Integrated analysis of electrical stimulation effects on Pseudomonas aeruginosa PAO1 inoculated denitrifying community: targeted and untargeted metabolomic analysis of phenazine biosynthesis and quorum sensing

This study investigates how 0.8 V applied voltage modulates phenazine biosynthesis, quorum sensing (QS), and microbial interactions in Pseudomonas aeruginosa PAO1-inoculated microbial electrolysis cell (MEC) reactors. Voltage stimulation significantly enhanced phenazine derivatives (PYO: 8.65-fold;...

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Main Authors: Li Wu, Yong Liu, Jianping Deng, Shuanglin Gui, Hanbing Nie
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-06-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2025.1621417/full
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author Li Wu
Li Wu
Yong Liu
Yong Liu
Jianping Deng
Jianping Deng
Shuanglin Gui
Shuanglin Gui
Hanbing Nie
Hanbing Nie
author_facet Li Wu
Li Wu
Yong Liu
Yong Liu
Jianping Deng
Jianping Deng
Shuanglin Gui
Shuanglin Gui
Hanbing Nie
Hanbing Nie
author_sort Li Wu
collection DOAJ
description This study investigates how 0.8 V applied voltage modulates phenazine biosynthesis, quorum sensing (QS), and microbial interactions in Pseudomonas aeruginosa PAO1-inoculated microbial electrolysis cell (MEC) reactors. Voltage stimulation significantly enhanced phenazine derivatives (PYO: 8.65-fold; 1-OH-PHZ: 14.98-fold) and QS signals (C4-HSL: 2.88-fold; 3-OXO-C12-HSL: 2.21-fold), correlating with upregulated biosynthetic genes (phzG: 14.8-fold; rhlI: 15.2-fold). Electrical stimulation amplified QS cross-regulation, reinforcing Las-mediated positive feedback on Rhl/PQS systems while attenuating Rhl’s inhibition of PQS. Untargeted metabolomic analysis demonstrated significant alterations in bacterial metabolic activity under electrical stimulation, identifying 140 differential metabolites. Among these, indole, a signaling molecule with QS-like functionality, exhibited the highest VIP score as an upregulated metabolite, and another indole derivative, brassicanal A, was also elevated. KEGG pathway enrichment analysis highlighted that these metabolites were primarily associated with amino acid metabolism and transport, while anthranilic acid and L-tryptophan—key metabolites linked to both indole-related pathways and phenazine biosynthesis—were also identified. Correlation analysis between differential metabolites with microbial communities confirmed that Delftia and Burkholderiales were strongly associated with phenazine biosynthesis and QS activity in P. aeruginosa PAO1. These findings highlight voltage as a key driver of metabolic rewiring and microbial niche partitioning, optimizing MEC reactor performance for wastewater treatment. This work provides foundational insights into electro-stimulated biofilm engineering through targeted QS and metabolic pathway regulation.
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institution Kabale University
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publishDate 2025-06-01
publisher Frontiers Media S.A.
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spelling doaj-art-4cf7b5deb41e4d259c17a1cafc8cef672025-08-20T03:25:42ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-06-011610.3389/fmicb.2025.16214171621417Integrated analysis of electrical stimulation effects on Pseudomonas aeruginosa PAO1 inoculated denitrifying community: targeted and untargeted metabolomic analysis of phenazine biosynthesis and quorum sensingLi Wu0Li Wu1Yong Liu2Yong Liu3Jianping Deng4Jianping Deng5Shuanglin Gui6Shuanglin Gui7Hanbing Nie8Hanbing Nie9Jiangxi Provincial Key Laboratory of Greenhouse Gas Accounting and Carbon Reduction, Institute of Energy Research, Jiangxi Academy of Sciences, Nanchang, ChinaJiangxi Carbon Neutalization Research Center, Nanchang, ChinaJiangxi Provincial Key Laboratory of Greenhouse Gas Accounting and Carbon Reduction, Institute of Energy Research, Jiangxi Academy of Sciences, Nanchang, ChinaJiangxi Carbon Neutalization Research Center, Nanchang, ChinaJiangxi Provincial Key Laboratory of Greenhouse Gas Accounting and Carbon Reduction, Institute of Energy Research, Jiangxi Academy of Sciences, Nanchang, ChinaJiangxi Carbon Neutalization Research Center, Nanchang, ChinaJiangxi Provincial Key Laboratory of Greenhouse Gas Accounting and Carbon Reduction, Institute of Energy Research, Jiangxi Academy of Sciences, Nanchang, ChinaJiangxi Carbon Neutalization Research Center, Nanchang, ChinaJiangxi Provincial Key Laboratory of Greenhouse Gas Accounting and Carbon Reduction, Institute of Energy Research, Jiangxi Academy of Sciences, Nanchang, ChinaJiangxi Carbon Neutalization Research Center, Nanchang, ChinaThis study investigates how 0.8 V applied voltage modulates phenazine biosynthesis, quorum sensing (QS), and microbial interactions in Pseudomonas aeruginosa PAO1-inoculated microbial electrolysis cell (MEC) reactors. Voltage stimulation significantly enhanced phenazine derivatives (PYO: 8.65-fold; 1-OH-PHZ: 14.98-fold) and QS signals (C4-HSL: 2.88-fold; 3-OXO-C12-HSL: 2.21-fold), correlating with upregulated biosynthetic genes (phzG: 14.8-fold; rhlI: 15.2-fold). Electrical stimulation amplified QS cross-regulation, reinforcing Las-mediated positive feedback on Rhl/PQS systems while attenuating Rhl’s inhibition of PQS. Untargeted metabolomic analysis demonstrated significant alterations in bacterial metabolic activity under electrical stimulation, identifying 140 differential metabolites. Among these, indole, a signaling molecule with QS-like functionality, exhibited the highest VIP score as an upregulated metabolite, and another indole derivative, brassicanal A, was also elevated. KEGG pathway enrichment analysis highlighted that these metabolites were primarily associated with amino acid metabolism and transport, while anthranilic acid and L-tryptophan—key metabolites linked to both indole-related pathways and phenazine biosynthesis—were also identified. Correlation analysis between differential metabolites with microbial communities confirmed that Delftia and Burkholderiales were strongly associated with phenazine biosynthesis and QS activity in P. aeruginosa PAO1. These findings highlight voltage as a key driver of metabolic rewiring and microbial niche partitioning, optimizing MEC reactor performance for wastewater treatment. This work provides foundational insights into electro-stimulated biofilm engineering through targeted QS and metabolic pathway regulation.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1621417/fullPseudomonas aeruginosa PAO1quorum sensingphenazine derivativemicrobial electrolysis celluntargeted metabolomic analysis
spellingShingle Li Wu
Li Wu
Yong Liu
Yong Liu
Jianping Deng
Jianping Deng
Shuanglin Gui
Shuanglin Gui
Hanbing Nie
Hanbing Nie
Integrated analysis of electrical stimulation effects on Pseudomonas aeruginosa PAO1 inoculated denitrifying community: targeted and untargeted metabolomic analysis of phenazine biosynthesis and quorum sensing
Frontiers in Microbiology
Pseudomonas aeruginosa PAO1
quorum sensing
phenazine derivative
microbial electrolysis cell
untargeted metabolomic analysis
title Integrated analysis of electrical stimulation effects on Pseudomonas aeruginosa PAO1 inoculated denitrifying community: targeted and untargeted metabolomic analysis of phenazine biosynthesis and quorum sensing
title_full Integrated analysis of electrical stimulation effects on Pseudomonas aeruginosa PAO1 inoculated denitrifying community: targeted and untargeted metabolomic analysis of phenazine biosynthesis and quorum sensing
title_fullStr Integrated analysis of electrical stimulation effects on Pseudomonas aeruginosa PAO1 inoculated denitrifying community: targeted and untargeted metabolomic analysis of phenazine biosynthesis and quorum sensing
title_full_unstemmed Integrated analysis of electrical stimulation effects on Pseudomonas aeruginosa PAO1 inoculated denitrifying community: targeted and untargeted metabolomic analysis of phenazine biosynthesis and quorum sensing
title_short Integrated analysis of electrical stimulation effects on Pseudomonas aeruginosa PAO1 inoculated denitrifying community: targeted and untargeted metabolomic analysis of phenazine biosynthesis and quorum sensing
title_sort integrated analysis of electrical stimulation effects on pseudomonas aeruginosa pao1 inoculated denitrifying community targeted and untargeted metabolomic analysis of phenazine biosynthesis and quorum sensing
topic Pseudomonas aeruginosa PAO1
quorum sensing
phenazine derivative
microbial electrolysis cell
untargeted metabolomic analysis
url https://www.frontiersin.org/articles/10.3389/fmicb.2025.1621417/full
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