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Frontiers of Environmental Science & Engineering

ISSN 2095-2201

ISSN 2095-221X(Online)

CN 10-1013/X

Postal Subscription Code 80-973

2018 Impact Factor: 3.883

Front. Environ. Sci. Eng.    2020, Vol. 14 Issue (1) : 14    https://doi.org/10.1007/s11783-019-1193-5
RESEARCH ARTICLE
A newly defined dioxygenase system from Mycobacterium vanbaalenii PYR-1 endowed with an enhanced activity of dihydroxylation of high-molecular-weight polyaromatic hydrocarbons
Yiquan Wu1,2, Ying Xu1,2(), Ningyi Zhou1,2
1. State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China
2. Joint International Research Laboratory of Metabolic & Developmental Sciences, Shanghai Jiao Tong University, Shanghai 200240, China
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Abstract

Mycobacterium vanbaalenii PYR-1 utilizes PAHs at different rates.

• Both NidA3B3 and FNidA3B3 catalyze high-molecular-weight PAHs dihydroxylation.

• NidA3B3 shows an enhanced activity with an endogenous electron transport chain.

• FNidA3B3 has an enhanced activity by 50% approximately compared with NidA3B3.

• FNidA3B3/NidA3B3 and NidAB in the same strain come from different ancestors.

NidA3B3 is a terminal dioxygenase whose favorable substrates are high-molecular-weight polyaromatic hydrocarbons (PAHs) from Mycobacterium vanbaalenii PYR-1, a powerful PAHs degradation strain. NidA3B3 was reported to incorporate a dioxygen into the benzene ring of PAHs when equipped with an exogenous electron transport chain components PhdCD from Nocardioides sp. strain KP7 by biotransformation, but this enzyme system was not particularly efficient. In this study, strain PYR-1 was confirmed to utilize four different PAHs at different growth rates. When PhtAcAd, an endogenous electron transport chain of a phthalate dioxygenase system, was substituted for PhdCD to couple with NidA3B3, the specific activity to convert phenanthrene by strain BL21(DE3) [pNidA3B3-PhAcAd] was 0.15±0.03 U/mg, but the specific activity of strain BL21(DE3) [pNidA3B3-PhdCD] was only 0.025±0.006 U/mg. In addition, FNidA3, encoded by a newly defined ORF, has a prolonged 19-amino acid sequence at the N-terminal compared with NidA3. FNidA3B3 increased the activity by 50% approximately than NidA3B3 when using PhtAcAd. Components of the electron transport chain PhtAc and PhtAd were purified and characterized. The Km, kcat, kcat/Km values of the PhtAd were 123±26.9 M, 503±49.9 min1, 4.1 M1·min1, respectively. And the Km, kcat, kcat/Km values of the ferredoxin PhtAc were 52.5±9.7 M, 3.8±0.19 min1 and 0.07 M1·min1, respectively. Basing on the phylogenetic analysis, NidA3/FNidA3 were far from its isoenzyme NidA from the same strain. Combining their primary differences of transcriptional pattern in vivo, it indicated that the functionally similar Rieske dioxygenases NidA3B3/FNidA3B3 and NidAB might originate from different ancestors.

Keywords Biodegradation      polyaromatic hydrocarbons      biotransformation      ring-hydroxylating dioxygenase system     
Corresponding Author(s): Ying Xu   
Issue Date: 27 November 2019
 Cite this article:   
Yiquan Wu,Ying Xu,Ningyi Zhou. A newly defined dioxygenase system from Mycobacterium vanbaalenii PYR-1 endowed with an enhanced activity of dihydroxylation of high-molecular-weight polyaromatic hydrocarbons[J]. Front. Environ. Sci. Eng., 2020, 14(1): 14.
 URL:  
https://academic.hep.com.cn/fese/EN/10.1007/s11783-019-1193-5
https://academic.hep.com.cn/fese/EN/Y2020/V14/I1/14
Fig.1  Schema of a catalytic cycle byFNidA3B3/NidA3B3-PhtAcAd. A molecule of dioxygen is incorporated into PAHs with the aid of two electrons provided by NADH.
Strains /Plasmids Characteristics Source
Strains
Mycobacterium vanbaalenii PYR-1 Wild type; PAHs degradation bacterium Leibniz-Institut DSMZ (German)
E.coli BL21 (DE3) FompT hsdSB (RbmB) gal (c I 857 ind1 Sam7 nin5 lacUV5 T7gene1) dcm (DE3) Novagen
E.coli T1 F??80lacZ?M15 (lacZYA-argF)U169 recA1 endA1 hsdR17(rk?, mk+) phoA supE44 l-thi-1 gyrA96 relA1 tonA Novagen
Plasmids
pETDuet-1 Ampr, co-expression vector Novagen
pFNidA3B3 fnidA3B3 cloned into pETDuet-1 This study
pNidA3B3 nidA3B3 cloned into pETDuet-1 This study
pFNidA3B3-PhtAcAd fnidA3B3 and phtAcAd cloned into pETDuet-1 This study
pNidA3B3-PhtAcAd nidA3B3 and phtAcAd cloned into pETDuet-1 This study
pNidA3B3-PhdCD nidA3B3 and phdCD cloned into pETDuet-1 This study
pPhtAc(His) phtAc cloned into pETDuet-1 with His tag This study
pPhtAd(His) phtAd cloned into pETDuet-1 with His tag This study
Tab.1  Strains  and plasmids used in the experiment
Primers Sequencesa)
FnidA3 (Nco I)-F TAAGAAGGAGATATACCATGGGCATGAGTGCTCACGTTC
nidB3 (BamH I)-R GCCGAGCTCGAATTCGGATCCTTAGATCCAGAATGACAG
nidA3 (Nco I)-F TAAGAAGGAGATATACCATGGGCATGGCGCCTGATGCGA
phtAc (Nde I)-F TAAGAAGGAGATATACATATGATGGGCGGAGTTATAAAG
phtAd (KpnI)-R TTTACCAGACTCGAGGGTACCCTATGGTGATCGCGTTGC
phtAc (BamH I)-F TCATCACCACAGCCAGGATCCGATGGGCGGAGTTATAAA
phtAc (Hind III)-R GCATTATGCGGCCGCAAGCTTTCATTCGTCTACGACTTC
phtAd (BamH I)-F TCATCACCACAGCCAGGATCCGATGACGTCGCGGGTCGT
phtAd (Hind III)-R GCATTATGCGGCCGCAAGCTTCTATGGTGATCGCGTTGC
pNidA3 (BamH I)-F TCATCACCACAGCCAGGATCCGATGAGTGCTCACGTTCT
Tab.2  Primers  of PCR used in the experiment
Fig.2  Growth of M. vanbaalenii PYR-1 in the M7H9 medium with PAHs. From left to right represents the growth in the M7H9 medium containing: fluoranthene, anthracene, phenanthrene, fluorene, DMF (N, N-Dimethylformamide), respectively.
Fig.3  GC-MS analysis of products from the phenanthrene biotransformation. (A), extracted ion chromatograms of derivatized products, m/z 356 [M]; the reaction yielded 3 products in total; (B) MS of the peak of cis-9, 10-dihydrodiol-phenanthrene at 19.05 min; (C) MS of the peak of cis-3, 4-dihydrodiol-phenanthrene at 19.99 min; (D) MS of the peak of cis-1,2-dihydrodiol-phenanthrene at 20.63 min.
Electron transport chain Specific activitya)
(U/mg)
Relative activityb)
(%)
PhtAcAd 0.15±0.03 100
PhdCD 0.025±0.006 16.7±2.3
Tab.3  Activity  comparison of compatibility of electron transport chain PhtAcAd and PhdCD with NidA3B3
Fig.4  Time course of biotransformation of phenanthrene. The initial phenanthrene was set 100%; the final dihydrodiol produced by strain BL21(DE3) [pFNidA3B3-PhtAcAd] was set 100%. The sphere in solid line represents phenanthrene consumption by strain BL21(DE3) [pFNidA3B3-PhtAcAd], the square in solid line represents dihydrodiols production by strain BL21(DE3) [pFNidA3B3-PhtAcAd]; the triangle in dot line represents phenanthrene consumption by strain BL21(DE3) [pNidA3B3-PhtAcAd]; the inverted triangle in dot line represents dihydrodiols production by strain BL21(DE3) [pNidA3B3-PhtAcAd]. FNidA3B3 means strain BL21(DE3) [pFNidA3B3-PhtAcAd]; NidA3B3 means strain BL21(DE3) [pNidA3B3-PhtAcAd].
Fig.5  Enzymatic activities of components of the electron transport chain. (A) SDS-PAGE of the terminal oxygenase, FNidA3B3; (B) SDS-PAGE of components of the electron transport chain, PhtAc and PhtAd; (C) reduction of Cyt c by PhtAc-PhtAd using NADH; (D) dynamic analysis of PhtAd to reduce DCPIP. Cyt c means cytochrome c.
Fig.6  Phylogenetic  analysis of functionally validated PAHs-ring-hydroxylating dioxygenases.
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