Transition Metals and Organic Ligands Influence Biodegradation of 1,4-Dioxane

1,4-Dioxane, a contaminant increasingly detected in water supplies, is a public health concern because it is classified as a possible human carcinogen. 1,4-Dioxane can be biodegraded by aerobic bacteria via monooxygenase-catalyzed reactions. While these metalloenzymes require trace metals as cofacto...

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Published inApplied biochemistry and biotechnology Vol. 173; no. 1; pp. 291 - 306
Main Authors Pornwongthong, Peerapong, Mulchandani, Anjali, Gedalanga, Phillip B, Mahendra, Shaily
Format Journal Article
LanguageEnglish
Published Boston Springer-Verlag 01.05.2014
Springer US
Springer
Springer Nature B.V
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Abstract 1,4-Dioxane, a contaminant increasingly detected in water supplies, is a public health concern because it is classified as a possible human carcinogen. 1,4-Dioxane can be biodegraded by aerobic bacteria via monooxygenase-catalyzed reactions. While these metalloenzymes require trace metals as cofactors in their catalytic sites, these metals may be toxic at elevated concentrations. In this study, the effects of transition metals on 1,4-dioxane biodegradation by Pseudonocardia dioxanivorans CB1190, a monooxygenase-expressing bacterium, were investigated. Dose-dependent inhibition of 1,4-dioxane biodegradation by Cd(II), Cu(II), and Ni(II) was observed, whereas Zn(II) had no measurable effect on biodegradation rates. 1,4-Dioxane biodegradation in cultures exposed to 2 mg/L Cu(II) was restored in the presence of 0.005, 0.05, and 0.5 mM alginin, 0.05, and 0.5 mM cysteine, and 0.005 mM tannin. These results indicated that specific ligands bind with transition metals and alleviate bacterial toxicity. In parallel experiments, tannin and cysteine inhibited 1,4-dioxane biodegradation, but alginin, BSA, and SRNOM did not affect the biodegradation rates. Thus, monooxygenase-catalyzed biodegradation rates are subject to interactions among transition metals and natural organic ligands in the environment. Mechanistic insights and quantitative data obtained in this study will be useful for designing bioremediation strategies at sites simultaneously contaminated with metals and organic pollutants.
AbstractList 1,4-Dioxane, a contaminant increasingly detected in water supplies, is a public health concern because it is classified as a possible human carcinogen. 1,4-Dioxane can be biodegraded by aerobic bacteria via monooxygenase-catalyzed reactions. While these metalloenzymes require trace metals as cofactors in their catalytic sites, these metals may be toxic at elevated concentrations. In this study, the effects of transition metals on 1,4-dioxane biodegradation by Pseudonocardia dioxanivorans CB1190, a monooxygenase-expressing bacterium, were investigated. Dose-dependent inhibition of 1,4-dioxane biodegradation by Cd(II), Cu(II), and Ni(II) was observed, whereas Zn(II) had no measurable effect on biodegradation rates. 1,4-Dioxane biodegradation in cultures exposed to 2 mg/L Cu(II) was restored in the presence of 0.005, 0.05, and 0.5 mM alginin, 0.05, and 0.5 mM cysteine, and 0.005 mM tannin. These results indicated that specific ligands bind with transition metals and alleviate bacterial toxicity. In parallel experiments, tannin and cysteine inhibited 1,4-dioxane biodegradation, but alginin, BSA, and SRNOM did not affect the biodegradation rates. Thus, monooxygenase-catalyzed biodegradation rates are subject to interactions among transition metals and natural organic ligands in the environment. Mechanistic insights and quantitative data obtained in this study will be useful for designing bioremediation strategies at sites simultaneously contaminated with metals and organic pollutants.
1,4-Dioxane, a contaminant increasingly detected in water supplies, is a public health concern because it is classified as a possible human carcinogen. 1,4-Dioxane can be biodegraded by aerobic bacteria via monooxygenase-catalyzed reactions. While these metalloenzymes require trace metals as cofactors in their catalytic sites, these metals may be toxic at elevated concentrations. In this study, the effects of transition metals on 1,4-dioxane biodegradation by Pseudonocardia dioxanivorans CB1190, a monooxygenase-expressing bacterium, were investigated. Dose-dependent inhibition of 1,4-dioxane biodegradation by Cd(II), Cu(II), and Ni(II) was observed, whereas Zn(II) had no measurable effect on biodegradation rates. 1,4-Dioxane biodegradation in cultures exposed to 2 mg/L Cu(II) was restored in the presence of 0.005, 0.05, and 0.5 mM alginin, 0.05, and 0.5 mM cysteine, and 0.005 mM tannin. These results indicated that specific ligands bind with transition metals and alleviate bacterial toxicity. In parallel experiments, tannin and cysteine inhibited 1,4-dioxane biodegradation, but alginin, BSA, and SRNOM did not affect the biodegradation rates. Thus, monooxygenase-catalyzed biodegradation rates are subject to interactions among transition metals and natural organic ligands in the environment. Mechanistic insights and quantitative data obtained in this study will be useful for designing bioremediation strategies at sites simultaneously contaminated with metals and organic pollutants.1,4-Dioxane, a contaminant increasingly detected in water supplies, is a public health concern because it is classified as a possible human carcinogen. 1,4-Dioxane can be biodegraded by aerobic bacteria via monooxygenase-catalyzed reactions. While these metalloenzymes require trace metals as cofactors in their catalytic sites, these metals may be toxic at elevated concentrations. In this study, the effects of transition metals on 1,4-dioxane biodegradation by Pseudonocardia dioxanivorans CB1190, a monooxygenase-expressing bacterium, were investigated. Dose-dependent inhibition of 1,4-dioxane biodegradation by Cd(II), Cu(II), and Ni(II) was observed, whereas Zn(II) had no measurable effect on biodegradation rates. 1,4-Dioxane biodegradation in cultures exposed to 2 mg/L Cu(II) was restored in the presence of 0.005, 0.05, and 0.5 mM alginin, 0.05, and 0.5 mM cysteine, and 0.005 mM tannin. These results indicated that specific ligands bind with transition metals and alleviate bacterial toxicity. In parallel experiments, tannin and cysteine inhibited 1,4-dioxane biodegradation, but alginin, BSA, and SRNOM did not affect the biodegradation rates. Thus, monooxygenase-catalyzed biodegradation rates are subject to interactions among transition metals and natural organic ligands in the environment. Mechanistic insights and quantitative data obtained in this study will be useful for designing bioremediation strategies at sites simultaneously contaminated with metals and organic pollutants.
1,4-Dioxane, a contaminant increasingly detected in water supplies, is a public health concern because it is classified as a possible human carcinogen. 1,4-Dioxane can be biodegraded by aerobic bacteria via monooxygenase-catalyzed reactions. While these metalloenzymes require trace metals as cofactors in their catalytic sites, these metals may be toxic at elevated concentrations. In this study, the effects of transition metals on 1,4-dioxane biodegradation by Pseudonocardia dioxanivorans CB1190, a monooxygenase-expressing bacterium, were investigated. Dose-dependent inhibition of 1,4-dioxane biodegradation by Cd(II), Cu(II), and Ni(II) was observed, whereas Zn(II) had no measurable effect on biodegradation rates. 1,4-Dioxane biodegradation in cultures exposed to 2 mg/L Cu(II) was restored in the presence of 0.005, 0.05, and 0.5 mM alginin, 0.05, and 0.5 mM cysteine, and 0.005 mM tannin. These results indicated that specific ligands bind with transition metals and alleviate bacterial toxicity. In parallel experiments, tannin and cysteine inhibited 1,4-dioxane biodegradation, but alginin, BSA, and SRNOM did not affect the biodegradation rates. Thus, monooxygenase-catalyzed biodegradation rates are subject to interactions among transition metals and natural organic ligands in the environment. Mechanistic insights and quantitative data obtained in this study will be useful for designing bioremediation strategies at sites simultaneously contaminated with metals and organic pollutants.
1,4-Dioxane, a contaminant increasingly detected in water supplies, is a public health concern because it is classified as a possible human carcinogen. 1,4-Dioxane can be biodegraded by aerobic bacteria via monooxygenase-catalyzed reactions. While these metalloenzymes require trace metals as cofactors in their catalytic sites, these metals may be toxic at elevated concentrations. In this study, the effects of transition metals on 1,4-dioxane biodegradation by Pseudonocardia dioxanivorans CB1190, a monooxygenase-expressing bacterium, were investigated. Dose-dependent inhibition of 1,4-dioxane biodegradation by Cd(II), Cu(II), and Ni(II) was observed, whereas Zn(II) had no measurable effect on biodegradation rates. 1,4-Dioxane biodegradation in cultures exposed to 2 mg/L Cu(II) was restored in the presence of 0.005, 0.05, and 0.5 mM alginin, 0.05, and 0.5 mM cysteine, and 0.005 mM tannin. These results indicated that specific ligands bind with transition metals and alleviate bacterial toxicity. In parallel experiments, tannin and cysteine inhibited 1,4-dioxane biodegradation, but alginin, BSA, and SRNOM did not affect the biodegradation rates. Thus, monooxygenase-catalyzed biodegradation rates are subject to interactions among transition metals and natural organic ligands in the environment. Mechanistic insights and quantitative data obtained in this study will be useful for designing bioremediation strategies at sites simultaneously contaminated with metals and organic pollutants.[PUBLICATION ABSTRACT]
1,4-Dioxane, a contaminant increasingly detected in water supplies, is a public health concern because it is classified as a possible human carcinogen. 1,4-Dioxane can be biodegraded by aerobic bacteria via monooxygenase-catalyzed reactions. While these metalloenzymes require trace metals as cofactors in their catalytic sites, these metals may be toxic at elevated concentrations. In this study, the effects of transition metals on 1,4-dioxane biodegradation by Pseudonocardia dioxanivorans CB1190, a monooxygenase-expressing bacterium, were investigated. Dose-dependent inhibition of 1,4-dioxane biodegradation by Cd(II), Cu(II), and Ni(II) was observed, whereas Zn(II) had no measurable effect on biodegradation rates. 1,4-Dioxane biodegradation in cultures exposed to 2 mg/L Cu(II) was restored in the presence of 0.005, 0.05, and 0.5 mM alginin, 0.05, and 0.5 mM cysteine, and 0.005 mM tannin. These results indicated that specific ligands bind with transition metals and alleviate bacterial toxicity. In parallel experiments, tannin and cysteine inhibited 1,4-dioxane biodegradation, but alginin, BSA, and SRNOM did not affect the biodegradation rates. Thus, monooxygenase-catalyzed biodegradation rates are subject to interactions among transition metals and natural organic ligands in the environment. Mechanistic insights and quantitative data obtained in this study will be useful for designing bioremediation strategies at sites simultaneously contaminated with metals and organic pollutants.
Author Pornwongthong, Peerapong
Gedalanga, Phillip B
Mulchandani, Anjali
Mahendra, Shaily
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ISSN 0273-2289
1559-0291
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IsPeerReviewed true
IsScholarly true
Issue 1
Keywords Oxygenase
Dioxane
Bioavailable
Biotransformation
Metal resistance
Metal–ligand complex
Trace metals
Bioavailability
Natural organic matter
NOM
Co-contaminants
Metal ions
Biodegradation
Organic matter
Enzyme
Ligand
Metal ion
Metal
Complexes
Resistance
Oxidoreductases
Metal―ligand complex
Contaminant
Language English
License http://www.springer.com/tdm
CC BY 4.0
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ObjectType-Feature-1
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content type line 23
PMID 24627120
PQID 1520289319
PQPubID 54110
PageCount 16
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proquest_miscellaneous_1521325938
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crossref_citationtrail_10_1007_s12010_014_0841_2
crossref_primary_10_1007_s12010_014_0841_2
springer_journals_10_1007_s12010_014_0841_2
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  year: 2014
  text: 2014-05-01
  day: 01
PublicationDecade 2010
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PublicationSubtitle Part A: Enzyme Engineering and Biotechnology
PublicationTitle Applied biochemistry and biotechnology
PublicationTitleAbbrev Appl Biochem Biotechnol
PublicationTitleAlternate Appl Biochem Biotechnol
PublicationYear 2014
Publisher Springer-Verlag
Springer US
Springer
Springer Nature B.V
Publisher_xml – name: Springer-Verlag
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– reference: DiSpiritoAAZahnJAGrahamDWKimHJLariveCKDerrickTSCopper-binding compounds from Methylosinus trichosporium OB3bJournal of Bacteriology1998180360636131:CAS:528:DyaK1cXks1egt7k%3D
– reference: LinC-WChenS-YChengY-WEffect of metals on biodegradation kinetics for methyl tert-butyl etherBiochemical Engineering Journal20063225321:CAS:528:DC%2BD28XhtVygt7nP10.1016/j.bej.2006.07.010
– reference: MinBRAttwoodGTReillyKSunWPetersJSBarryTNLotus corniculatus condensed tannins decrease in vivo populations of proteolytic bacteria and affect nitrogen metabolism in the rumen of sheepCanadian Journal of Microbiology2002489119211:CAS:528:DC%2BD38XpsFOqurk%3D10.1139/w02-087
– reference: RiisVBabelWPucciOHInfluence of heavy metals on the microbial degradation of diesel fuelChemosphere2002495595681:CAS:528:DC%2BD38Xnt1Crtrs%3D10.1016/S0045-6535(02)00386-7
– reference: ShuttleworthKLUnzRFGrowth of filamentous bacteria in the presence of heavy metalsWater Science and Technology1988204854871:CAS:528:DyaL1MXktFajs7s%3D
– reference: KelleySLAitchisonEWDeshpandeMSchnoorJLAlvarezPJJBiodegradation of 1,4-dioxane in planted and unplanted soil: effect of bioaugmentation with Amycolata sp. CB1190Water Research200135379138001:CAS:528:DC%2BD3MXms1Crt7k%3D10.1016/S0043-1354(01)00129-4
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– reference: HarrisCLCysteine and growth inhibition of Escherichia coli: threonine deaminase as the target enzymeJournal of Bacteriology1981145103110351:CAS:528:DyaL3MXhtFOks7k%3D
– reference: AbeADistribution of 1,4-dioxane in relation to possible sources in the water environmentScience of the Total Environment199922741471:CAS:528:DyaK1MXhsVemu7w%3D10.1016/S0048-9697(99)00003-0
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– reference: BhuvaneswaranCSreenivasanARegeDVEffect of cysteine on respiration and catalyse synthesis by Saccharomyces cerevisiaeBiochemistry Journal1964925045081:CAS:528:DyaF2cXksV2lt7g%3D
– reference: NakajimaATanakaMKameshimaYOkadaKSonophotocatalytic destruction of 1,4-dioxane in aqueous systems by HF-treated TiO2 powderJournal of Photochemistry and Photobiology A: Chemistry200416775791:CAS:528:DC%2BD2cXnt1Kiu7Y%3D10.1016/j.jphotochem.2004.04.013
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– reference: NiesDHMicrobial heavy-metal resistanceApplied Microbiology and Biotechnology1999517307501:CAS:528:DyaK1MXks1OhtLY%3D10.1007/s002530051457
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Snippet 1,4-Dioxane, a contaminant increasingly detected in water supplies, is a public health concern because it is classified as a possible human carcinogen....
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StartPage 291
SubjectTerms Actinomycetales - metabolism
Aerobic bacteria
bacteria
Bioavailability
Biochemistry
Bioconversions. Hemisynthesis
Biodegradation
Biodegradation, Environmental
Biological and medical sciences
Bioremediation
Biotechnology
cadmium
Chemistry
Chemistry and Materials Science
Contaminants
Copper
cysteine
Dioxanes - chemistry
Dioxanes - metabolism
Fundamental and applied biological sciences. Psychology
Ions
Metal concentrations
Metals
Metals - chemistry
Metals - metabolism
Methods. Procedures. Technologies
Nickel
pollutants
Pseudonocardia
Public health
Tannins
toxicity
Trace elements
Trace metals
Water Pollutants, Chemical - chemistry
Water Pollutants, Chemical - metabolism
Water supply
zinc
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Title Transition Metals and Organic Ligands Influence Biodegradation of 1,4-Dioxane
URI https://link.springer.com/article/10.1007/s12010-014-0841-2
https://www.ncbi.nlm.nih.gov/pubmed/24627120
https://www.proquest.com/docview/1520289319
https://www.proquest.com/docview/1521325938
https://www.proquest.com/docview/1524408445
https://www.proquest.com/docview/1999964853
Volume 173
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