Combination of ARTP mutagenesis and color-mediated high-throughput screening to enhance 1-naphthol yield from microbial oxidation of naphthalene in aqueous system

Abstract

Strain QCG of the aerobic bacteria Bacillus cereus is capable of producing 1-naphthol from naphthalene, this strain was first isolated and characterized in this study. Strain QCG was mutagenized to enhance 1-naphthol production, using atmospheric and room temperature plasma (ARTP) technology. Then, a microbial clone screening system was used to accelerate the operation. Meanwhile, a novel color-mediated high-throughput screening using 4-aminoantipyrine was performed to screen mutants. The optimal mutant strain QCG4 produced 19.58±0.34 mg∙L^‒1 1-naphthol from naphthalene that was 47.32% higher than that of the original strain (13.29±0.28 mg∙L^‒1). In addition, the optimal conditions for 1-naphthol production via whole-cell catalysis of strain QCG4 were determined to be an OD₆₀₀ of 40, 150 mg∙L^‒1 naphthalene, and 7.5% dimethyl formamide as a co-solvent at pH 7.5 and 26°C for 3 h, resulting in 41.18±0.12 mg∙L^‒1 1-naphthol, i.e., the mutant strain produces a 2.1-fold higher yield compared to the original strain.

Graphical abstract

Keywords

Bacillus cereus QCG / naphthalene / 1-naphthol / ARTP mutagenesis / high-throughput screening / 4-aminoantipyrine

References

[1] Back R C. Carbamate insecticides, significant developments in eight years with sevin insecticides. Journal of Agricultural and Food Chemistry, 1965, 13(3): 198–199

[2] Canada K A, Sachiyo I, Shim H, Wood T K. Directed evolution of toluene ortho-monooxygenase for enhanced 1-naphthol synthesis and chlorinated ethene degradation. Journal of Bacteriology, 2002, 184(2): 344–349

[3] Molina-Espeja P, Cañellas M, Plou F J, Hofrichter M, Lucas F, Guallar V, Alcalde M. Synthesis of 1-naphthol by a natural peroxygenase engineered by directed evolution. ChemBioChem, 2016, 17(4): 341–349

[4] Zhang T Y, Yang Q S, Lu Z, Liu X, Wang Z, Li X X. Progress of catalytic synthesis of naphthol. Chemical Industry & Engineering Progress, 2009, 28(1): 55–61

[5] Martínez A T, Ruiz-Duenas F J, Camarero S, Serrano A, Linde D, Lund H, Vind J, Tovborg M, Herold-Majumdar O M, Hofrichter M, Oxidoreductases on their way to industrial biotransformations. Biotechnology Advances, 2017, 35(4): 1322–1332

[6] Zhang A L, Wei G G, Mo X F, Zhou N, Chen K Q, Ouyang P K. Enzymatic hydrolysis of chitin pretreated by bacterial fermentation to obtain pure N-acetyl-D-glucosamine. Green Chemistry, 2018, 20(10): 2320–2327

[7] Tomás-Gallardo L, Gomezalvarez H, Santero E, Floriano B. Combination of degradation pathways for naphthalene utilization in Rhodococcus sp. strain TFB. Microbial Biotechnology, 2014, 7(2): 100–113

[8] Zeinali M, Vossoughi M, Ardestani S K. Naphthalene metabolism in Nocardia otitidiscaviarum strain TSH1, a moderately thermophilic microorganism. Chemosphere, 2008, 72(6): 905–909

[9] Das M, Bhattacharya A, Banu S, Kotoky J. Enhanced biodegradation of anthracene by Bacillus cereus strain JMG-01 isolated from hydrocarbon contaminated soils. Soil & Sediment Contamination, 2017, 26(5): 510–525

[10] Liu L, Schmid R D, Urlacher V B. Cloning, expression, and characterization of a self-sufficient cytochrome P450 monooxygenase from Rhodococcus ruber DSM 44319. Applied Microbiology and Biotechnology, 2006, 72(5): 876–882

[11] Rui L Y, Kwon Y M, Fishman A, Reardon K F, Wood T K. Saturation mutagenesis of toluene ortho-monooxygenase of Burkholderia cepacia G4 for Enhanced 1-naphthol synthesis and chloroform degradation. Applied and Environmental Microbiology, 2004, 70(6): 3246–3252

[12] Garikipati S V B J, Mciver A M, Peeples T L. Whole-cell biocatalysis for 1-naphthol production in liquid-liquid biphasic systems. Applied and Environmental Microbiology, 2009, 75(20): 6545–6552

[13] Garikipati S V B J, Peeples T L. Solvent resistance pumps of Pseudomonas putida S12: Applications in 1-naphthol production and biocatalyst engineering. Journal of Biotechnology, 2015, 210(1): 91–99

[14] Liu R M, Liang L Y, Cao W J, Wu M K, Chen K Q, Ma J F, Jiang M, Wei P, Ouyang P K. Succinate production by metabolically engineered Escherichia coli using sugarcane bagasse hydrolysate as the carbon source. Bioresource Technology, 2013, 135(3): 574–577

[15] Inoue M, Inoue T, Okami M, Sayama M, Hirai Y. ChemInform abstract: Bacterial oxidation of naphthalene to 1-naphthol. ChemInform, 2010, 26(1): 1315–1316

[16] Inoue T, Yasuyoshi T, Morishita N, Sayama M, Inoue M. Oxydation of polycyclic aromatic hydrocarbons in the presence of bacteria. Nippon Kagaku Kaishi, 1998, (3): 196–200

[17] Wang M Z, Yang Y, Chen Z H, Chen Y Z, Wen Y M, Chen B L. Removal of nutrients from undiluted anaerobically treated piggery wastewater by improved microalgae. Bioresource Technology, 2016, 222: 130–138

[18] Zhang Y, He M L, Zou S M, Fei C, Yan Y Q, Zheng S Y, Rajper A A, Wang C H. Breeding of high biomass and lipid producing Desmodesmus sp. by Ethylmethane sulfonate-induced mutation. Bioresource Technology, 2016, 207: 268–275

[19] Zhang X, Zhang X M, Xu G Q, Zhang X J, Shi J S, Xu Z H. Integration of ARTP mutagenesis with biosensor-mediated high-throughput screening to improve L-serine yield in Corynebacterium glutamicum. Applied Microbiology and Biotechnology, 2018, 102(4): 1–13

[20] Laroussi M, Leipold F. Evaluation of the roles of reactive species, heat, and UV radiation in the inactivation of bacterial cells by air plasmas at atmospheric pressure. International Journal of Mass Spectrometry, 2004, 233(1): 81–86

[21] Li G, Li H P, Wang L Y, Wang S, Zhao H X, Xin W T. Genetic effects of radio-frequency, atmospheric-pressure glow discharges with helium. Applied Physics Letters, 2008, 92(22): 221504

[22] Dong W L, Wang F, Huang F, Wang Y, Zhou J, Ye X, Li Z K, Hou Y, Huang Y, Ma J, Jiang M, Cui Z. Metabolic pathway involved in 6-chloro-2-benzoxazolinone degradation by Pigmentiphaga sp. strain DL-8 and identification of the novel metal-dependent hydrolase CbaA. Applied and Environmental Microbiology, 2016, 82(14): 4169–4179

[23] Binder S, Schendzielorz G, Stäbler N, Krumbach K, Hoffmann K, Bott M, Eggeling L. A high-throughput approach to identify genomic variants of bacterial metabolite producers at the single-cell level. Genome Biology, 2012, 13(5): R40

[24] Liu Y N, Li Q G, Zheng P, Zhang Z D, Liu Y F, Sun C M, Cao G Q, Zhou W J, Wang X W, Zhang D W, et al. Developing a high-throughput screening method for threonine overproduction based on an artificial promoter. Microbial Cell Factories, 2015, 14(1): 121

[25] Brosius J, Dull T J, Sleeter D D, Noller H F. Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli. Journal of Molecular Biology, 1981, 148(2): 107–127

[26] Hao Z K, Cai Y J, Liao X R, Liang X H, Liu J Y, Fang Z Y, Hu M M, Zhang D B. Chitinolyticbacter meiyuanensis SYBC-H₁^T, Gen. Nov., sp. Nov., a chitin-degrading bacterium isolated from soil. Current Microbiology, 2011, 62(6): 1732–1738

[27] Thompson J D, Gibson T J, Plewniak F, Jeanmougin F, Higgins D G. The CLUSTAL X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 1997, 25(25): 4876–4882

[28] Vralstad T, Myhre E, Schumacher T. Molecular diversity and phylogenetic affinities of symbiotic root-associated ascomycetes of the helotiales in burnt and metal polluted habitats. New Phytologist, 2002, 105(1): 131–148

[29] Ludwig W, Strunk O, Klugbauer S, Klugbauer N, Weizenegger M, Neumaier J, Bachleitner M, Schleifer K H. Bacterial phylogeny based on comparative sequence analysis. Electrophoresis, 2010, 19(4): 554–568

[30] Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 1980, 16(2): 111–120

[31] Norwitz G, Keliher P N. Effect of acidity and alkalinity on the distillation of phenol: Interferences of aromatic amines and formaldehyde with the 4-aminoantipyrine spectro-photometric method for phenol. Analytica Chimica Acta, 1980, 119(1): 99–111

[32] Lu Y, Wang L Y, Ma K, Li G, Zhang C, Zhao H X, Lai Q H, Li H P, Xing X H. Characteristics of hydrogen production of an Enterobacter aerogenes mutant generated by a new atmospheric and room temperature plasma (ARTP). Biochemical Engineering Journal, 2011, 55(1): 17–22

[33] Cao S, Zhou X, Jin W B, Wang F, Tu R J, Han S F, Chen H Y, Chen C, Xie G J, Ma F. Improving of lipid productivity of the oleaginous microalgae Chlorella pyrenoidosa via atmospheric and room temperature plasma (ARTP). Bioresource Technology, 2017, 244(2): 1400–1406

[34] Gu C K, Wang G Y, Mai S, Wu P F, Wu J R, Wang G H, Liu H J, Zhang J A. ARTP mutation and genome shuffling of ABE fermentation symbiotic system for improvement of butanol production. Applied Microbiology and Biotechnology, 2017, 101(5): 2189–2199

[35] Cao X M, Luo Z S, Zeng W Z, Xu S, Zhao L Q, Zhou J W. Enhanced avermectin production by Streptomyces avermitilis ATCC 31267 using high-throughput screening aided by fluorescence-activated cell sorting. Applied Microbiology and Biotechnology, 2018, 102(2): 703–712

[36] Li H Y, Zeng W Z, Zhou J W. High-throughput screening of Methylobacterium extorquens for high production of pyrroloquinoline quinone. Chinese Journal of Biotechnology, 2018, 34(5): 794–802

[37] Zhang X, Zhang X M, Xu G Q, Zhang X, Shi J, Xu Z. Integration of ARTP mutagenesis with biosensor-mediated high-throughput screening to improve L-serine yield in Corynebacterium glutamicum. Applied Microbiology and Biotechnology, 2018, 102(14): 5939–5951

[38] Wang L Y, Huang Z L, Li G, Zhao H X, Xing X H, Sun W T, Li H P, Gou Z X, Bao C Y. Novel mutation breeding method for Streptomyces avermitilis using an atmospheric pressure glow discharge plasma. Journal of Applied Microbiology, 2010, 108(3): 851–858

[39] Hassanshahian M, Boroujeni N A. Enrichment and identification of naphthalene degrading bacteria from the Persian Gulf. Marine Pollution Bulletin, 2016, 107(1): 59–65

[40] Tao Y, Bentley W E, Wood T K. Phenol and 2-naphthol production by toluene 4-monooxygenases using an aqueous/dioctyl phthalate system. Applied Microbiology and Biotechnology, 2005, 68(5): 614–621

Acknowledgments

This work was supported by COVESTRO, the National Key Research and Development Program (Grant No. 2016YFA0204300), the Jiangsu Province Natural Science Foundation for Youths (No. BK20170997), and China Postdoctoral Science Foundation (Nos. 2018M642237 and 2017T100359).

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