Physicochemical Rationale of Matrix Effects Involved in the Response of Hydrogel-Embedded Luminescent Metal Biosensors
There is currently a critical need for understanding how the response and activity of whole-cell bacterial reporters positioned in a complex biological or environmental matrix are impacted by the physicochemical properties of their micro-environment. Accordingly, a comprehensive analysis of the biol...
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MDPI AG
2024-11-01
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| author | Elise Rotureau Christophe Pagnout Jérôme F. L. Duval |
| author_facet | Elise Rotureau Christophe Pagnout Jérôme F. L. Duval |
| author_sort | Elise Rotureau |
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| description | There is currently a critical need for understanding how the response and activity of whole-cell bacterial reporters positioned in a complex biological or environmental matrix are impacted by the physicochemical properties of their micro-environment. Accordingly, a comprehensive analysis of the bioluminescence response of Cd(II)-inducible PzntA-<i>luxCDABE Escherichia coli</i> biosensors embedded in silica-based hydrogels is reported to decipher how metal bioavailability, cell photoactivity and ensuing light bioproduction are impacted by the hydrogel environment and the associated matrix effects. The analysis includes the account of (i) Cd speciation and accumulation in the host hydrogels, in connection with their reactivity and electrostatic properties, and (ii) the reduced bioavailability of resources for the biosensors confined (deep) inside the hydrogels. The measurements of the bioluminescence response of the Cd(II) inducible-<i>lux</i> biosensors in both hydrogels and free-floating cell suspensions are completed by those of the constitutive <i>rrnB</i> P1-<i>luxCDABE E. coli</i> so as to probe cell metabolic activity in these two situations. The approach contributes to unraveling the connections between the electrostatic hydrogel charge, the nutrient/metal bioavailabilities and the resulting Cd-triggered bioluminescence output. Biosensors are hosted in hydrogels with thickness varying between 0 mm (the free-floating cell situation) and 1.6 mm, and are exposed to total Cd concentrations from 0 to 400 nM. The partitioning of bioavailable metals at the hydrogel/solution interface following intertwined metal speciation, diffusion and Boltzmann electrostatic accumulation is addressed by stripping chronopotentiometry. In turn, we detail how the bioluminescence maxima generated by the Cd-responsive cells under all tested Cd concentration and hydrogel thickness conditions collapse remarkably well on a <i>single plot</i> featuring the dependence of bioluminescence on free Cd concentration at the individual cell level. Overall, the construction of this <i>master curve</i> integrates the contributions of key and often overlooked processes that govern the bioavailability properties of metals in 3D matrices. Accordingly, the work opens perspectives for quantitative and mechanistic monitoring of metals by biosensors in environmental systems like biofilms or sediments. |
| format | Article |
| id | doaj-art-4afa664128044ce3863bf2824a7d6093 |
| institution | OA Journals |
| issn | 2079-6374 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | MDPI AG |
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| series | Biosensors |
| spelling | doaj-art-4afa664128044ce3863bf2824a7d60932025-08-20T02:28:02ZengMDPI AGBiosensors2079-63742024-11-01141155210.3390/bios14110552Physicochemical Rationale of Matrix Effects Involved in the Response of Hydrogel-Embedded Luminescent Metal BiosensorsElise Rotureau0Christophe Pagnout1Jérôme F. L. Duval2Université de Lorraine, CNRS, LIEC, F-54000 Nancy, FranceUniversité de Lorraine, CNRS, LIEC, F-57000 Metz, FranceUniversité de Lorraine, CNRS, LIEC, F-54000 Nancy, FranceThere is currently a critical need for understanding how the response and activity of whole-cell bacterial reporters positioned in a complex biological or environmental matrix are impacted by the physicochemical properties of their micro-environment. Accordingly, a comprehensive analysis of the bioluminescence response of Cd(II)-inducible PzntA-<i>luxCDABE Escherichia coli</i> biosensors embedded in silica-based hydrogels is reported to decipher how metal bioavailability, cell photoactivity and ensuing light bioproduction are impacted by the hydrogel environment and the associated matrix effects. The analysis includes the account of (i) Cd speciation and accumulation in the host hydrogels, in connection with their reactivity and electrostatic properties, and (ii) the reduced bioavailability of resources for the biosensors confined (deep) inside the hydrogels. The measurements of the bioluminescence response of the Cd(II) inducible-<i>lux</i> biosensors in both hydrogels and free-floating cell suspensions are completed by those of the constitutive <i>rrnB</i> P1-<i>luxCDABE E. coli</i> so as to probe cell metabolic activity in these two situations. The approach contributes to unraveling the connections between the electrostatic hydrogel charge, the nutrient/metal bioavailabilities and the resulting Cd-triggered bioluminescence output. Biosensors are hosted in hydrogels with thickness varying between 0 mm (the free-floating cell situation) and 1.6 mm, and are exposed to total Cd concentrations from 0 to 400 nM. The partitioning of bioavailable metals at the hydrogel/solution interface following intertwined metal speciation, diffusion and Boltzmann electrostatic accumulation is addressed by stripping chronopotentiometry. In turn, we detail how the bioluminescence maxima generated by the Cd-responsive cells under all tested Cd concentration and hydrogel thickness conditions collapse remarkably well on a <i>single plot</i> featuring the dependence of bioluminescence on free Cd concentration at the individual cell level. Overall, the construction of this <i>master curve</i> integrates the contributions of key and often overlooked processes that govern the bioavailability properties of metals in 3D matrices. Accordingly, the work opens perspectives for quantitative and mechanistic monitoring of metals by biosensors in environmental systems like biofilms or sediments.https://www.mdpi.com/2079-6374/14/11/552whole-cell metal bioreportersbioluminescencehydrogel matricesmetallic contaminantsspeciationelectrostatics |
| spellingShingle | Elise Rotureau Christophe Pagnout Jérôme F. L. Duval Physicochemical Rationale of Matrix Effects Involved in the Response of Hydrogel-Embedded Luminescent Metal Biosensors Biosensors whole-cell metal bioreporters bioluminescence hydrogel matrices metallic contaminants speciation electrostatics |
| title | Physicochemical Rationale of Matrix Effects Involved in the Response of Hydrogel-Embedded Luminescent Metal Biosensors |
| title_full | Physicochemical Rationale of Matrix Effects Involved in the Response of Hydrogel-Embedded Luminescent Metal Biosensors |
| title_fullStr | Physicochemical Rationale of Matrix Effects Involved in the Response of Hydrogel-Embedded Luminescent Metal Biosensors |
| title_full_unstemmed | Physicochemical Rationale of Matrix Effects Involved in the Response of Hydrogel-Embedded Luminescent Metal Biosensors |
| title_short | Physicochemical Rationale of Matrix Effects Involved in the Response of Hydrogel-Embedded Luminescent Metal Biosensors |
| title_sort | physicochemical rationale of matrix effects involved in the response of hydrogel embedded luminescent metal biosensors |
| topic | whole-cell metal bioreporters bioluminescence hydrogel matrices metallic contaminants speciation electrostatics |
| url | https://www.mdpi.com/2079-6374/14/11/552 |
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