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Ferroptosis is the key cellular process mediating Bisphenol A responses in Chlamydomonas and a promising target for enhancing microalgae-based bioremediation
Microplastics are one of the major pollutants in aquatic environments. Among their components, Bisphenol A (BPA) is one of the most abundant and dangerous, leading to endocrine disorders deriving even in different types of cancer in mammals. However, despite this evidence, the xenobiotic effects of...
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Published in: | Journal of hazardous materials 2023-04, Vol.448, p.130997-130997, Article 130997 |
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creator | Carbó, María Chaturvedi, Palak Álvarez, Ana Pineda-Cevallos, Daniela Ghatak, Arindam González, Pablo Rodríguez Cañal, María Jesús Weckwerth, Wolfram Valledor, Luis |
description | Microplastics are one of the major pollutants in aquatic environments. Among their components, Bisphenol A (BPA) is one of the most abundant and dangerous, leading to endocrine disorders deriving even in different types of cancer in mammals. However, despite this evidence, the xenobiotic effects of BPA over plantae and microalgae still need to be better understood at the molecular level. To fill this gap, we characterized the physiological and proteomic response of Chlamydomonas reinhardtii during long-term BPA exposure by analyzing physiological and biochemical parameters combined with proteomics. BPA imbalanced iron and redox homeostasis, disrupting cell function and triggering ferroptosis. Intriguingly, this microalgae defense against this pollutant is recovering at both molecular and physiological levels while starch accumulation at 72 h of BPA exposure. In this work, we addressed the molecular mechanisms involved in BPA exposure, demonstrating for the first time the induction of ferroptosis in a eukaryotic alga and how ROS detoxification mechanisms and other specific proteomic rearrangements reverted this situation. These results are of great significance not only for understanding the BPA toxicology or exploring the molecular mechanisms of ferroptosis in microalgae but also for defining novel target genes for microplastic bioremediation efficient strain development.
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•Chlamydomonas can bioaccumulate significant amounts of Bisphenol A (BPA).•BPA induced quick oxidative damage in Chlamydomonas, which reverted after 72 h.•Proteomics revealed the mechanisms involved in BPA detoxification.•Among them, ferroptosis was the key pathway involved in the initial detoxification.•Ferroptosis was described for the first time in microalgae and response to BPA. |
doi_str_mv | 10.1016/j.jhazmat.2023.130997 |
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[Display omitted]
•Chlamydomonas can bioaccumulate significant amounts of Bisphenol A (BPA).•BPA induced quick oxidative damage in Chlamydomonas, which reverted after 72 h.•Proteomics revealed the mechanisms involved in BPA detoxification.•Among them, ferroptosis was the key pathway involved in the initial detoxification.•Ferroptosis was described for the first time in microalgae and response to BPA.</description><identifier>ISSN: 0304-3894</identifier><identifier>EISSN: 1873-3336</identifier><identifier>DOI: 10.1016/j.jhazmat.2023.130997</identifier><identifier>PMID: 36860062</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Animals ; Biodegradation, Environmental ; BPA ; Chlamydomonas ; Chloroplast ; Environmental Pollutants ; Ferroptosis ; Mammals ; Microalgae ; Microplastics ; Mitochondria ; Plastics ; Proteomics ; Reactive Oxygen Species (ROS) ; Xenobiotics</subject><ispartof>Journal of hazardous materials, 2023-04, Vol.448, p.130997-130997, Article 130997</ispartof><rights>2023 The Authors</rights><rights>Copyright © 2023 The Authors. Published by Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c342t-28e20daf88bc4ff3d8128e2d7002cfad25422dfa81df66cd938bdccd7bae59c53</citedby><cites>FETCH-LOGICAL-c342t-28e20daf88bc4ff3d8128e2d7002cfad25422dfa81df66cd938bdccd7bae59c53</cites><orcidid>0000-0002-8217-9264 ; 0000-0003-1905-3922 ; 0000-0002-9719-6358 ; 0000-0002-1830-3056 ; 0000-0003-4706-9841 ; 0000-0002-1639-9672 ; 0000-0002-0636-365X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36860062$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Carbó, María</creatorcontrib><creatorcontrib>Chaturvedi, Palak</creatorcontrib><creatorcontrib>Álvarez, Ana</creatorcontrib><creatorcontrib>Pineda-Cevallos, Daniela</creatorcontrib><creatorcontrib>Ghatak, Arindam</creatorcontrib><creatorcontrib>González, Pablo Rodríguez</creatorcontrib><creatorcontrib>Cañal, María Jesús</creatorcontrib><creatorcontrib>Weckwerth, Wolfram</creatorcontrib><creatorcontrib>Valledor, Luis</creatorcontrib><title>Ferroptosis is the key cellular process mediating Bisphenol A responses in Chlamydomonas and a promising target for enhancing microalgae-based bioremediation</title><title>Journal of hazardous materials</title><addtitle>J Hazard Mater</addtitle><description>Microplastics are one of the major pollutants in aquatic environments. Among their components, Bisphenol A (BPA) is one of the most abundant and dangerous, leading to endocrine disorders deriving even in different types of cancer in mammals. However, despite this evidence, the xenobiotic effects of BPA over plantae and microalgae still need to be better understood at the molecular level. To fill this gap, we characterized the physiological and proteomic response of Chlamydomonas reinhardtii during long-term BPA exposure by analyzing physiological and biochemical parameters combined with proteomics. BPA imbalanced iron and redox homeostasis, disrupting cell function and triggering ferroptosis. Intriguingly, this microalgae defense against this pollutant is recovering at both molecular and physiological levels while starch accumulation at 72 h of BPA exposure. In this work, we addressed the molecular mechanisms involved in BPA exposure, demonstrating for the first time the induction of ferroptosis in a eukaryotic alga and how ROS detoxification mechanisms and other specific proteomic rearrangements reverted this situation. These results are of great significance not only for understanding the BPA toxicology or exploring the molecular mechanisms of ferroptosis in microalgae but also for defining novel target genes for microplastic bioremediation efficient strain development.
[Display omitted]
•Chlamydomonas can bioaccumulate significant amounts of Bisphenol A (BPA).•BPA induced quick oxidative damage in Chlamydomonas, which reverted after 72 h.•Proteomics revealed the mechanisms involved in BPA detoxification.•Among them, ferroptosis was the key pathway involved in the initial detoxification.•Ferroptosis was described for the first time in microalgae and response to BPA.</description><subject>Animals</subject><subject>Biodegradation, Environmental</subject><subject>BPA</subject><subject>Chlamydomonas</subject><subject>Chloroplast</subject><subject>Environmental Pollutants</subject><subject>Ferroptosis</subject><subject>Mammals</subject><subject>Microalgae</subject><subject>Microplastics</subject><subject>Mitochondria</subject><subject>Plastics</subject><subject>Proteomics</subject><subject>Reactive Oxygen Species (ROS)</subject><subject>Xenobiotics</subject><issn>0304-3894</issn><issn>1873-3336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNqFUcuO1DAQtBCIHXb5BJCPXDL4kYdzQsuIXZBW4sKerY7dmXhI7GBnVhr-hX9dRzNwRWqppVZVV3UXIe8423LG64-H7WGA3xMsW8GE3HLJ2rZ5QTZcNbKQUtYvyYZJVhZSteUVeZPSgTHGm6p8Ta5krWrGarEhf-4wxjAvIblEcy0D0p94ogbH8ThCpHMMBlOiE1oHi_N7-tmleUAfRnpLI6Y5-ISZ6-luGGE62TAFD4mCtxRW-uTSSlsg7nGhfYgU_QDerMPJmRhg3AMWHSS0tHMh4kUr-Bvyqocx4dtLvyaPd19-7L4WD9_vv-1uHwojS7EUQqFgFnqlOlP2vbSKryPbMCZMD1ZUpRC2B8VtX9fGtlJ11hjbdIBVayp5TT6c92a7v46YFp1Nry8Aj-GYtGgUr0VZqRVanaHZeEoRez1HN0E8ac70mow-6Esyek1Gn5PJvPcXiWOX7_vH-htFBnw6AzAf-uQw6mQcepN_EdEs2gb3H4lnxc6nRA</recordid><startdate>20230415</startdate><enddate>20230415</enddate><creator>Carbó, María</creator><creator>Chaturvedi, Palak</creator><creator>Álvarez, Ana</creator><creator>Pineda-Cevallos, Daniela</creator><creator>Ghatak, Arindam</creator><creator>González, Pablo Rodríguez</creator><creator>Cañal, María Jesús</creator><creator>Weckwerth, Wolfram</creator><creator>Valledor, Luis</creator><general>Elsevier B.V</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-8217-9264</orcidid><orcidid>https://orcid.org/0000-0003-1905-3922</orcidid><orcidid>https://orcid.org/0000-0002-9719-6358</orcidid><orcidid>https://orcid.org/0000-0002-1830-3056</orcidid><orcidid>https://orcid.org/0000-0003-4706-9841</orcidid><orcidid>https://orcid.org/0000-0002-1639-9672</orcidid><orcidid>https://orcid.org/0000-0002-0636-365X</orcidid></search><sort><creationdate>20230415</creationdate><title>Ferroptosis is the key cellular process mediating Bisphenol A responses in Chlamydomonas and a promising target for enhancing microalgae-based bioremediation</title><author>Carbó, María ; Chaturvedi, Palak ; Álvarez, Ana ; Pineda-Cevallos, Daniela ; Ghatak, Arindam ; González, Pablo Rodríguez ; Cañal, María Jesús ; Weckwerth, Wolfram ; Valledor, Luis</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c342t-28e20daf88bc4ff3d8128e2d7002cfad25422dfa81df66cd938bdccd7bae59c53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animals</topic><topic>Biodegradation, Environmental</topic><topic>BPA</topic><topic>Chlamydomonas</topic><topic>Chloroplast</topic><topic>Environmental Pollutants</topic><topic>Ferroptosis</topic><topic>Mammals</topic><topic>Microalgae</topic><topic>Microplastics</topic><topic>Mitochondria</topic><topic>Plastics</topic><topic>Proteomics</topic><topic>Reactive Oxygen Species (ROS)</topic><topic>Xenobiotics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Carbó, María</creatorcontrib><creatorcontrib>Chaturvedi, Palak</creatorcontrib><creatorcontrib>Álvarez, Ana</creatorcontrib><creatorcontrib>Pineda-Cevallos, Daniela</creatorcontrib><creatorcontrib>Ghatak, Arindam</creatorcontrib><creatorcontrib>González, Pablo Rodríguez</creatorcontrib><creatorcontrib>Cañal, María Jesús</creatorcontrib><creatorcontrib>Weckwerth, Wolfram</creatorcontrib><creatorcontrib>Valledor, Luis</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of hazardous materials</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Carbó, María</au><au>Chaturvedi, Palak</au><au>Álvarez, Ana</au><au>Pineda-Cevallos, Daniela</au><au>Ghatak, Arindam</au><au>González, Pablo Rodríguez</au><au>Cañal, María Jesús</au><au>Weckwerth, Wolfram</au><au>Valledor, Luis</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ferroptosis is the key cellular process mediating Bisphenol A responses in Chlamydomonas and a promising target for enhancing microalgae-based bioremediation</atitle><jtitle>Journal of hazardous materials</jtitle><addtitle>J Hazard Mater</addtitle><date>2023-04-15</date><risdate>2023</risdate><volume>448</volume><spage>130997</spage><epage>130997</epage><pages>130997-130997</pages><artnum>130997</artnum><issn>0304-3894</issn><eissn>1873-3336</eissn><abstract>Microplastics are one of the major pollutants in aquatic environments. Among their components, Bisphenol A (BPA) is one of the most abundant and dangerous, leading to endocrine disorders deriving even in different types of cancer in mammals. However, despite this evidence, the xenobiotic effects of BPA over plantae and microalgae still need to be better understood at the molecular level. To fill this gap, we characterized the physiological and proteomic response of Chlamydomonas reinhardtii during long-term BPA exposure by analyzing physiological and biochemical parameters combined with proteomics. BPA imbalanced iron and redox homeostasis, disrupting cell function and triggering ferroptosis. Intriguingly, this microalgae defense against this pollutant is recovering at both molecular and physiological levels while starch accumulation at 72 h of BPA exposure. In this work, we addressed the molecular mechanisms involved in BPA exposure, demonstrating for the first time the induction of ferroptosis in a eukaryotic alga and how ROS detoxification mechanisms and other specific proteomic rearrangements reverted this situation. These results are of great significance not only for understanding the BPA toxicology or exploring the molecular mechanisms of ferroptosis in microalgae but also for defining novel target genes for microplastic bioremediation efficient strain development.
[Display omitted]
•Chlamydomonas can bioaccumulate significant amounts of Bisphenol A (BPA).•BPA induced quick oxidative damage in Chlamydomonas, which reverted after 72 h.•Proteomics revealed the mechanisms involved in BPA detoxification.•Among them, ferroptosis was the key pathway involved in the initial detoxification.•Ferroptosis was described for the first time in microalgae and response to BPA.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>36860062</pmid><doi>10.1016/j.jhazmat.2023.130997</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-8217-9264</orcidid><orcidid>https://orcid.org/0000-0003-1905-3922</orcidid><orcidid>https://orcid.org/0000-0002-9719-6358</orcidid><orcidid>https://orcid.org/0000-0002-1830-3056</orcidid><orcidid>https://orcid.org/0000-0003-4706-9841</orcidid><orcidid>https://orcid.org/0000-0002-1639-9672</orcidid><orcidid>https://orcid.org/0000-0002-0636-365X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Biodegradation, Environmental BPA Chlamydomonas Chloroplast Environmental Pollutants Ferroptosis Mammals Microalgae Microplastics Mitochondria Plastics Proteomics Reactive Oxygen Species (ROS) Xenobiotics |
title | Ferroptosis is the key cellular process mediating Bisphenol A responses in Chlamydomonas and a promising target for enhancing microalgae-based bioremediation |
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