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Cometabolic biotransformation of 1,4-dioxane in mixtures with hexavalent chromium using attached and planktonic bacteria
Biological treatment of 1,4-dioxane, a probable human carcinogen and a recalcitrant contaminant of concern, is often complicated by the presence of inhibitory co-contaminants. Due to its use as a solvent, wetting agent, and stabilizer for chlorinated solvents employed in metal vapor degreasing, 1,4-...
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Published in: | The Science of the total environment 2020-03, Vol.706, p.135734, Article 135734 |
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description | Biological treatment of 1,4-dioxane, a probable human carcinogen and a recalcitrant contaminant of concern, is often complicated by the presence of inhibitory co-contaminants. Due to its use as a solvent, wetting agent, and stabilizer for chlorinated solvents employed in metal vapor degreasing, 1,4-dioxane has often been found to occur with a variety of co-contaminants, including heavy metals such as hexavalent chromium [Cr(VI)]. Cr(VI) also occurs naturally in groundwater due to geological formations, but also has sources that can coincide with 1,4-dioxane from anthropogenic activities such as metal vapor degreasing. Biodegradation of 1,4-dioxane can be accomplished by microbes that use it as a source of carbon or energy as well as those that cometabolize it after growth on other organic substrates. A propanotroph, Mycobacterium austroafricanum JOB5, was grown in planktonic pure cultures and biofilms to determine its ability to cometabolize 1,4-dioxane in the presence of varying concentrations of Cr(VI). 1,4-Dioxane cometabolism by JOB5 planktonic cells was uninhibited by Cr(VI) at levels up to 10 mg/L, while biofilms were only mildly inhibited at 10 mg/L. As an important part of the biofilms commonly found in subsurface aquifers and engineered systems, extracellular polymeric substances (EPS) were found to play an important role in preventing Cr(VI) exposure to cells. We observed that soluble EPS were able to bind to Cr(VI) and theorize that biofilm-associated EPS additionally served to impede penetration of the biofilm structure by Cr(VI), thus mitigating exposure and toxicity. These findings suggest that bioremediation would be a viable treatment strategy for 1,4-dioxane-contaminated waters that contain elevated levels of Cr(VI) in natural and built environments.
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•1,4-Dioxane (1,4-DX) & Cr(VI) potentially co-occur in contaminated groundwater.•JOB5 planktonic cells and biofilms degraded 1,4-DX even in the presence of Cr(VI).•Biodegradation rates were 103–105 times lower in biofilms than in planktonic cells.•Exopolysaccharides (EPS) mitigate Cr(VI) inhibition of 1,4-DX cometabolism.•1,4-DX can be successfully biodegraded even in the presence of Cr(VI) in water. |
doi_str_mv | 10.1016/j.scitotenv.2019.135734 |
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[Display omitted]
•1,4-Dioxane (1,4-DX) & Cr(VI) potentially co-occur in contaminated groundwater.•JOB5 planktonic cells and biofilms degraded 1,4-DX even in the presence of Cr(VI).•Biodegradation rates were 103–105 times lower in biofilms than in planktonic cells.•Exopolysaccharides (EPS) mitigate Cr(VI) inhibition of 1,4-DX cometabolism.•1,4-DX can be successfully biodegraded even in the presence of Cr(VI) in water.</description><identifier>ISSN: 0048-9697</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2019.135734</identifier><identifier>PMID: 31806311</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Bacteria ; Biodegradation, Environmental ; Biotransformation ; Chromium ; Cyclic ether ; Dichromate ; Dioxanes ; Exopolysaccharides ; Oxyanion ; Plankton ; Transition metal ; Water Pollutants, Chemical</subject><ispartof>The Science of the total environment, 2020-03, Vol.706, p.135734, Article 135734</ispartof><rights>2018 Elsevier B.V.</rights><rights>Copyright © 2018 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c420t-2077fc539e68e91580c8c7de3a5515a6f189789ce428630c1f568be0231c519d3</citedby><cites>FETCH-LOGICAL-c420t-2077fc539e68e91580c8c7de3a5515a6f189789ce428630c1f568be0231c519d3</cites><orcidid>0000-0003-3298-9602 ; 0000-0002-7299-2956</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31806311$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Johnson, Nicholas W.</creatorcontrib><creatorcontrib>Gedalanga, Phillip B.</creatorcontrib><creatorcontrib>Zhao, Linduo</creatorcontrib><creatorcontrib>Gu, Baohua</creatorcontrib><creatorcontrib>Mahendra, Shaily</creatorcontrib><title>Cometabolic biotransformation of 1,4-dioxane in mixtures with hexavalent chromium using attached and planktonic bacteria</title><title>The Science of the total environment</title><addtitle>Sci Total Environ</addtitle><description>Biological treatment of 1,4-dioxane, a probable human carcinogen and a recalcitrant contaminant of concern, is often complicated by the presence of inhibitory co-contaminants. Due to its use as a solvent, wetting agent, and stabilizer for chlorinated solvents employed in metal vapor degreasing, 1,4-dioxane has often been found to occur with a variety of co-contaminants, including heavy metals such as hexavalent chromium [Cr(VI)]. Cr(VI) also occurs naturally in groundwater due to geological formations, but also has sources that can coincide with 1,4-dioxane from anthropogenic activities such as metal vapor degreasing. Biodegradation of 1,4-dioxane can be accomplished by microbes that use it as a source of carbon or energy as well as those that cometabolize it after growth on other organic substrates. A propanotroph, Mycobacterium austroafricanum JOB5, was grown in planktonic pure cultures and biofilms to determine its ability to cometabolize 1,4-dioxane in the presence of varying concentrations of Cr(VI). 1,4-Dioxane cometabolism by JOB5 planktonic cells was uninhibited by Cr(VI) at levels up to 10 mg/L, while biofilms were only mildly inhibited at 10 mg/L. As an important part of the biofilms commonly found in subsurface aquifers and engineered systems, extracellular polymeric substances (EPS) were found to play an important role in preventing Cr(VI) exposure to cells. We observed that soluble EPS were able to bind to Cr(VI) and theorize that biofilm-associated EPS additionally served to impede penetration of the biofilm structure by Cr(VI), thus mitigating exposure and toxicity. These findings suggest that bioremediation would be a viable treatment strategy for 1,4-dioxane-contaminated waters that contain elevated levels of Cr(VI) in natural and built environments.
[Display omitted]
•1,4-Dioxane (1,4-DX) & Cr(VI) potentially co-occur in contaminated groundwater.•JOB5 planktonic cells and biofilms degraded 1,4-DX even in the presence of Cr(VI).•Biodegradation rates were 103–105 times lower in biofilms than in planktonic cells.•Exopolysaccharides (EPS) mitigate Cr(VI) inhibition of 1,4-DX cometabolism.•1,4-DX can be successfully biodegraded even in the presence of Cr(VI) in water.</description><subject>Bacteria</subject><subject>Biodegradation, Environmental</subject><subject>Biotransformation</subject><subject>Chromium</subject><subject>Cyclic ether</subject><subject>Dichromate</subject><subject>Dioxanes</subject><subject>Exopolysaccharides</subject><subject>Oxyanion</subject><subject>Plankton</subject><subject>Transition metal</subject><subject>Water Pollutants, Chemical</subject><issn>0048-9697</issn><issn>1879-1026</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNqFkMtOwzAQRS0EoqXwC-APIMUTJ7G9rCpeEhIbWEeOM6EujV3Zbil_T6tAt8zmbu5jdAi5ATYFBtXdchqNTT6h205zBmoKvBS8OCFjkEJlwPLqlIwZK2SmKiVG5CLGJdufkHBORhwkqzjAmOzmvsekG7-yhjbWp6Bd7HzodbLeUd9RuC2y1vqddkito73dpU3ASL9sWtAF7vRWr9AlahbB93bT00207oPqlLRZYEu1a-l6pd1n8u6woU3CYPUlOev0KuLVr07I-8P92_wpe3l9fJ7PXjJT5CxlOROiMyVXWElUUEpmpBEtcl2WUOqqA6mEVAaLXFacGejKSjbIcg6mBNXyCRFDrwk-xoBdvQ621-G7BlYfWNbL-siyPrCsB5b75PWQXG-aHttj7g_e3jAbDLj_f2sxHIrQGWxtQJPq1tt_R34A-D6MFg</recordid><startdate>20200301</startdate><enddate>20200301</enddate><creator>Johnson, Nicholas W.</creator><creator>Gedalanga, Phillip B.</creator><creator>Zhao, Linduo</creator><creator>Gu, Baohua</creator><creator>Mahendra, Shaily</creator><general>Elsevier B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><orcidid>https://orcid.org/0000-0003-3298-9602</orcidid><orcidid>https://orcid.org/0000-0002-7299-2956</orcidid></search><sort><creationdate>20200301</creationdate><title>Cometabolic biotransformation of 1,4-dioxane in mixtures with hexavalent chromium using attached and planktonic bacteria</title><author>Johnson, Nicholas W. ; Gedalanga, Phillip B. ; Zhao, Linduo ; Gu, Baohua ; Mahendra, Shaily</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c420t-2077fc539e68e91580c8c7de3a5515a6f189789ce428630c1f568be0231c519d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Bacteria</topic><topic>Biodegradation, Environmental</topic><topic>Biotransformation</topic><topic>Chromium</topic><topic>Cyclic ether</topic><topic>Dichromate</topic><topic>Dioxanes</topic><topic>Exopolysaccharides</topic><topic>Oxyanion</topic><topic>Plankton</topic><topic>Transition metal</topic><topic>Water Pollutants, Chemical</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Johnson, Nicholas W.</creatorcontrib><creatorcontrib>Gedalanga, Phillip B.</creatorcontrib><creatorcontrib>Zhao, Linduo</creatorcontrib><creatorcontrib>Gu, Baohua</creatorcontrib><creatorcontrib>Mahendra, Shaily</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><jtitle>The Science of the total environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Johnson, Nicholas W.</au><au>Gedalanga, Phillip B.</au><au>Zhao, Linduo</au><au>Gu, Baohua</au><au>Mahendra, Shaily</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cometabolic biotransformation of 1,4-dioxane in mixtures with hexavalent chromium using attached and planktonic bacteria</atitle><jtitle>The Science of the total environment</jtitle><addtitle>Sci Total Environ</addtitle><date>2020-03-01</date><risdate>2020</risdate><volume>706</volume><spage>135734</spage><pages>135734-</pages><artnum>135734</artnum><issn>0048-9697</issn><eissn>1879-1026</eissn><abstract>Biological treatment of 1,4-dioxane, a probable human carcinogen and a recalcitrant contaminant of concern, is often complicated by the presence of inhibitory co-contaminants. Due to its use as a solvent, wetting agent, and stabilizer for chlorinated solvents employed in metal vapor degreasing, 1,4-dioxane has often been found to occur with a variety of co-contaminants, including heavy metals such as hexavalent chromium [Cr(VI)]. Cr(VI) also occurs naturally in groundwater due to geological formations, but also has sources that can coincide with 1,4-dioxane from anthropogenic activities such as metal vapor degreasing. Biodegradation of 1,4-dioxane can be accomplished by microbes that use it as a source of carbon or energy as well as those that cometabolize it after growth on other organic substrates. A propanotroph, Mycobacterium austroafricanum JOB5, was grown in planktonic pure cultures and biofilms to determine its ability to cometabolize 1,4-dioxane in the presence of varying concentrations of Cr(VI). 1,4-Dioxane cometabolism by JOB5 planktonic cells was uninhibited by Cr(VI) at levels up to 10 mg/L, while biofilms were only mildly inhibited at 10 mg/L. As an important part of the biofilms commonly found in subsurface aquifers and engineered systems, extracellular polymeric substances (EPS) were found to play an important role in preventing Cr(VI) exposure to cells. We observed that soluble EPS were able to bind to Cr(VI) and theorize that biofilm-associated EPS additionally served to impede penetration of the biofilm structure by Cr(VI), thus mitigating exposure and toxicity. These findings suggest that bioremediation would be a viable treatment strategy for 1,4-dioxane-contaminated waters that contain elevated levels of Cr(VI) in natural and built environments.
[Display omitted]
•1,4-Dioxane (1,4-DX) & Cr(VI) potentially co-occur in contaminated groundwater.•JOB5 planktonic cells and biofilms degraded 1,4-DX even in the presence of Cr(VI).•Biodegradation rates were 103–105 times lower in biofilms than in planktonic cells.•Exopolysaccharides (EPS) mitigate Cr(VI) inhibition of 1,4-DX cometabolism.•1,4-DX can be successfully biodegraded even in the presence of Cr(VI) in water.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>31806311</pmid><doi>10.1016/j.scitotenv.2019.135734</doi><orcidid>https://orcid.org/0000-0003-3298-9602</orcidid><orcidid>https://orcid.org/0000-0002-7299-2956</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bacteria Biodegradation, Environmental Biotransformation Chromium Cyclic ether Dichromate Dioxanes Exopolysaccharides Oxyanion Plankton Transition metal Water Pollutants, Chemical |
title | Cometabolic biotransformation of 1,4-dioxane in mixtures with hexavalent chromium using attached and planktonic bacteria |
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