Single cell ICP-MS to evaluate the interaction behaviour for Cd, Ce and U with Streptomyces coelicolor spores
Streptomyces are important soil bacteria used for bioremediation of metal-contaminated soils, however, it is still unknown how metal-selective Streptomyces are and which mechanisms are involved during their capture. In this work, we exposed S. coelicolor spores to environmentally relevant concentrat...
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creator | Hellmann, Steffen García-Cancela, Paula Alonso-Fernández, Sergio Corte-Rodríguez, Mario Bettmer, Jörg Manteca, Angel Merten, Dirk Gil-Díaz, Teba Schäfer, Thorsten Montes-Bayón, María |
description | Streptomyces are important soil bacteria used for bioremediation of metal-contaminated soils, however, it is still unknown how metal-selective Streptomyces are and which mechanisms are involved during their capture. In this work, we exposed S. coelicolor spores to environmentally relevant concentrations (0.1, 1, 10, 100 μM) of Ce, U and Cd in solid medium for one week to investigate the uptake behaviour of hyphae in the newly formed spores. Additionally, metal adsorption onto the spores was explored by incubating inactive, ungerminated spores for one day in aqueous metal solution. The spore-washing treatment was key to distinguishing between strongly spore-associated (e.g. incorporation; Tris-EDTA buffer) and weakly spore-associated metals (Tris buffer alone minus Tris-EDTA). Single cell (sc) ICP-MS was used to quantify metal-associated content in individual spores. Our results revealed element-specific adsorption onto inactive spores showing that out of the total metal exposure, both strongly (Ce: 58%; U: 54%; Cd: 28%) and weakly (Ce: 12%; U: 1%; Cd: 18%) adsorbed metals occur. However, scICP-MS showed that from metal-amended solid medium, only Ce and U were strongly spore-associated (averages 0.040 and 0.062 fg spore−1 for 10 μM exposures, respectively) while Cd was below the limit of detection (< 0.006 fg spore−1). We propose that hyphae only metabolically interact with Ce in a controlled manner but uncontrolled with U, as 66–73% Ce and only 2–4% U were inherited from adsorbed content. We conclude that Streptomyces spore-metal interaction starts with a relevant adsorption step of Ce, U and Cd as presented for aqueous conditions. If spores start to germinate, hyphae are capable of effectively encapsulating Ce and U, but not Cd. This study brings light into the still unknown field of metal interactions with Streptomyces and applied understanding for more efficient and metal-specific use of Streptomyces in bioremediation of metal-polluted soils.
[Display omitted]
•Single cell ICP-MS was used to quantify metal association with spores.•Distinction between weak adsorption and strong association (metal-spore).•Ce, U and Cd showed spore-adsorption in aqueous conditions.•Ce and U were strongly spore-associated after growing in metal-amended solid medium.•Spore association metabolically controlled for Ce and uncontrolled for U. |
doi_str_mv | 10.1016/j.chemosphere.2023.140633 |
format | Article |
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[Display omitted]
•Single cell ICP-MS was used to quantify metal association with spores.•Distinction between weak adsorption and strong association (metal-spore).•Ce, U and Cd showed spore-adsorption in aqueous conditions.•Ce and U were strongly spore-associated after growing in metal-amended solid medium.•Spore association metabolically controlled for Ce and uncontrolled for U.</description><identifier>ISSN: 0045-6535</identifier><identifier>EISSN: 1879-1298</identifier><identifier>DOI: 10.1016/j.chemosphere.2023.140633</identifier><language>eng</language><publisher>Elsevier Ltd</publisher><subject>adsorption ; Association ; Bioaccumulation ; bioremediation ; Cadmium ; Cerium ; detection limit ; Gram-positive bacteria ; hyphae ; soil ; Streptomyces coelicolor ; Uranium</subject><ispartof>Chemosphere (Oxford), 2024-01, Vol.347, p.140633-140633, Article 140633</ispartof><rights>2023 The Authors</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3533-50964b597ffe6716d3a00c60d11a5e8ee002b5b172413898994832f643b02bd3</citedby><cites>FETCH-LOGICAL-c3533-50964b597ffe6716d3a00c60d11a5e8ee002b5b172413898994832f643b02bd3</cites><orcidid>0000-0002-8596-2828 ; 0000-0001-6114-9405 ; 0000-0003-0109-4101 ; 0000-0003-2829-033X ; 0000-0003-2320-2708 ; 0000-0001-7927-9240</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S004565352302903X$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3536,27903,27904,65309</link.rule.ids></links><search><creatorcontrib>Hellmann, Steffen</creatorcontrib><creatorcontrib>García-Cancela, Paula</creatorcontrib><creatorcontrib>Alonso-Fernández, Sergio</creatorcontrib><creatorcontrib>Corte-Rodríguez, Mario</creatorcontrib><creatorcontrib>Bettmer, Jörg</creatorcontrib><creatorcontrib>Manteca, Angel</creatorcontrib><creatorcontrib>Merten, Dirk</creatorcontrib><creatorcontrib>Gil-Díaz, Teba</creatorcontrib><creatorcontrib>Schäfer, Thorsten</creatorcontrib><creatorcontrib>Montes-Bayón, María</creatorcontrib><title>Single cell ICP-MS to evaluate the interaction behaviour for Cd, Ce and U with Streptomyces coelicolor spores</title><title>Chemosphere (Oxford)</title><description>Streptomyces are important soil bacteria used for bioremediation of metal-contaminated soils, however, it is still unknown how metal-selective Streptomyces are and which mechanisms are involved during their capture. In this work, we exposed S. coelicolor spores to environmentally relevant concentrations (0.1, 1, 10, 100 μM) of Ce, U and Cd in solid medium for one week to investigate the uptake behaviour of hyphae in the newly formed spores. Additionally, metal adsorption onto the spores was explored by incubating inactive, ungerminated spores for one day in aqueous metal solution. The spore-washing treatment was key to distinguishing between strongly spore-associated (e.g. incorporation; Tris-EDTA buffer) and weakly spore-associated metals (Tris buffer alone minus Tris-EDTA). Single cell (sc) ICP-MS was used to quantify metal-associated content in individual spores. Our results revealed element-specific adsorption onto inactive spores showing that out of the total metal exposure, both strongly (Ce: 58%; U: 54%; Cd: 28%) and weakly (Ce: 12%; U: 1%; Cd: 18%) adsorbed metals occur. However, scICP-MS showed that from metal-amended solid medium, only Ce and U were strongly spore-associated (averages 0.040 and 0.062 fg spore−1 for 10 μM exposures, respectively) while Cd was below the limit of detection (< 0.006 fg spore−1). We propose that hyphae only metabolically interact with Ce in a controlled manner but uncontrolled with U, as 66–73% Ce and only 2–4% U were inherited from adsorbed content. We conclude that Streptomyces spore-metal interaction starts with a relevant adsorption step of Ce, U and Cd as presented for aqueous conditions. If spores start to germinate, hyphae are capable of effectively encapsulating Ce and U, but not Cd. This study brings light into the still unknown field of metal interactions with Streptomyces and applied understanding for more efficient and metal-specific use of Streptomyces in bioremediation of metal-polluted soils.
[Display omitted]
•Single cell ICP-MS was used to quantify metal association with spores.•Distinction between weak adsorption and strong association (metal-spore).•Ce, U and Cd showed spore-adsorption in aqueous conditions.•Ce and U were strongly spore-associated after growing in metal-amended solid medium.•Spore association metabolically controlled for Ce and uncontrolled for U.</description><subject>adsorption</subject><subject>Association</subject><subject>Bioaccumulation</subject><subject>bioremediation</subject><subject>Cadmium</subject><subject>Cerium</subject><subject>detection limit</subject><subject>Gram-positive bacteria</subject><subject>hyphae</subject><subject>soil</subject><subject>Streptomyces coelicolor</subject><subject>Uranium</subject><issn>0045-6535</issn><issn>1879-1298</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqNkU2L2zAURUVpoWna_6DZzaJOnyTLsZaDmY9AhikkXQtZfh4r2JYrKSn59-OQWXTXrt7inXvhcgi5YbBiwIofh5XtcPBx6jDgigMXK5ZDIcQHsmDlWmWMq_IjWQDkMiukkJ_JlxgPAHNYqgUZdm587ZFa7Hu6qX5mzzuaPMWT6Y8mIU0dUjcmDMYm50daY2dOzh8DbX2gVfOdVkjN2NBf9I9LHd2lgFPyw9lipNZj76zvZzJOPmD8Sj61po_47f0uyf7hfl89ZduXx011t82skEJkElSR11Kt2xaLNSsaYQBsAQ1jRmKJCMBrWbM1z5koValUXgreFrmo50cjluT2WjsF__uIMenBxctCM6I_Ri2YzNlcz-U_UV6WiucAUs2ouqI2-BgDtnoKbjDhrBnoiwx90H_J0BcZ-ipjzlbXLM6rTw6DjtbhaLFxAW3SjXf_0fIGuvGXag</recordid><startdate>202401</startdate><enddate>202401</enddate><creator>Hellmann, Steffen</creator><creator>García-Cancela, Paula</creator><creator>Alonso-Fernández, Sergio</creator><creator>Corte-Rodríguez, Mario</creator><creator>Bettmer, Jörg</creator><creator>Manteca, Angel</creator><creator>Merten, Dirk</creator><creator>Gil-Díaz, Teba</creator><creator>Schäfer, Thorsten</creator><creator>Montes-Bayón, María</creator><general>Elsevier Ltd</general><scope>6I.</scope><scope>AAFTH</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-8596-2828</orcidid><orcidid>https://orcid.org/0000-0001-6114-9405</orcidid><orcidid>https://orcid.org/0000-0003-0109-4101</orcidid><orcidid>https://orcid.org/0000-0003-2829-033X</orcidid><orcidid>https://orcid.org/0000-0003-2320-2708</orcidid><orcidid>https://orcid.org/0000-0001-7927-9240</orcidid></search><sort><creationdate>202401</creationdate><title>Single cell ICP-MS to evaluate the interaction behaviour for Cd, Ce and U with Streptomyces coelicolor spores</title><author>Hellmann, Steffen ; García-Cancela, Paula ; Alonso-Fernández, Sergio ; Corte-Rodríguez, Mario ; Bettmer, Jörg ; Manteca, Angel ; Merten, Dirk ; Gil-Díaz, Teba ; Schäfer, Thorsten ; Montes-Bayón, María</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3533-50964b597ffe6716d3a00c60d11a5e8ee002b5b172413898994832f643b02bd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>adsorption</topic><topic>Association</topic><topic>Bioaccumulation</topic><topic>bioremediation</topic><topic>Cadmium</topic><topic>Cerium</topic><topic>detection limit</topic><topic>Gram-positive bacteria</topic><topic>hyphae</topic><topic>soil</topic><topic>Streptomyces coelicolor</topic><topic>Uranium</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hellmann, Steffen</creatorcontrib><creatorcontrib>García-Cancela, Paula</creatorcontrib><creatorcontrib>Alonso-Fernández, Sergio</creatorcontrib><creatorcontrib>Corte-Rodríguez, Mario</creatorcontrib><creatorcontrib>Bettmer, Jörg</creatorcontrib><creatorcontrib>Manteca, Angel</creatorcontrib><creatorcontrib>Merten, Dirk</creatorcontrib><creatorcontrib>Gil-Díaz, Teba</creatorcontrib><creatorcontrib>Schäfer, Thorsten</creatorcontrib><creatorcontrib>Montes-Bayón, María</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Chemosphere (Oxford)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hellmann, Steffen</au><au>García-Cancela, Paula</au><au>Alonso-Fernández, Sergio</au><au>Corte-Rodríguez, Mario</au><au>Bettmer, Jörg</au><au>Manteca, Angel</au><au>Merten, Dirk</au><au>Gil-Díaz, Teba</au><au>Schäfer, Thorsten</au><au>Montes-Bayón, María</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Single cell ICP-MS to evaluate the interaction behaviour for Cd, Ce and U with Streptomyces coelicolor spores</atitle><jtitle>Chemosphere (Oxford)</jtitle><date>2024-01</date><risdate>2024</risdate><volume>347</volume><spage>140633</spage><epage>140633</epage><pages>140633-140633</pages><artnum>140633</artnum><issn>0045-6535</issn><eissn>1879-1298</eissn><abstract>Streptomyces are important soil bacteria used for bioremediation of metal-contaminated soils, however, it is still unknown how metal-selective Streptomyces are and which mechanisms are involved during their capture. In this work, we exposed S. coelicolor spores to environmentally relevant concentrations (0.1, 1, 10, 100 μM) of Ce, U and Cd in solid medium for one week to investigate the uptake behaviour of hyphae in the newly formed spores. Additionally, metal adsorption onto the spores was explored by incubating inactive, ungerminated spores for one day in aqueous metal solution. The spore-washing treatment was key to distinguishing between strongly spore-associated (e.g. incorporation; Tris-EDTA buffer) and weakly spore-associated metals (Tris buffer alone minus Tris-EDTA). Single cell (sc) ICP-MS was used to quantify metal-associated content in individual spores. Our results revealed element-specific adsorption onto inactive spores showing that out of the total metal exposure, both strongly (Ce: 58%; U: 54%; Cd: 28%) and weakly (Ce: 12%; U: 1%; Cd: 18%) adsorbed metals occur. However, scICP-MS showed that from metal-amended solid medium, only Ce and U were strongly spore-associated (averages 0.040 and 0.062 fg spore−1 for 10 μM exposures, respectively) while Cd was below the limit of detection (< 0.006 fg spore−1). We propose that hyphae only metabolically interact with Ce in a controlled manner but uncontrolled with U, as 66–73% Ce and only 2–4% U were inherited from adsorbed content. We conclude that Streptomyces spore-metal interaction starts with a relevant adsorption step of Ce, U and Cd as presented for aqueous conditions. If spores start to germinate, hyphae are capable of effectively encapsulating Ce and U, but not Cd. This study brings light into the still unknown field of metal interactions with Streptomyces and applied understanding for more efficient and metal-specific use of Streptomyces in bioremediation of metal-polluted soils.
[Display omitted]
•Single cell ICP-MS was used to quantify metal association with spores.•Distinction between weak adsorption and strong association (metal-spore).•Ce, U and Cd showed spore-adsorption in aqueous conditions.•Ce and U were strongly spore-associated after growing in metal-amended solid medium.•Spore association metabolically controlled for Ce and uncontrolled for U.</abstract><pub>Elsevier Ltd</pub><doi>10.1016/j.chemosphere.2023.140633</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-8596-2828</orcidid><orcidid>https://orcid.org/0000-0001-6114-9405</orcidid><orcidid>https://orcid.org/0000-0003-0109-4101</orcidid><orcidid>https://orcid.org/0000-0003-2829-033X</orcidid><orcidid>https://orcid.org/0000-0003-2320-2708</orcidid><orcidid>https://orcid.org/0000-0001-7927-9240</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | adsorption Association Bioaccumulation bioremediation Cadmium Cerium detection limit Gram-positive bacteria hyphae soil Streptomyces coelicolor Uranium |
title | Single cell ICP-MS to evaluate the interaction behaviour for Cd, Ce and U with Streptomyces coelicolor spores |
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