Omics and mechanistic insights into di-(2-ethylhexyl) phthalate degradation in the O2-fluctuating estuarine sediments

Di-(2-ethylhexyl) phthalate (DEHP) represents the most used phthalate plasticizer with an annual production above the millions of tons worldwide. Due to its inadequate disposal, outstanding chemical stability, and extremely low solubility (3 mg/L), endocrine-disrupting DEHP often accumulates in urba...

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Veröffentlicht in:Chemosphere (Oxford) 2022-07, Vol.299, p.134406-134406, Article 134406
Hauptverfasser: Wang, Po-Hsiang, Chen, Yi-Lung, Wu, Tien-Yu, Wu, Yu-Wei, Wang, Tzi-Yuan, Shih, Chao-Jen, Wei, Sean Ting-Shyang, Lai, Yi-Li, Liu, Cheng-Xuan, Chiang, Yin-Ru
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container_title Chemosphere (Oxford)
container_volume 299
creator Wang, Po-Hsiang
Chen, Yi-Lung
Wu, Tien-Yu
Wu, Yu-Wei
Wang, Tzi-Yuan
Shih, Chao-Jen
Wei, Sean Ting-Shyang
Lai, Yi-Li
Liu, Cheng-Xuan
Chiang, Yin-Ru
description Di-(2-ethylhexyl) phthalate (DEHP) represents the most used phthalate plasticizer with an annual production above the millions of tons worldwide. Due to its inadequate disposal, outstanding chemical stability, and extremely low solubility (3 mg/L), endocrine-disrupting DEHP often accumulates in urban estuarine sediments at concentrations above the predicted no-effect concentration (20–100 mg/kg). Our previous study suggested that microbial DEHP degradation in estuarine sediments proceeds synergistically where DEHP side-chain hydrolysis to form phthalic acid represents a bottleneck. Here, we resolved this bottleneck and deconstructed the microbial synergy in O2-fluctuating estuarine sediments. Metagenomic analysis and RNA sequencing suggested that orthologous genes encoding extracellular DEHP hydrolase NCU65476 in Acidovorax sp. strain 210-6 are often flanked by the co-expressed composite transposon and are widespread in aquatic environments worldwide. Therefore, we developed a turbidity-based microplate assay to characterize NCU65476. The optimized assay conditions (with 1 mM Ca2+ and pH 6.0) increased the DEHP hydrolysis rate by a factor of 10. Next, we isolated phthalic acid-degrading Hydrogenophaga spp. and Thauera chlorobenzoica from Guandu estuarine sediment to study the effect of O2(aq) on their metabolic synergy with strain 210-6. The results of co-culture experiments suggested that after DEHP side-chain hydrolysis by strain 210-6, phthalic acid can be degraded by Hydrogenophaga sp. when O2(aq) is above 1 mg/L or degraded by Thauera chlorobenzoica anaerobically. Altogether, our data demonstrates that DEHP could be degraded synergistically in estuarine sediments via divergent pathways responding to O2 availability. The optimized conditions for NCU65476 could facilitate the practice of DEHP bioremediation in estuarine sediments. [Display omitted] •New family of PAE hydrolases found to be present in aquatic environments worldwide.•Extracellular DEHP hydrolase NCU65476 hydrolyzes both PAE side-chains.•Characterizing optimal DEHP hydrolysis conditions via turbidity-based microplate assay.•Divergent DEHP degradation pathways operate in O2-fluctuating estuarine sediments.
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Due to its inadequate disposal, outstanding chemical stability, and extremely low solubility (3 mg/L), endocrine-disrupting DEHP often accumulates in urban estuarine sediments at concentrations above the predicted no-effect concentration (20–100 mg/kg). Our previous study suggested that microbial DEHP degradation in estuarine sediments proceeds synergistically where DEHP side-chain hydrolysis to form phthalic acid represents a bottleneck. Here, we resolved this bottleneck and deconstructed the microbial synergy in O2-fluctuating estuarine sediments. Metagenomic analysis and RNA sequencing suggested that orthologous genes encoding extracellular DEHP hydrolase NCU65476 in Acidovorax sp. strain 210-6 are often flanked by the co-expressed composite transposon and are widespread in aquatic environments worldwide. Therefore, we developed a turbidity-based microplate assay to characterize NCU65476. The optimized assay conditions (with 1 mM Ca2+ and pH 6.0) increased the DEHP hydrolysis rate by a factor of 10. Next, we isolated phthalic acid-degrading Hydrogenophaga spp. and Thauera chlorobenzoica from Guandu estuarine sediment to study the effect of O2(aq) on their metabolic synergy with strain 210-6. The results of co-culture experiments suggested that after DEHP side-chain hydrolysis by strain 210-6, phthalic acid can be degraded by Hydrogenophaga sp. when O2(aq) is above 1 mg/L or degraded by Thauera chlorobenzoica anaerobically. Altogether, our data demonstrates that DEHP could be degraded synergistically in estuarine sediments via divergent pathways responding to O2 availability. The optimized conditions for NCU65476 could facilitate the practice of DEHP bioremediation in estuarine sediments. 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Due to its inadequate disposal, outstanding chemical stability, and extremely low solubility (3 mg/L), endocrine-disrupting DEHP often accumulates in urban estuarine sediments at concentrations above the predicted no-effect concentration (20–100 mg/kg). Our previous study suggested that microbial DEHP degradation in estuarine sediments proceeds synergistically where DEHP side-chain hydrolysis to form phthalic acid represents a bottleneck. Here, we resolved this bottleneck and deconstructed the microbial synergy in O2-fluctuating estuarine sediments. Metagenomic analysis and RNA sequencing suggested that orthologous genes encoding extracellular DEHP hydrolase NCU65476 in Acidovorax sp. strain 210-6 are often flanked by the co-expressed composite transposon and are widespread in aquatic environments worldwide. Therefore, we developed a turbidity-based microplate assay to characterize NCU65476. The optimized assay conditions (with 1 mM Ca2+ and pH 6.0) increased the DEHP hydrolysis rate by a factor of 10. Next, we isolated phthalic acid-degrading Hydrogenophaga spp. and Thauera chlorobenzoica from Guandu estuarine sediment to study the effect of O2(aq) on their metabolic synergy with strain 210-6. The results of co-culture experiments suggested that after DEHP side-chain hydrolysis by strain 210-6, phthalic acid can be degraded by Hydrogenophaga sp. when O2(aq) is above 1 mg/L or degraded by Thauera chlorobenzoica anaerobically. Altogether, our data demonstrates that DEHP could be degraded synergistically in estuarine sediments via divergent pathways responding to O2 availability. The optimized conditions for NCU65476 could facilitate the practice of DEHP bioremediation in estuarine sediments. [Display omitted] •New family of PAE hydrolases found to be present in aquatic environments worldwide.•Extracellular DEHP hydrolase NCU65476 hydrolyzes both PAE side-chains.•Characterizing optimal DEHP hydrolysis conditions via turbidity-based microplate assay.•Divergent DEHP degradation pathways operate in O2-fluctuating estuarine sediments.</abstract><pub>Elsevier Ltd</pub><doi>10.1016/j.chemosphere.2022.134406</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-7791-8264</orcidid><orcidid>https://orcid.org/0000-0001-7840-7423</orcidid><orcidid>https://orcid.org/0000-0002-9170-8228</orcidid><orcidid>https://orcid.org/0000-0003-3783-6429</orcidid><orcidid>https://orcid.org/0000-0001-9900-0972</orcidid><orcidid>https://orcid.org/0000-0002-5603-1194</orcidid><oa>free_for_read</oa></addata></record>
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subjects Biodegradation
Bioremediation
Carboxylesterase
Estuarine sediment
Horizontal gene transfer
Phthalate ester
title Omics and mechanistic insights into di-(2-ethylhexyl) phthalate degradation in the O2-fluctuating estuarine sediments
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