitigation potential. ACS Omega 2:8108–8117. https://doi.org/10.1021/acsomega.7b01429
Makky EA, Ali MJ (2017) Microbial fermentation biotechnology of cooked chicken bone novel substrate for L-asparaginase production. Karbala Int J Mod Sci 3:202–211. https://doi.org/10.1016/j.kijoms.2017.08.007
Paz A, Costa-Trigo I, Tugores F, Míguez M, Montaña J, Domínguez JM (2019) Biotransformation of phenolic compounds by Bacillus aryabhattai. Bioprocess Biosyst Eng 42:1671–1679. https://doi.org/10.1007/s00449-019-02163-0
Galanakis CM (2018) Phenols recovered from olive mill wastewater as additives in meat products. Trends Food Sci Technol 79:98–105. https://doi.org/10.1016/j.tifs.2018.07.010
Yoshida T, Sugano Y (2015) A structural and functional perspective of DyP-type peroxidase family. Arch Biochem Biophys 574:49–55. https://doi.org/10.1016/j.abb.2015.01.022
Noda S, Shirai T, Oyama S, Kondo A (2016) Metabolic design of a platform Escherichia coli strain producing various chorismate derivatives. Metab Eng 33:119–129. https://doi.org/10.1016/j.ymben.2015.11.007
Wang J, Shen X, Rey J, Yuan Q, Yan Y (2017) Recent advances in microbial production of aromatic natural products and their derivatives. Appl Microbiol Biotechnol 102:47–61. https://doi.org/10.1007/s00253-017-8599-4
Lee JH, Wendisch VF (2017) Biotechnological production of aromatic compounds of the extended shikimate pathway from renewable biomass. J Biotechnol 257:211–221. https://doi.org/10.1016/j.jbiotec.2016.11.016
Kallscheuer N, Marienhagen J (2018) Corynebacterium glutamicum as platform for the production of hydroxybenzoic acids. Microb Cell Factories 17:1–13. https://doi.org/10.1186/s12934-018-0923-x
Liu L, Li W, Li X, Sun X, Yuan Q (2019) Constructing an efficient salicylate biosynthesis platform by Escherichia coli chromosome integration. J Biotechnol 298:5–10. https://doi.org/10.1016/j.jbiotec.2019.04.004
Shrivastava A, Khan AA, Khurshid M et al (2016) Recent developments in L-asparaginase discovery and its potential as anticancer agent. Crit Rev Oncol Hematol 100:1–10. https://doi.org/10.1016/j.critrevonc.2015.01.002
Lanvers-Kaminsky C (2017) Asparaginase pharmacology: challenges still to be faced. Cancer Chemother Pharmacol 79:439–450. https://doi.org/10.1007/s00280-016-3236-y
Binod P, Sindhu R, Madhavan A, Abraham A, Mathew AK, Beevi US, Sukumaran RK, Singh SP, Pandey A (2017) Recent developments in L-glutaminase production and applications – an overview. Bioresour Technol 245:1766–1774. https://doi.org/10.1016/j.biortech.2017.05.059
Acknowledgments
We are grateful to Professor George Zervakis for providing the olive mill wastewater, and to the “Consellería de Cultura, Educación e Ordenación Universitaria” of Xunta de Galicia (Spain) for the postdoctoral fellowship of Alicia Pérez Paz (ED481B2018/073). Professor Nikolaos Thomaidis and his research group TrAMS are acknowledged for providing the LC-MS analysis of olive mill wastewater.
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Paz, A., Nikolaivits, E. & Topakas, E. Valorization of olive mill wastewater towards the production of L-asparaginases. Biomass Conv. Bioref. 11, 539–546 (2021). https://doi.org/10.1007/s13399-020-00725-x
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DOI: https://doi.org/10.1007/s13399-020-00725-x