Comparative genomic analysis of isoproturon‐mineralizing sphingomonads reveals the isoproturon catabolic mechanism

Yan, Xin; Gu, Tao; Yi, ZhongQuan; Huang, Junwei; Liu, Xiaowei; Zhang, Ji; Xu, Xihui; Xin, Zhihong; Hong, Qing; He, Jun; Spain, Jim C.; Li, Shunpeng; Jiang, Jiandong

doi:10.1111/1462-2920.13413

Cited by 40 publications

(28 citation statements)

References 65 publications

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“…Potentially, the ferredoxin and ferredoxin reductase genes do not cluster with dpeA1A2. Similar phenomena have also been observed for certain RHO genes responsible for xenobiotic metabolism (1,26,32,35,36). According to Kweon et al (3), RHO dioxygenases possess two types of ferredoxin, namely, the [2Fe-2S] type and the [3Fe-4S] type, and three types of reductase, namely, the glutathione reductase (GR) type, the FNR N (ferredoxin-NADP ϩ reductase with the [2Fe-2S] ferredoxin domain connected to the N terminus of the flavin binding domain) type, and the FNR C (ferredoxin-NADP ϩ reductase with the [2Fe-2S] ferredoxin domain connected to the C terminus of the NAD domain) type.…”

Section: Orf Analysis Of the Dpe Gene Cluster And Screening Of The Gesupporting

confidence: 79%

Degradation of Diphenyl Ether in Sphingobium phenoxybenzoativorans SC_3 Is Initiated by a Novel Ring Cleavage Dioxygenase

Cai

Chen

et al. 2017

Appl Environ Microbiol

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Sphingobium phenoxybenzoativorans SC_3 degrades and utilizes diphenyl ether (DE) or 2-carboxy-DE as its sole carbon and energy source. In this study, we report the degradation of DE and 2-carboxy-DE initiated by a novel ring cleavage angular dioxygenase (diphenyl ether dioxygenase [Dpe]) in the strain. Dpe functions at the angular carbon and its adjacent carbon (C-1a, C-2) of a benzene ring in DE (or the 2-carboxybenzene ring in 2-carboxy-DE) and cleaves the C-1aOC-2 bond (decarboxylation occurs simultaneously for 2-carboxy-DE), yielding 2,4-hexadienal phenyl ester, which is subsequently hydrolyzed to muconic acid semialdehyde and phenol. Dpe is a type IV Rieske non-heme iron oxygenase (RHO) and consists of three components: a hetero-oligomer oxygenase, a [2Fe-2S]-type ferredoxin, and a glutathione reductase (GR)-type reductase. Genetic analyses revealed that dpeA1A2 plays an essential role in the degradation and utilization of DE and 2-carboxy-DE in S. phenoxybenzoativorans SC_3. Enzymatic study showed that transformation of 1 molecule of DE needs two molecules of oxygen and two molecules of NADH, supporting the assumption that the cleavage of DE catalyzed by Dpe is a continuous two-step dioxygenation process: DE is dioxygenated at C-1a and C-2 to form a hemiacetal-like intermediate, which is further deoxygenated, resulting in the cleavage of the C-1aOC-2 bond to form one molecule of 2,4-hexadienal phenyl ester and two molecules of H 2 O. This study extends our knowledge of the mode and mechanism of ring cleavage of aromatic compounds.IMPORTANCE Benzene ring cleavage, catalyzed by dioxygenase, is the key and speed-limiting step in the aerobic degradation of aromatic compounds. As previously reported, in the ring cleavage of DEs, the benzene ring needs to be first dihydroxylated at a lateral position and subsequently dehydrogenated and opened through extradiol cleavage. This process requires three enzymes (two dioxygenases and one dehydrogenase). In this study, we identified a novel angular dioxygenase (Dpe) in S. phenoxybenzoativorans SC_3. Under Dpe-mediated catalysis, the benzene ring of DE is dioxygenated at the angular position (C-1a, C-2), resulting in the cleavage of the C-1aOC-2 bond to generate a novel product, 2,4-hexadienal phenyl ester. This process needs only one angular dioxygenase, Dpe. Thus, the ring cleavage catalyzed by Dpe represents a novel mechanism of benzene ring cleavage.

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Section: Orf Analysis Of the Dpe Gene Cluster And Screening Of The Gesupporting

confidence: 79%

Degradation of Diphenyl Ether in Sphingobium phenoxybenzoativorans SC_3 Is Initiated by a Novel Ring Cleavage Dioxygenase

Cai

Chen

et al. 2017

Appl Environ Microbiol

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“…The IS6100 element is a member of the IS6 family and has an extremely broad host range (32). IS6100 has been found to be associated with the genes (lin, mpd, and adoQTA1A2B) involved in the catabolism of hexachlorocyclohexane, methyl parathion, and aniline (23,33,34). ISRsp3 containing a transposase gene pair (istA-istB) belongs to the IS21 family (20).…”

Section: Discussionmentioning

confidence: 99%

“…The linABCDEF genes for the catabolism of hexachlorocyclohexane (HCH) are found in the HCH-mineralizing sphingomonads isolated all over the world (22). Similarly, the genes involved in the isoproturon-catabolic pathway are highly conserved among the isoproturon-mineralizing sphingomonads (23). Considering these facts, we hypothesized that the genes involved in carbofuran catabolism might also be conserved (likely with Ͼ95% similarity) among carbofuran-degrading sphingomonads.…”

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confidence: 99%

Hydrolase CehA and Monooxygenase CfdC Are Responsible for Carbofuran Degradation in Sphingomonas sp. Strain CDS-1

Yan

Wen

et al. 2018

Appl Environ Microbiol

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Carbofuran, a broad-spectrum systemic insecticide, has been extensively used for approximately 50 years. Diverse carbofuran-degrading bacteria have been described, among which sphingomonads have exhibited an extraordinary ability to catabolize carbofuran; other bacteria can only convert carbofuran to carbofuran phenol, while all carbofuran-degrading sphingomonads can degrade both carbofuran and carbofuran phenol. However, the genetic basis of carbofuran catabolism in sphingomonads has not been well elucidated. In this work, we sequenced the draft genome of sp. strain CDS-1 that can transform both carbofuran and carbofuran phenol but fails to grow on them. On the basis of the hypothesis that the genes involved in carbofuran catabolism are highly conserved among carbofuran-degrading sphingomonads, two such genes, and , were predicted from the 84 open reading frames (ORFs) that share ≥95% nucleic acid similarities between strain CDS-1 and another sphingomonad sp. strain KN65.2 that is able to mineralize the benzene ring of carbofuran. The results of the gene knockout, genetic complementation, heterologous expression, and enzymatic experiments reveal that and are responsible for the conversion of carbofuran and carbofuran phenol, respectively, in strain CDS-1. CehA hydrolyzes carbofuran to carbofuran phenol. CfdC, a reduced flavin mononucleotide (FMNH)- or reduced flavin adenine dinucleotide (FADH)-dependent monooxygenase, hydroxylates carbofuran phenol at the benzene ring in the presence of NADH, FMN/FAD, and the reductase CfdX. It is worth noting that we found that carbaryl hydrolase CehA, which was previously demonstrated to have no activity toward carbofuran, can actually convert carbofuran to carbofuran phenol, albeit with very low activity. Due to the extensive use of carbofuran over the past 50 years, bacteria have evolved catabolic pathways to mineralize this insecticide, which plays an important role in eliminating carbofuran residue in the environment. This study revealed the genetic determinants of carbofuran degradation in sp. strain CDS-1. We speculate that the close homologues and are highly conserved among other carbofuran-degrading sphingomonads and play the same roles as those described here. These findings deepen our understanding of the microbial degradation mechanism of carbofuran and lay a foundation for the better use of microbes to remediate carbofuran contamination.

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“…Recently, Yan et al . 10 showed via comparative genomics the key role of plasmid-localized transposons in the evolution of novel metabolic pathways for the degradation of phenylurea herbicides by Sphingomonads.…”

Section: Resultsmentioning

confidence: 99%

“…Advances in high-throughput sequencing have shed light into the full genetic armoury of xenobiotic-degrading bacteria 9,10 , making protein annotation, metabolic pathway prediction and reconstruction feasible 11,12 . However, the mere presence of putative catabolic genes in a bacterial genome does not guarantee biodegradability in a given environment 13 .…”

Section: Introductionmentioning

confidence: 99%

Metabolic pathway and cell adaptation mechanisms revealed through genomic, proteomic and transcription analysis of a Sphingomonas haloaromaticamans strain degrading ortho-phenylphenol

Perruchon

Vasileiadis

Rousidou

et al. 2017

Sci Rep

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Ortho-phenylphenol (OPP) is a fungicide contained in agro-industrial effluents produced by fruit-packaging plants. Within the frame of developing bio-strategies to detoxify these effluents, an OPP-degrading Sphingomonas haloaromaticamans strain was isolated. Proteins/genes with a putative catabolic role and bacterium adaptation mechanisms during OPP degradation were identified via genomic and proteomic analysis. Transcription analysis of all putative catabolic genes established their role in the metabolism of OPP. The formation of key transformation products was verified by chromatographic analysis. Genomic analysis identified two orthologous operons encoding the ortho-cleavage of benzoic acid (BA) (ben/cat). The second ben/cat operon was located in a 92-kb scaffold along with (i) an operon (opp) comprising genes for the transformation of OPP to BA and 2-hydroxypenta-2,4-dienoate (and genes for its transformation) and (ii) an incomplete biphenyl catabolic operon (bph). Proteomics identified 13 up-regulated catabolic proteins when S. haloaromaticamans was growing on OPP and/or BA. Transcription analysis verified the key role of the catabolic operons located in the 92-kb scaffold, and flanked by transposases, on the transformation of OPP by S. haloaromaticamans. A flavin-dependent monoxygenase (OppA1), one of the most up-regulated proteins in the OPP-growing cells, was isolated via heterologous expression and its catabolic activity was verified in vitro.

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Comparative genomic analysis of isoproturon‐mineralizing sphingomonads reveals the isoproturon catabolic mechanism

Cited by 40 publications

References 65 publications

Degradation of Diphenyl Ether in Sphingobium phenoxybenzoativorans SC_3 Is Initiated by a Novel Ring Cleavage Dioxygenase

Degradation of Diphenyl Ether in Sphingobium phenoxybenzoativorans SC_3 Is Initiated by a Novel Ring Cleavage Dioxygenase

Hydrolase CehA and Monooxygenase CfdC Are Responsible for Carbofuran Degradation in Sphingomonas sp. Strain CDS-1

Metabolic pathway and cell adaptation mechanisms revealed through genomic, proteomic and transcription analysis of a Sphingomonas haloaromaticamans strain degrading ortho-phenylphenol

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