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Signal Synthase-Type versus Catabolic Monooxygenases: Retracing 3-Hydroxylation of 2-Alkylquinolones and Their -Oxides by Pseudomonas aeruginosa and Other Pulmonary Pathogens. | LitMetric

AI Article Synopsis

Article Abstract

The multiple biological activities of 2-alkylquinolones (AQs) are crucial for virulence of , conferring advantages during infection and in polymicrobial communities. Whereas 2-heptyl-3-hydroxyquinolin-4(1)-one (the " quinolone signal" [PQS]) is an important quorum sensing signal molecule, 2-alkyl-1-hydroxyquinolin-4(1)-ones (also known as 2-alkyl-4-hydroxyquinoline -oxides [AQNOs]) are antibiotics inhibiting respiration. Hydroxylation of the PQS precursor 2-heptylquinolin-4(1)-one (HHQ) by the signal synthase PqsH boosts AQ quorum sensing. Remarkably, the same reaction, catalyzed by the ortholog AqdB, is used by to initiate degradation of AQs. The antibiotic 2-heptyl-1-hydroxyquinolin-4(1)-one (HQNO) is hydroxylated by to the less toxic derivative PQS--oxide (PQS-NO), a reaction probably also catalyzed by a PqsH/AqdB ortholog. In this study, we provide a comparative analysis of four AQ 3-monooxygenases of different organisms. Due to the major impact of AQ/AQNO 3-hydroxylation on the biological activities of the compounds, we surmised adaptations on the enzymatic and/or physiological level to serve either the producer or target organisms. Our results indicate that all enzymes share similar features and are incapable of discriminating between AQs and AQNOs. PQS-NO, hence, occurs as a native metabolite of although the unfavorable AQNO 3-hydroxylation is minimized by export as shown for HQNO, involving at least one multidrug efflux pump. Moreover, is capable of degrading the AQNO heterocycle by concerted action of AqdB and dioxygenase AqdC. However, and orthologs disfavor AQNOs despite their higher toxicity, suggesting that catalytic constraints restrict evolutionary adaptation and lead to the preference of non--oxide substrates by AQ 3-monooxygenases., , and are major players in bacterial chronic infections and particularly common colonizers of cystic fibrosis (CF) lung tissue. Whereas is an early onset pathogen in CF, establishes at later stages. occurs at all stages but has a lower epidemiological incidence. The dynamics of how these pathogens interact can affect survival and therapeutic success. 2-Alkylquinolone (AQ) and 2-alkylhydroxyquinoline -oxide (AQNO) production is a major factor of virulence. The 3-position of the AQ scaffold is critical, both for attenuation of AQ toxicity or degradation by competitors, as well as for full unfolding of quorum sensing. Despite lacking signaling functionality, AQNOs have the strongest impact on suppression of Gram-positives. Because evidence for 3-hydroxylation of AQNOs has been reported, it is desirable to understand the extent by which AQ 3-monooxygenases contribute to manipulation of AQ/AQNO equilibrium, resistance, and degradation.

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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8105023PMC
http://dx.doi.org/10.1128/AEM.02241-20DOI Listing

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