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Cyanobacterial cell-wall components as emerging environmental toxicants - detection and holistic monitoring by cellular signaling biosensors
Cyanobacterial blooms constitute a recognized danger to aquatic environment and public health not only due to presence of main group of cyanotoxins, such as microcystins, cylindrospermopsin or anatoxin-a, but also other emerging bioactivities. An innovative approach identifying such bioactivities is...
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Published in: | The Science of the total environment 2022-02, Vol.807 (Pt 2), p.150645-150645, Article 150645 |
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creator | Gągała-Borowska, Ilona Karwaciak, Iwona Jaros, Dorota Ratajewski, Marcin Kokociński, Mikołaj Jurczak, Tomasz Remlein, Bartłomiej Rudnicka, Kinga Pułaski, Łukasz Mankiewicz-Boczek, Joanna |
description | Cyanobacterial blooms constitute a recognized danger to aquatic environment and public health not only due to presence of main group of cyanotoxins, such as microcystins, cylindrospermopsin or anatoxin-a, but also other emerging bioactivities. An innovative approach identifying such bioactivities is the application of cellular biosensors based on reporter genes which detect the impact of cyanobacterial cells and components on actual human cells in a physiological-like setting. In the present study biosensor cell lines detecting four different types of bioactivities (ARE – oxidative stress, NFKBRE – immunomodulatory pathogen-associated molecular patterns, AHRE – persistent organic pollutants, GRE – endocrine disruptors) were exposed to concentrated cyanobacterial cells from 21 environmental bloom samples and from eight cultures (Microcystis aeruginosa, Aphanizomenon flos-aquae, Planktothrix agardhii and Raphidiopsis raciborskii). The AHRE and GRE biosensors did not detect any relevant bioactivity. In turn, ARE biosensors were significantly activated by bloom samples from Jeziorsko (180–250%) and Sulejów (250–400%) reservoirs with the highest cyanobacterial biomass, while activation by cultures was weak/undetectable. The same biosensors were stimulated by microcystin-LR (250%) and anatoxin-a (150%). The NFKBRE biosensors were activated to varying extent (140–650%) by most bloom and culture samples, pointing to potential immunomodulatory toxic effects on humans. Lipopolysaccharide and lipoproteins were identified as responsible for NFKBRE activation (probably via pattern recognition receptors), while peptidoglycan had no bioactivity in this assay. Thus, the holistic approach to sample analysis with the application of cellular biosensors geared towards 4 separate pathways/bioactivities was validated for identification of novel bioactivities in organisms with recognized public health significance (e.g. this study is the first to describe cyanobacterial lipoproteins as potential environmental immunomodulators). Moreover, the ability of cellular biosensors to be activated by intact cyanobacterial cells from blooms provides proof of concept of their direct application for environmental monitoring, especially comparison of potential threats without need for chemical analysis and identification of toxicants.
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•Novel bioactive components in cyanobacterial blooms are identified.•Reporter gene-based cellular biosensors were used for bioactivity assay.• |
doi_str_mv | 10.1016/j.scitotenv.2021.150645 |
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[Display omitted]
•Novel bioactive components in cyanobacterial blooms are identified.•Reporter gene-based cellular biosensors were used for bioactivity assay.•Lipopolysaccharide and lipoproteins were identified as potential immunomodulators.•Cellular biosensors are suitable for bioactivity monitoring of cyanobacterial blooms.</description><identifier>ISSN: 0048-9697</identifier><identifier>EISSN: 1879-1026</identifier><identifier>DOI: 10.1016/j.scitotenv.2021.150645</identifier><identifier>PMID: 34637876</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Biosensing Techniques ; Biosensors ; Cyanobacteria ; Cyanobacteria Toxins ; Cyanotoxins ; Humans ; Lipopolysaccharide ; Lipoproteins ; NFkappaB</subject><ispartof>The Science of the total environment, 2022-02, Vol.807 (Pt 2), p.150645-150645, Article 150645</ispartof><rights>2021</rights><rights>Copyright © 2021. Published by Elsevier B.V.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c371t-609c12a69b1b88bcdae1cac0f95359710b6a8750a79621f2e3859755bd7964ce3</citedby><cites>FETCH-LOGICAL-c371t-609c12a69b1b88bcdae1cac0f95359710b6a8750a79621f2e3859755bd7964ce3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,777,781,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34637876$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gągała-Borowska, Ilona</creatorcontrib><creatorcontrib>Karwaciak, Iwona</creatorcontrib><creatorcontrib>Jaros, Dorota</creatorcontrib><creatorcontrib>Ratajewski, Marcin</creatorcontrib><creatorcontrib>Kokociński, Mikołaj</creatorcontrib><creatorcontrib>Jurczak, Tomasz</creatorcontrib><creatorcontrib>Remlein, Bartłomiej</creatorcontrib><creatorcontrib>Rudnicka, Kinga</creatorcontrib><creatorcontrib>Pułaski, Łukasz</creatorcontrib><creatorcontrib>Mankiewicz-Boczek, Joanna</creatorcontrib><title>Cyanobacterial cell-wall components as emerging environmental toxicants - detection and holistic monitoring by cellular signaling biosensors</title><title>The Science of the total environment</title><addtitle>Sci Total Environ</addtitle><description>Cyanobacterial blooms constitute a recognized danger to aquatic environment and public health not only due to presence of main group of cyanotoxins, such as microcystins, cylindrospermopsin or anatoxin-a, but also other emerging bioactivities. An innovative approach identifying such bioactivities is the application of cellular biosensors based on reporter genes which detect the impact of cyanobacterial cells and components on actual human cells in a physiological-like setting. In the present study biosensor cell lines detecting four different types of bioactivities (ARE – oxidative stress, NFKBRE – immunomodulatory pathogen-associated molecular patterns, AHRE – persistent organic pollutants, GRE – endocrine disruptors) were exposed to concentrated cyanobacterial cells from 21 environmental bloom samples and from eight cultures (Microcystis aeruginosa, Aphanizomenon flos-aquae, Planktothrix agardhii and Raphidiopsis raciborskii). The AHRE and GRE biosensors did not detect any relevant bioactivity. In turn, ARE biosensors were significantly activated by bloom samples from Jeziorsko (180–250%) and Sulejów (250–400%) reservoirs with the highest cyanobacterial biomass, while activation by cultures was weak/undetectable. The same biosensors were stimulated by microcystin-LR (250%) and anatoxin-a (150%). The NFKBRE biosensors were activated to varying extent (140–650%) by most bloom and culture samples, pointing to potential immunomodulatory toxic effects on humans. Lipopolysaccharide and lipoproteins were identified as responsible for NFKBRE activation (probably via pattern recognition receptors), while peptidoglycan had no bioactivity in this assay. Thus, the holistic approach to sample analysis with the application of cellular biosensors geared towards 4 separate pathways/bioactivities was validated for identification of novel bioactivities in organisms with recognized public health significance (e.g. this study is the first to describe cyanobacterial lipoproteins as potential environmental immunomodulators). Moreover, the ability of cellular biosensors to be activated by intact cyanobacterial cells from blooms provides proof of concept of their direct application for environmental monitoring, especially comparison of potential threats without need for chemical analysis and identification of toxicants.
[Display omitted]
•Novel bioactive components in cyanobacterial blooms are identified.•Reporter gene-based cellular biosensors were used for bioactivity assay.•Lipopolysaccharide and lipoproteins were identified as potential immunomodulators.•Cellular biosensors are suitable for bioactivity monitoring of cyanobacterial blooms.</description><subject>Biosensing Techniques</subject><subject>Biosensors</subject><subject>Cyanobacteria</subject><subject>Cyanobacteria Toxins</subject><subject>Cyanotoxins</subject><subject>Humans</subject><subject>Lipopolysaccharide</subject><subject>Lipoproteins</subject><subject>NFkappaB</subject><issn>0048-9697</issn><issn>1879-1026</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNqFUctOHDEQtKKgsDx-IfExl1nsefhxRKtAIiHlAmerx9O78WrG3theYP8hH42HBa7xxVa5uqq7i5BvnC054-Jqu0zW5ZDRPy5rVvMl75hou09kwZXUFWe1-EwWjLWq0kLLU3KW0paVIxX_Qk6bVjRSSbEg_1YH8KEHmzE6GKnFcayeYCyvMO2CR58ThURxwrhxfkOLo4vBT-Wj0HN4dhZmTkUHzGizC56CH-ifMLqUnaVT8KXTONf2h1f9_QiRJrfxML6iLiT0KcR0QU7WMCa8fLvPycPNj_vVz-ru9-2v1fVdZRvJcyWYtrwGoXveK9XbAZBbsGytu6bTkrNegJIdA6lFzdc1NqrAXdcPBWgtNufk-1F3F8PfPaZsJpfmzsBj2CdTd4pLLdtWFao8Um0MKUVcm110E8SD4czMUZit-YjCzFGYYxSl8uubyb6fcPioe999IVwfCVhGfXQYZyH0FgcXyyLNENx_TV4A3sei6g</recordid><startdate>20220210</startdate><enddate>20220210</enddate><creator>Gągała-Borowska, Ilona</creator><creator>Karwaciak, Iwona</creator><creator>Jaros, Dorota</creator><creator>Ratajewski, Marcin</creator><creator>Kokociński, Mikołaj</creator><creator>Jurczak, Tomasz</creator><creator>Remlein, Bartłomiej</creator><creator>Rudnicka, Kinga</creator><creator>Pułaski, Łukasz</creator><creator>Mankiewicz-Boczek, Joanna</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><scope>7X8</scope></search><sort><creationdate>20220210</creationdate><title>Cyanobacterial cell-wall components as emerging environmental toxicants - detection and holistic monitoring by cellular signaling biosensors</title><author>Gągała-Borowska, Ilona ; Karwaciak, Iwona ; Jaros, Dorota ; Ratajewski, Marcin ; Kokociński, Mikołaj ; Jurczak, Tomasz ; Remlein, Bartłomiej ; Rudnicka, Kinga ; Pułaski, Łukasz ; Mankiewicz-Boczek, Joanna</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c371t-609c12a69b1b88bcdae1cac0f95359710b6a8750a79621f2e3859755bd7964ce3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Biosensing Techniques</topic><topic>Biosensors</topic><topic>Cyanobacteria</topic><topic>Cyanobacteria Toxins</topic><topic>Cyanotoxins</topic><topic>Humans</topic><topic>Lipopolysaccharide</topic><topic>Lipoproteins</topic><topic>NFkappaB</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gągała-Borowska, Ilona</creatorcontrib><creatorcontrib>Karwaciak, Iwona</creatorcontrib><creatorcontrib>Jaros, Dorota</creatorcontrib><creatorcontrib>Ratajewski, Marcin</creatorcontrib><creatorcontrib>Kokociński, Mikołaj</creatorcontrib><creatorcontrib>Jurczak, Tomasz</creatorcontrib><creatorcontrib>Remlein, Bartłomiej</creatorcontrib><creatorcontrib>Rudnicka, Kinga</creatorcontrib><creatorcontrib>Pułaski, Łukasz</creatorcontrib><creatorcontrib>Mankiewicz-Boczek, Joanna</creatorcontrib><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>The Science of the total environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gągała-Borowska, Ilona</au><au>Karwaciak, Iwona</au><au>Jaros, Dorota</au><au>Ratajewski, Marcin</au><au>Kokociński, Mikołaj</au><au>Jurczak, Tomasz</au><au>Remlein, Bartłomiej</au><au>Rudnicka, Kinga</au><au>Pułaski, Łukasz</au><au>Mankiewicz-Boczek, Joanna</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cyanobacterial cell-wall components as emerging environmental toxicants - detection and holistic monitoring by cellular signaling biosensors</atitle><jtitle>The Science of the total environment</jtitle><addtitle>Sci Total Environ</addtitle><date>2022-02-10</date><risdate>2022</risdate><volume>807</volume><issue>Pt 2</issue><spage>150645</spage><epage>150645</epage><pages>150645-150645</pages><artnum>150645</artnum><issn>0048-9697</issn><eissn>1879-1026</eissn><abstract>Cyanobacterial blooms constitute a recognized danger to aquatic environment and public health not only due to presence of main group of cyanotoxins, such as microcystins, cylindrospermopsin or anatoxin-a, but also other emerging bioactivities. An innovative approach identifying such bioactivities is the application of cellular biosensors based on reporter genes which detect the impact of cyanobacterial cells and components on actual human cells in a physiological-like setting. In the present study biosensor cell lines detecting four different types of bioactivities (ARE – oxidative stress, NFKBRE – immunomodulatory pathogen-associated molecular patterns, AHRE – persistent organic pollutants, GRE – endocrine disruptors) were exposed to concentrated cyanobacterial cells from 21 environmental bloom samples and from eight cultures (Microcystis aeruginosa, Aphanizomenon flos-aquae, Planktothrix agardhii and Raphidiopsis raciborskii). The AHRE and GRE biosensors did not detect any relevant bioactivity. In turn, ARE biosensors were significantly activated by bloom samples from Jeziorsko (180–250%) and Sulejów (250–400%) reservoirs with the highest cyanobacterial biomass, while activation by cultures was weak/undetectable. The same biosensors were stimulated by microcystin-LR (250%) and anatoxin-a (150%). The NFKBRE biosensors were activated to varying extent (140–650%) by most bloom and culture samples, pointing to potential immunomodulatory toxic effects on humans. Lipopolysaccharide and lipoproteins were identified as responsible for NFKBRE activation (probably via pattern recognition receptors), while peptidoglycan had no bioactivity in this assay. Thus, the holistic approach to sample analysis with the application of cellular biosensors geared towards 4 separate pathways/bioactivities was validated for identification of novel bioactivities in organisms with recognized public health significance (e.g. this study is the first to describe cyanobacterial lipoproteins as potential environmental immunomodulators). Moreover, the ability of cellular biosensors to be activated by intact cyanobacterial cells from blooms provides proof of concept of their direct application for environmental monitoring, especially comparison of potential threats without need for chemical analysis and identification of toxicants.
[Display omitted]
•Novel bioactive components in cyanobacterial blooms are identified.•Reporter gene-based cellular biosensors were used for bioactivity assay.•Lipopolysaccharide and lipoproteins were identified as potential immunomodulators.•Cellular biosensors are suitable for bioactivity monitoring of cyanobacterial blooms.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>34637876</pmid><doi>10.1016/j.scitotenv.2021.150645</doi><tpages>1</tpages></addata></record> |
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subjects | Biosensing Techniques Biosensors Cyanobacteria Cyanobacteria Toxins Cyanotoxins Humans Lipopolysaccharide Lipoproteins NFkappaB |
title | Cyanobacterial cell-wall components as emerging environmental toxicants - detection and holistic monitoring by cellular signaling biosensors |
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