Enhanced Exoelectrogenic Activity of <i>Cupriavidus metallidurans</i> in Bioelectrochemical Systems through the Expression of a Constitutively Active Diguanylate Cyclase

Electroactive bacteria have a wide range of applications, including electricity production, bioremediation, and the sensing of toxic compounds. Bacterial biofilm formation is often mediated by the second messenger cyclic guanosine monophosphate (c-di-GMP) synthesized by a diguanylate cyclase (DGC)....

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Main Authors: Pablo Alviz-Gazitua, Anna Espinoza-Tofalos, Francesca Formicola, Nicolas Guiliani, Raymond J. Turner, Andrea Franzetti, Michael Seeger
Format: Article
Language:English
Published: MDPI AG 2022-06-01
Series:Environments
Subjects:
Online Access:https://www.mdpi.com/2076-3298/9/7/80
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author Pablo Alviz-Gazitua
Anna Espinoza-Tofalos
Francesca Formicola
Nicolas Guiliani
Raymond J. Turner
Andrea Franzetti
Michael Seeger
author_facet Pablo Alviz-Gazitua
Anna Espinoza-Tofalos
Francesca Formicola
Nicolas Guiliani
Raymond J. Turner
Andrea Franzetti
Michael Seeger
author_sort Pablo Alviz-Gazitua
collection DOAJ
description Electroactive bacteria have a wide range of applications, including electricity production, bioremediation, and the sensing of toxic compounds. Bacterial biofilm formation is often mediated by the second messenger cyclic guanosine monophosphate (c-di-GMP) synthesized by a diguanylate cyclase (DGC). The role of c-di-GMP in the expression of c-type cytochromes has been previously reported. The aim of this study was to determine the bioelectrogenic activity of <i>Cupriavidus metallidurans</i> strain CH34 pJB<i>pleD</i>*, which possesses a constitutively active DGC that increases c-di-GMP levels. Notably, the heterologous expression of the constitutively active DGC in <i>C. metallidurans</i> strain CH34 pJB<i>pleD</i>* showed a higher biofilm formation and increased the electrical current production up to 560%. In addition, <i>C. metallidurans</i> CH34 pJB<i>pleD</i>* showed increased levels of c-type cytochrome-associated transcripts compared with the wild-type strain CH34. Scanning electron microscopies revealed a denser extracellular matrix with an increased exopolymeric substance content in the CH34 pJB<i>pleD</i>* biofilm on the electrode surface. The results of this study suggest that higher levels of c-di-GMP synthesized by a constitutively active diguanylate cyclase in <i>C. metallidurans</i> strain CH34 pJB<i>pleD</i>* activated the formation of an electroactive biofilm on the electrode, enhancing its exoelectrogenic activity.
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spelling doaj.art-c886c9c1b57748bab621495d97fdf0642023-12-03T15:01:29ZengMDPI AGEnvironments2076-32982022-06-01978010.3390/environments9070080Enhanced Exoelectrogenic Activity of <i>Cupriavidus metallidurans</i> in Bioelectrochemical Systems through the Expression of a Constitutively Active Diguanylate CyclasePablo Alviz-Gazitua0Anna Espinoza-Tofalos1Francesca Formicola2Nicolas Guiliani3Raymond J. Turner4Andrea Franzetti5Michael Seeger6Laboratorio de Microbiología Molecular y Biotecnología Ambiental, Departamento de Química & Centro de Biotecnología Dr. Daniel Alkalay Lowitt, Universidad Técnica Federico Santa María, Valparaíso 2390123, ChileDepartment of Earth and Environmental Sciences, University of Milano-Bicocca, 20126 Milan, ItalyDepartment of Earth and Environmental Sciences, University of Milano-Bicocca, 20126 Milan, ItalyLaboratorio de Comunicación Bacteriana, Departamento de Biología, Facultad de Ciencias, Universidad de Chile, Santiago 7800003, ChileDepartment of Biological Sciences, University of Calgary, Calgary, AB T2N1N4, CanadaDepartment of Earth and Environmental Sciences, University of Milano-Bicocca, 20126 Milan, ItalyLaboratorio de Microbiología Molecular y Biotecnología Ambiental, Departamento de Química & Centro de Biotecnología Dr. Daniel Alkalay Lowitt, Universidad Técnica Federico Santa María, Valparaíso 2390123, ChileElectroactive bacteria have a wide range of applications, including electricity production, bioremediation, and the sensing of toxic compounds. Bacterial biofilm formation is often mediated by the second messenger cyclic guanosine monophosphate (c-di-GMP) synthesized by a diguanylate cyclase (DGC). The role of c-di-GMP in the expression of c-type cytochromes has been previously reported. The aim of this study was to determine the bioelectrogenic activity of <i>Cupriavidus metallidurans</i> strain CH34 pJB<i>pleD</i>*, which possesses a constitutively active DGC that increases c-di-GMP levels. Notably, the heterologous expression of the constitutively active DGC in <i>C. metallidurans</i> strain CH34 pJB<i>pleD</i>* showed a higher biofilm formation and increased the electrical current production up to 560%. In addition, <i>C. metallidurans</i> CH34 pJB<i>pleD</i>* showed increased levels of c-type cytochrome-associated transcripts compared with the wild-type strain CH34. Scanning electron microscopies revealed a denser extracellular matrix with an increased exopolymeric substance content in the CH34 pJB<i>pleD</i>* biofilm on the electrode surface. The results of this study suggest that higher levels of c-di-GMP synthesized by a constitutively active diguanylate cyclase in <i>C. metallidurans</i> strain CH34 pJB<i>pleD</i>* activated the formation of an electroactive biofilm on the electrode, enhancing its exoelectrogenic activity.https://www.mdpi.com/2076-3298/9/7/80bioelectrochemical system<i>Cupriavidus metallidurans</i>c-di-GMPelectroactive bacteriadiguanylate cyclaseexoelectrogenic activity
spellingShingle Pablo Alviz-Gazitua
Anna Espinoza-Tofalos
Francesca Formicola
Nicolas Guiliani
Raymond J. Turner
Andrea Franzetti
Michael Seeger
Enhanced Exoelectrogenic Activity of <i>Cupriavidus metallidurans</i> in Bioelectrochemical Systems through the Expression of a Constitutively Active Diguanylate Cyclase
Environments
bioelectrochemical system
<i>Cupriavidus metallidurans</i>
c-di-GMP
electroactive bacteria
diguanylate cyclase
exoelectrogenic activity
title Enhanced Exoelectrogenic Activity of <i>Cupriavidus metallidurans</i> in Bioelectrochemical Systems through the Expression of a Constitutively Active Diguanylate Cyclase
title_full Enhanced Exoelectrogenic Activity of <i>Cupriavidus metallidurans</i> in Bioelectrochemical Systems through the Expression of a Constitutively Active Diguanylate Cyclase
title_fullStr Enhanced Exoelectrogenic Activity of <i>Cupriavidus metallidurans</i> in Bioelectrochemical Systems through the Expression of a Constitutively Active Diguanylate Cyclase
title_full_unstemmed Enhanced Exoelectrogenic Activity of <i>Cupriavidus metallidurans</i> in Bioelectrochemical Systems through the Expression of a Constitutively Active Diguanylate Cyclase
title_short Enhanced Exoelectrogenic Activity of <i>Cupriavidus metallidurans</i> in Bioelectrochemical Systems through the Expression of a Constitutively Active Diguanylate Cyclase
title_sort enhanced exoelectrogenic activity of i cupriavidus metallidurans i in bioelectrochemical systems through the expression of a constitutively active diguanylate cyclase
topic bioelectrochemical system
<i>Cupriavidus metallidurans</i>
c-di-GMP
electroactive bacteria
diguanylate cyclase
exoelectrogenic activity
url https://www.mdpi.com/2076-3298/9/7/80
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