Abstract
In this work we investigated the enzymes produced by Bacillus aryabhattai BA03, particularly in those involved in ligninolytic activities such as laccases (Lac), lignin peroxidases (LiP) and Mn-dependent peroxidase (MnD-P). In this way, the maximal production of Lac (0.069 ± 0.000 U/mL) was obtained at pH 9, and 37 ºC after 72 h. LiP expressed the highest activity at 96 h in acid medium at 37 ºC (0.741 ± 0.029 U/mL). Meanwhile, the strain produced MnD-P (1.052 ± 0.001 U/mL) at the highest temperature assayed (44 ºC) and pH 7 at 72 h. In addition, this microorganism produced resistant endospores able to germinate after the sterilization program (121 ºC, 15 min) showing a high enzymatic activity. Using the heat-treated culture as inoculum, the percentage of decolorization of 150 mg/L of Coomassie Brillant Blue reached 89.42 ± 0.11% in only 24 h. These results open the use of these enzymes and endospores in bioremediation processes carried out under different temperatures and pH values.
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References
Organization for Economic Cooperation and Development (2005) A framework for biotechnology statistics. OECD Publishing. https://www.oecd.org/sti/inno/34935605.pdf. Accesed 28 Dec 2019
Heux S, Meynial-Salles I, O’Donohue MJ, Dumon C (2015) White biotechnology: state of the art strategies for the development of biocatalysts for biorefining. Biotechnol Adv 33:1653–1670. https://doi.org/10.1016/j.biotechadv.2015.08.004
Choi JM, Han SS, Kim HS (2015) Industrial applications of enzyme biocatalysis: current status and future aspects. Biotechnol Adv 33:1443–1454. https://doi.org/10.1016/j.biotechadv.2015.02.014
Alcalde M, Ferrer M, Plou FJ, Ballesteros A (2006) Environmental biocatalysis: from remediation with enzymes to novel green processes. Trends Biotechnol 24:281–287. https://doi.org/10.1016/j.tibtech.2006.04.002
Singhania RR, Patel AK, Thomas L, et al (2015) Chapter 13—industrial enzymes. In: Pandey A, Hofer R, Larroche C, et al (eds) Industrial biorefineries & white biotechnology. Elsevier, Amsterdam, pp 473–497
Falade AO, Nwodo UU, Iweriebor BC (2017) Lignin peroxidase functionalities and prospective applications. Microbiologyopen 6:1–14. https://doi.org/10.1002/mbo3.394
Singh RL, Singh PK, Singh RP (2015) Enzymatic decolorization and degradation of azo dyes—a review. Int Biodeterior Biodegrad 104:21–31. https://doi.org/10.1016/j.ibiod.2015.04.027
Chandra R, Chowdhary P (2015) Properties of bacterial laccases and their application in bioremediation of industrial wastes. Environ Sci Process Impacts 17:326–342. https://doi.org/10.1039/C4EM00627E
Roth S, Spiess AC (2015) Laccases for biorefinery applications: a critical review on challenges and perspectives. Bioprocess Biosyst Eng 38:2285–2313. https://doi.org/10.1007/s00449-015-1475-7
Pezzella C, Guarino L, Piscitelli A (2015) How to enjoy laccases. Cell Mol Life Sci 72:923–940. https://doi.org/10.1007/s00018-014-1823-9
Fernandes Rigamonte Alves T, Batista Da Silveira W, Lopes Passos FM, Zucchi TD (2014) Laccases from actinobacteria—what we have and what to expect. Adv Microbiol 4:285–296. https://doi.org/10.4236/aim.2014.46035
Margot J, Bennati-Granier C, Maillard J (2013) Bacterial versus fungal laccase: potential for micropollutant degradation. AMB Express 3:63. https://doi.org/10.1186/2191-0855-3-63
Siroosi M, Amoozegar MA, Khajeh K (2016) Purification and characterization of an alkaline chloride-tolerant laccase from a halotolerant bacterium, Bacillus sp. strain WT. J Mol Catal B 134:89–97. https://doi.org/10.1016/j.molcatb.2016.10.001
Gonzalo de G, Colpa DI, Habib MHM, Fraaije MW (2016) Bacterial enzymes involved in lignin degradation. J Biotechnol 236:110–119. https://doi.org/10.1016/j.jbiotec.2016.08.011
Sondhi S, Sharma P, George N, et al (2015) An extracellular thermo-alkali-stable laccase from Bacillus tequilensis SN4, with a potential to biobleach softwood pulp. 3 Biotech 5:175–185. https://doi.org/10.1007/s13205-014-0207-z
Gong G, Kim S, Lee SM (2017) Complete genome sequence of Bacillus sp. 275, producing extracellular cellulolytic, xylanolytic and ligninolytic enzymes. J Biotechnol 254:59–62. https://doi.org/10.1016/j.jbiotec.2017.05.021
Asina FNU, Brzonova I, Kozliak E (2017) Microbial treatment of industrial lignin: successes, problems and challenges. Renew Sustain Energy Rev 77:1179–1205. https://doi.org/10.1016/j.rser.2017.03.098
Tian JH, Pourcher AM, Klingelschmitt F (2016) Class P dye-decolorizing peroxidase gene: degenerated primers design and phylogenetic analysis. J Microbiol Methods 130:148–153. https://doi.org/10.1016/j.mimet.2016.09.016
Dawkar VV, Jadhav UU, Tamboli DP, Govindwar SP (2010) Efficient industrial dye decolorization by Bacillus sp. VUS with its enzyme system. Ecotoxicol Environ Saf 73:1696–1703. https://doi.org/10.1016/j.ecoenv.2010.07.002
Paz A, Carballo J, Pérez MJ, Domínguez JM (2017) Biological treatment of model dyes and textile wastewaters. Chemosphere 181:168–177. https://doi.org/10.1016/j.chemosphere.2017.04.046
Paz A, Outeiriño D, Souza de P, Oliveira R, Domínguez JM (2018) Fed-batch production of vanillin by Bacillus aryabhattai BA03 N Biotechnol 40:186–191. https://doi.org/10.1016/j.nbt.2017.07.012
Paz A, Costa-Trigo I, Tugores F (2019) Biotransformation of phenolic compounds by Bacillus aryabhattai. Bioprocess Biosyst Eng. https://doi.org/10.1007/s00449-019-02163-0
Krieg NR, Smibert RA, Sikorski J, Tindall BJ (2007) Phenotypic characterization and the principles of comparative systematics. In: Methods for general and molecular microbiology 3rd edn. American Society of Microbiology, Washington D.C., p 330–393
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
Kuwahara M, Glenn JK, Morgan MA, Gold MH (1984) Separation and characterization of two extracelluar H2O2-dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Lett 169:247–250. https://doi.org/10.1016/0014-5793(84)80327-0
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. https://doi.org/10.1007/s11274-016-2113-5
Huang XF, Santhanam N, Badri DV (2013) Isolation and characterization of lignin-degrading bacteria from rainforest soils. Biotechnol Bioeng 110:1616–1626. https://doi.org/10.1002/bit.24833
Chang YC, Choi DB, Takamizawa K, Kikuchi S (2014) Isolation of Bacillus sp. strains capable of decomposing alkali lignin and their application in combination with lactic acid bacteria for enhancing cellulase performance. Bioresour Technol 152:429–436. https://doi.org/10.1016/j.biortech.2013.11.032
Liu W, Liu C, Liu L (2017) Simultaneous decolorization of sulfonated azo dyes and reduction of hexavalent chromium under high salt condition by a newly isolated salt-tolerant strain Bacillus circulans BWL1061. Ecotoxicol Environ Saf 141:9–16. https://doi.org/10.1016/j.ecoenv.2017.03.005
Ozer A, Uzuner U, Guler HI (2018) Improved pulp bleaching potential of Bacillus subtilis WB800 through overexpression of three lignolytic enzymes from various bacteria. Biotechnol Appl Biochem 65:560–571. https://doi.org/10.1002/bab.1637
Khelil O, Choubane S, Cheba BA (2015) Co-production of cellulases and manganese peroxidases by Bacillus sp. R2 and Bacillus Cereus 11778 on waste newspaper: application in dyes decolourization. Procedia Technol 19:980–987. https://doi.org/10.1016/j.protcy.2015.02.140
Cupul WC, Abarca GH, Carrera DM, Vázquez RR (2014) Enhancement of ligninolytic enzyme activities in a Trametes maxima-Paecilomyces carneus co-culture: key factors revealed after screening using a Plackett-Burman experimental design. Electron J Biotechnol 17:114–121. https://doi.org/10.1016/j.ejbt.2014.04.007
Logan NA, De Vos P (2009) Volume 3: the firmicutes. In: Vos P, Garrity G, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer K-H, Whitman W (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York, p 1450
Abel-Santos E (2014) Endospores, sporulation and germination Molecular medical microbiology, 2nd edn. Elsevier Ltd, Amsterdam, p 163–178
Lazazzera BA (2000) Quorum sensing and starvation: signals for entry into stationary phase. Curr Opin Microbiol 3:177–182 https://doi.org/10.1016/S1369-5274(00)00072-2
Li Y, Jin K, Ghosh S (2014) Structural and functional snalysis of the GerD spore germination protein of Bacillus species. J Mol Biol 426:1995–2008. https://doi.org/10.1016/j.jmb.2014.02.004
Sen SK, Raut S, Bandyopadhyay P, Raut S (2016) Fungal decolouration and degradation of azo dyes: a review. Fungal Biol Rev 30 112 133 https://doi.org/10.1016/j.fbr.2016.06.003
Zhang C, Diao H, Lu F (2012) Degradation of triphenylmethane dyes using a temperature and pH stable spore laccase from a novel strain of Bacillus vallismortis. Bioresour Technol 126:80–86. https://doi.org/10.1016/j.biortech.2012.09.055
Lu L, Zhao M, Li GF (2012) Decolorization of synthetic dyes by immobilized spore from Bacillus amyloliquefaciens. Catal Commun 26:58–62. https://doi.org/10.1016/j.catcom.2012.04.024
Das R, Li G, Mai B, An T (2018) Spore cells from BPA degrading bacteria Bacillus sp. GZB displaying high laccase activity and stability for BPA degradation. Sci Total Environ 640–641:798–806
yKoschorreck K, Richter SM, Ene AB (2008) Cloning and characterization of a new laccase from Bacillus licheniformis catalyzing dimerization of phenolic acids. Appl Microbiol Biotechnol 79:217–224. https://doi.org/10.1007/s00253-008-1417-2
Acknowledgments
We are grateful to the Spanish Ministry of Economy and Competitiveness for the financial support given for this study (Project CTQ2015-71436-C2-1-R), which has partial financial support from the FEDER funds of the European Union, and to the “Consellería de Cultura, Educación e Ordenación Universitaria” of Xunta de Galicia for Alicia Pérez Paz’s postdoctoral fellowship ED481B 2018/073, and FAPESP (São Paulo Research Foundation) for the process n. 2018/25511-1. This study forms part of the activities of the Group with Potential for Growth (ED431B 2018/54-GPC), the Xunta de Galicia (Spain).
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Paz, A., Costa-Trigo, I., Oliveira, R.P.S. et al. Ligninolytic Enzymes of Endospore-Forming Bacillus aryabhattai BA03. Curr Microbiol 77, 702–709 (2020). https://doi.org/10.1007/s00284-019-01856-9
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DOI: https://doi.org/10.1007/s00284-019-01856-9