Combination of ARTP mutagenesis and color-mediated high-throughput screening to enhance 1-naphthol yield from microbial oxidation of naphthalene in aqueous system
1. College of Biotechnology and Pharmaceutical Engineering, Nanjing Tech University, Nanjing 211800, China 2. State Key Laboratory of Materials-Oriented Chemical Engineering, Nanjing Tech University, Nanjing 211800, China
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.
. [J]. Frontiers of Chemical Science and Engineering, 2020, 14(5): 793-801.
Chenggang Qiu, Alei Zhang, Sha Tao, Kang Li, Kequan Chen, Pingkai Ouyang. Combination of ARTP mutagenesis and color-mediated high-throughput screening to enhance 1-naphthol yield from microbial oxidation of naphthalene in aqueous system. Front. Chem. Sci. Eng., 2020, 14(5): 793-801.
R C Back. Carbamate insecticides, significant developments in eight years with sevin insecticides. Journal of Agricultural and Food Chemistry, 1965, 13(3): 198–199 https://doi.org/10.1021/jf60139a001
2
K A Canada, I Sachiyo, H Shim, T K Wood. Directed evolution of toluene ortho-monooxygenase for enhanced 1-naphthol synthesis and chlorinated ethene degradation. Journal of Bacteriology, 2002, 184(2): 344–349 https://doi.org/10.1128/JB.184.2.344-349.2002
3
P Molina-Espeja, M Cañellas, F J Plou, M Hofrichter, F Lucas, V Guallar, M Alcalde. Synthesis of 1-naphthol by a natural peroxygenase engineered by directed evolution. ChemBioChem, 2016, 17(4): 341–349 https://doi.org/10.1002/cbic.201500493
4
T Y Zhang, Q S Yang, Z Lu, X Liu, Z Wang, X X Li. Progress of catalytic synthesis of naphthol. Chemical Industry & Engineering Progress, 2009, 28(1): 55–61
5
A T Martínez , F J Ruiz-Duenas, S Camarero, A Serrano, D Linde, H Lund, J Vind, M Tovborg, O M Herold-Majumdar, M Hofrichter, et al. Oxidoreductases on their way to industrial biotransformations. Biotechnology Advances, 2017, 35(4): 1322–1332 https://doi.org/10.1016/j.biotechadv.2017.06.003
6
A L Zhang, G G Wei, X F Mo, N Zhou, K Q Chen, P K Ouyang. Enzymatic hydrolysis of chitin pretreated by bacterial fermentation to obtain pure N-acetyl-D-glucosamine. Green Chemistry, 2018, 20(10): 2320–2327 https://doi.org/10.1039/C8GC00265G
7
L Tomás-Gallardo, H Gomezalvarez, E Santero, B Floriano. Combination of degradation pathways for naphthalene utilization in Rhodococcus sp. strain TFB. Microbial Biotechnology, 2014, 7(2): 100–113 https://doi.org/10.1111/1751-7915.12096
8
M Zeinali, M Vossoughi, S K Ardestani. Naphthalene metabolism in Nocardia otitidiscaviarum strain TSH1, a moderately thermophilic microorganism. Chemosphere, 2008, 72(6): 905–909 https://doi.org/10.1016/j.chemosphere.2008.03.038
9
M Das, A Bhattacharya, S Banu, J Kotoky. Enhanced biodegradation of anthracene by Bacillus cereus strain JMG-01 isolated from hydrocarbon contaminated soils. Soil & Sediment Contamination, 2017, 26(5): 510–525 https://doi.org/10.1080/15320383.2017.1357111
10
L Liu, R D Schmid, V B Urlacher. 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 https://doi.org/10.1007/s00253-006-0355-0
11
L Y Rui, Y M Kwon, A Fishman, K F Reardon, T K Wood. 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 https://doi.org/10.1128/AEM.70.6.3246-3252.2004
12
S V B J Garikipati, A M Mciver, T L Peeples. Whole-cell biocatalysis for 1-naphthol production in liquid-liquid biphasic systems. Applied and Environmental Microbiology, 2009, 75(20): 6545–6552 https://doi.org/10.1128/AEM.00434-09
13
S V B J Garikipati, T L Peeples. Solvent resistance pumps of Pseudomonas putida S12: Applications in 1-naphthol production and biocatalyst engineering. Journal of Biotechnology, 2015, 210(1): 91–99 https://doi.org/10.1016/j.jbiotec.2015.06.419
14
R M Liu, L Y Liang, W J Cao, M K Wu, K Q Chen, J F Ma, M Jiang, P Wei, P K Ouyang. Succinate production by metabolically engineered Escherichia coli using sugarcane bagasse hydrolysate as the carbon source. Bioresource Technology, 2013, 135(3): 574–577 https://doi.org/10.1016/j.biortech.2012.08.120
15
M Inoue, T Inoue, M Okami, M Sayama, Y Hirai. ChemInform abstract: Bacterial oxidation of naphthalene to 1-naphthol. ChemInform, 2010, 26(1): 1315–1316 https://doi.org/10.1002/chin.199501126
16
T Inoue, T Yasuyoshi, N Morishita, M Sayama, M Inoue. Oxydation of polycyclic aromatic hydrocarbons in the presence of bacteria. Nippon Kagaku Kaishi, 1998, (3): 196–200 https://doi.org/10.1246/nikkashi.1998.196
17
M Z Wang, Y Yang, Z H Chen, Y Z Chen, Y M Wen, B L Chen. Removal of nutrients from undiluted anaerobically treated piggery wastewater by improved microalgae. Bioresource Technology, 2016, 222: 130–138 https://doi.org/10.1016/j.biortech.2016.09.128
18
Y Zhang, M L He, S M Zou, C Fei, Y Q Yan, S Y Zheng, A A Rajper, C H Wang. Breeding of high biomass and lipid producing Desmodesmus sp. by Ethylmethane sulfonate-induced mutation. Bioresource Technology, 2016, 207: 268–275 https://doi.org/10.1016/j.biortech.2016.01.120
19
X Zhang, X M Zhang, G Q Xu, X J Zhang, J S Shi, Z H Xu. 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 https://doi.org/10.1007/s00253-018-9025-2
20
M Laroussi, F Leipold. 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 https://doi.org/10.1016/j.ijms.2003.11.016
21
G Li, H P Li, L Y Wang, S Wang, H X Zhao, W T Xin . Genetic effects of radio-frequency, atmospheric-pressure glow discharges with helium. Applied Physics Letters, 2008, 92(22): 221504
22
W L Dong, F Wang, F Huang, Y Wang, J Zhou, X Ye, Z K Li, Y Hou, Y Huang, J Ma, M Jiang, Z Cui. 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 https://doi.org/10.1128/AEM.00532-16
23
S Binder, G Schendzielorz, N Stäbler, K Krumbach, K Hoffmann, M Bott, L Eggeling. A high-throughput approach to identify genomic variants of bacterial metabolite producers at the single-cell level. Genome Biology, 2012, 13(5): R40 https://doi.org/10.1186/gb-2012-13-5-r40
24
Y N Liu, Q G Li, P Zheng, Z D Zhang, Y F Liu, C M Sun, G Q Cao, W J Zhou, X W Wang, D W Zhang, et al. Developing a high-throughput screening method for threonine overproduction based on an artificial promoter. Microbial Cell Factories, 2015, 14(1): 121 https://doi.org/10.1186/s12934-015-0311-8
25
J Brosius, T J Dull, D D Sleeter, H F Noller. Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli. Journal of Molecular Biology, 1981, 148(2): 107–127 https://doi.org/10.1016/0022-2836(81)90508-8
26
Z K Hao, Y J Cai, X R Liao, X H Liang, J Y Liu, Z Y Fang, M M Hu, D B Zhang. Chitinolyticbacter meiyuanensis SYBC-H1T, Gen. Nov., sp. Nov., a chitin-degrading bacterium isolated from soil. Current Microbiology, 2011, 62(6): 1732–1738 https://doi.org/10.1007/s00284-011-9921-5
27
J D Thompson, T J Gibson, F Plewniak, F Jeanmougin, D G Higgins. The CLUSTAL X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 1997, 25(25): 4876–4882 https://doi.org/10.1093/nar/25.24.4876
28
T Vralstad, E Myhre, T Schumacher. 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 https://doi.org/10.1046/j.1469-8137.2002.00444.x
29
W Ludwig, O Strunk, S Klugbauer, N Klugbauer, M Weizenegger, J Neumaier, M Bachleitner, K H Schleifer. Bacterial phylogeny based on comparative sequence analysis. Electrophoresis, 2010, 19(4): 554–568 https://doi.org/10.1002/elps.1150190416
30
M Kimura. 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 https://doi.org/10.1007/BF01731581
31
G Norwitz, P N Keliher. 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 https://doi.org/10.1016/S0003-2670(00)00034-9
32
Y Lu, L Y Wang, K Ma, G Li, C Zhang, H X Zhao, Q H Lai, H P Li, X H Xing. 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 https://doi.org/10.1016/j.bej.2011.02.020
33
S Cao, X Zhou, W B Jin, F Wang, R J Tu, S F Han, H Y Chen, C Chen, G J Xie, F Ma. Improving of lipid productivity of the oleaginous microalgae Chlorella pyrenoidosa via atmospheric and room temperature plasma (ARTP). Bioresource Technology, 2017, 244(2): 1400–1406 https://doi.org/10.1016/j.biortech.2017.05.039
34
C K Gu, G Y Wang, S Mai, P F Wu, J R Wu, G H Wang, H J Liu, J A Zhang. ARTP mutation and genome shuffling of ABE fermentation symbiotic system for improvement of butanol production. Applied Microbiology and Biotechnology, 2017, 101(5): 2189–2199 https://doi.org/10.1007/s00253-017-8093-z
35
X M Cao, Z S Luo, W Z Zeng, S Xu, L Q Zhao, J W Zhou. 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 https://doi.org/10.1007/s00253-017-8658-x
36
H Y Li, W Z Zeng, J W Zhou. High-throughput screening of Methylobacterium extorquens for high production of pyrroloquinoline quinone. Chinese Journal of Biotechnology, 2018, 34(5): 794–802
37
X Zhang, X M Zhang, G Q Xu, X Zhang, J Shi, Z Xu. 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 https://doi.org/10.1007/s00253-018-9025-2
38
L Y Wang, Z L Huang, G Li, H X Zhao, X H Xing, W T Sun, H P Li, Z X Gou, C Y Bao. Novel mutation breeding method for Streptomyces avermitilis using an atmospheric pressure glow discharge plasma. Journal of Applied Microbiology, 2010, 108(3): 851–858 https://doi.org/10.1111/j.1365-2672.2009.04483.x
39
M Hassanshahian, N A Boroujeni. Enrichment and identification of naphthalene degrading bacteria from the Persian Gulf. Marine Pollution Bulletin, 2016, 107(1): 59–65 https://doi.org/10.1016/j.marpolbul.2016.04.020
40
Y Tao, W E Bentley, T K Wood. Phenol and 2-naphthol production by toluene 4-monooxygenases using an aqueous/dioctyl phthalate system. Applied Microbiology and Biotechnology, 2005, 68(5): 614–621 https://doi.org/10.1007/s00253-005-1939-9
