Coenzyme Q biosynthesis in the biopesticide Shenqinmycin-producing <i>Pseudomonas aeruginosa</i> strain M18

Jiang, Haixia; Wang, Jing; Zhou, Lian; Jin, Zi-Jing; Cao, Xue-Qiang; Líu, Hao; Chen, Haifeng; He, Yanan

doi:10.1007/s10295-019-02179-1

Cited by 10 publications

(8 citation statements)

References 42 publications

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“…Biosynthesis of UQ in aerobic conditions has been widely studied and includes a series of enzymatic reactions in which a benzene ring undergoes a series of modifications involving a prenylation, a decarboxylation, three methylations, and three hydroxylations (27). Our chemical analysis identified UQ9 as the major quinone in the membranes of aerobically grown P. aeruginosa cells, which is in agreement with the literature (7,16). We found in P. aeruginosa homologues of the genes known to be involved in UQ biosynthesis in E. coli, except ubiF (Table S1).…”

Section: Discussionsupporting

confidence: 88%

“…As listed in Table S1, the analysis disclosed the presence of 11 homologous proteins (IspB, UbiA to UbiE, UbiG to UbiJ and UbiX). As reported previously, the functional homolog of UbiF is a Coq7-like hydroxylase (15) and the corresponding PA0655 protein was shown to be essential for aerobic UQ9 biosynthesis (16). Overall, we propose that the O2-dependent UQ biosynthetic pathways in P. aeruginosa and E. coli share a similar pattern (Fig.…”

Section: Identification Of Ubi Genes In the Genome Of P Aeruginosa Psupporting

confidence: 84%

“…NPP and DMQ9 are UQ9 biosynthetic intermediates (see Fig. S2) and UQ8 was already detected in Pseudomonas lipid extracts in aerobic conditions (16). Taken together, these results suggest that P. aeruginosa possesses an O2independent UQ biosynthetic pathway, which produces the major quinone species observed under anaerobic conditions.…”

Section: Discussionsupporting

confidence: 56%

“…We found in P. aeruginosa homologues of the genes known to be involved in UQ biosynthesis in E. coli, except ubiF (Table S1). Indeed, as already published, P. aeruginosa exhibits a yeast COQ7 protein homolog, which catalyzes the same reaction as UbiF from E. coli (15,16). Thereby, both bacteria share a similar UQ biosynthetic pathway involving three hydroxylases -UbiI, UbiH and UbiF or COQ7using O2 as a co-substrate ( Fig.…”

Section: Discussionsupporting

confidence: 54%

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The O2-independent pathway of ubiquinone biosynthesis is essential for denitrification in Pseudomonas aeruginosa

Michaud

Elsen

et al. 2020

Journal of Biological Chemistry

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Many proteobacteria, such as Escherichia coli, contain two main types of quinones: benzoquinones, represented by ubiquinone (UQ) and naphthoquinones, such as menaquinone (MK), and dimethyl-menaquinone (DMK). MK and DMK function predominantly in anaerobic respiratory chains, whereas UQ is the major electron carrier in the reduction of dioxygen. However, this division of labor is probably not very strict. Indeed, a pathway that produces UQ under anaerobic conditions in an UbiU-, UbiV-, and UbiT-dependent manner has been discovered recently in E. coli. Its physiological relevance is not yet understood, because MK and DMK are also present in E. coli. Here, we established that UQ9 is the major quinone of Pseudomonas aeruginosa and is required for growth under anaerobic respiration (i.e. denitrification). We demonstrate that the ORFs PA3911, PA3912, and PA3913, which are homologs of the E. coli ubiT, ubiV, and ubiU genes, respectively, are essential for UQ9 biosynthesis and, thus, for denitrification in P. aeruginosa. These three genes here are called ubiTPa, ubiVPa, and ubiUPa. We show that UbiVPa accommodates an iron–sulfur [4Fe-4S] cluster. Moreover, we report that UbiUPa and UbiTPa can bind UQ and that the isoprenoid tail of UQ is the structural determinant required for recognition by these two Ubi proteins. Since the denitrification metabolism of P. aeruginosa is believed to be important for the pathogenicity of this bacterium in individuals with cystic fibrosis, our results highlight that the O2-independent UQ biosynthetic pathway may represent a target for antibiotics development to manage P. aeruginosa infections.

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Section: Discussionsupporting

confidence: 88%

Section: Identification Of Ubi Genes In the Genome Of P Aeruginosa Psupporting

confidence: 84%

Section: Discussionsupporting

confidence: 56%

Section: Discussionsupporting

confidence: 54%

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The O2-independent pathway of ubiquinone biosynthesis is essential for denitrification in Pseudomonas aeruginosa

Michaud

Elsen

et al. 2020

Journal of Biological Chemistry

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“…We note that the expression of UbiJ from X. campestris was also unable to complement an E. coli ΔubiJ strain (18). Francisella spp shares with P. aeruginosa and X. campestris a yeast Coq7 protein homolog, which catalyzes the C6-hydroxylation as UbiF from E. coli (17,18,29). As we demonstrated previously, the Coq7 proteins are found in all three subclasses, alpha-, beta-and gamma-proteobacteria.…”

Section: Discussionmentioning

confidence: 51%

The Biosynthetic Pathway of Ubiquinone Contributes to Pathogenicity of Francisella novicida

et al. 2021

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Francisella tularensis is the causative agent of tularemia. Because of its extreme infectivity and high mortality rate, this pathogen was classified as a biothreat agent. Francisella spp are strict aerobe and ubiquinone (UQ) has been previously identified in these bacteria. While the UQ biosynthetic pathways were extensively studied in Escherichia coli allowing the identification of fifteen Ubi-proteins to date, little is known about Francisella spp. In this study, and using Francisella novicida as a surrogate organism, we first identified UQ 8 as the major quinone found in the membranes of this bacterium. Then, we characterized the UQ biosynthetic pathway in F. novicida using a combination of bioinformatics, genetics and biochemical approaches. Our analysis disclosed the presence in Francisella of ten putative Ubi-proteins and we confirmed eight of them by heterologous complementation in E. coli . The UQ biosynthetic pathways from F. novicida and E. coli share a similar pattern. However, differences were highlighted: the decarboxylase remains unidentified in Francisella spp and homologs of the Ubi-proteins involved in the O 2 -independent UQ pathway are not present. This is in agreement with the strictly aerobic niche of this bacterium. Then, via two approaches, i.e. the use of an inhibitor (3-amino-4-hydroxybenzoic acid) and a transposon mutant, which both strongly impair the synthesis of UQ, we demonstrated that UQ is essential for the growth of F. novicida in a respiratory medium and contributes to its pathogenicity in Galleria mellonella used as an alternative animal model. Importance Francisella tularensis is the causative bacterium of tularemia and is classified as a biothreat agent. Using multidisciplinary approaches, we investigated the ubiquinone (UQ) biosynthetic pathway that operates in F. novicida used as a surrogate. We showed that UQ 8 is the major quinone identified in the membranes of Francisella novicida . We identified a new competitive inhibitor, which strongly decreased the biosynthesis of UQ. Our demonstration of the crucial role of UQ for the respiratory metabolism of F. novicida and for the involving in its pathogenicity in the Galleria mellonella model should stimulate the search for selective inhibitors of bacterial UQ biosynthesis.

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Advances in bacterial pathways for the biosynthesis of ubiquinone

Abby

Kazemzadeh

Vragniau

et al. 2020

Biochimica et Biophysica Acta (BBA) - Bioenergetics

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Coenzyme Q biosynthesis in the biopesticide Shenqinmycin-producing Pseudomonas aeruginosa strain M18

Cited by 10 publications

References 42 publications

The O2-independent pathway of ubiquinone biosynthesis is essential for denitrification in Pseudomonas aeruginosa

The O2-independent pathway of ubiquinone biosynthesis is essential for denitrification in Pseudomonas aeruginosa

The Biosynthetic Pathway of Ubiquinone Contributes to Pathogenicity of Francisella novicida

Advances in bacterial pathways for the biosynthesis of ubiquinone

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