Silver and Copper Acute Effects on Membrane Proteins and Impact on Photosynthetic and Respiratory Complexes in Bacteria

ABSTRACT Silver (Ag+) and copper (Cu+) ions have been used for centuries in industry, as well as antimicrobial agents in agriculture and health care. Nowadays, Ag+ is also widely used in the field of nanotechnology. Yet, the underlying mechanisms driving toxicity of Ag+ ions in vivo are poorly chara...

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Autores principales:	Reem Tambosi, Sylviane Liotenberg, Marie-Line Bourbon, Anne-Soisig Steunou, Marion Babot, Anne Durand, Nouari Kebaili, Soufian Ouchane
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	chlorophyll copper membrane complexes metal homeostasis photosynthesis respiration Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3ddb1587a0784c57ad925def426005fc
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spelling	oai:doaj.org-article:3ddb1587a0784c57ad925def426005fc2021-11-15T15:52:19ZSilver and Copper Acute Effects on Membrane Proteins and Impact on Photosynthetic and Respiratory Complexes in Bacteria10.1128/mBio.01535-182150-7511https://doaj.org/article/3ddb1587a0784c57ad925def426005fc2018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01535-18https://doaj.org/toc/2150-7511ABSTRACT Silver (Ag+) and copper (Cu+) ions have been used for centuries in industry, as well as antimicrobial agents in agriculture and health care. Nowadays, Ag+ is also widely used in the field of nanotechnology. Yet, the underlying mechanisms driving toxicity of Ag+ ions in vivo are poorly characterized. It is well known that exposure to excess metal impairs the photosynthetic apparatus of plants and algae. Here, we show that the light-harvesting complex II (LH2) is the primary target of Ag+ and Cu+ exposure in the purple bacterium Rubrivivax gelatinosus. Ag+ and Cu+ specifically inactivate the 800-nm absorbing bacteriochlorophyll a (B800), while Ni2+ or Cd2+ treatment had no effect. This was further supported by analyses of CuSO4- or AgNO3-treated membrane proteins. Indeed, this treatment induced changes in the LH2 absorption spectrum related to the disruption of the interaction of B800 molecules with the LH2 protein. This caused the release of B800 molecules and subsequently impacted the spectral properties of the carotenoids within the 850-nm absorbing LH2. Moreover, previous studies have suggested that Ag+ can affect the respiratory chain in mitochondria and bacteria. Our data demonstrated that exposure to Ag+, both in vivo and in vitro, caused a decrease of cytochrome c oxidase and succinate dehydrogenase activities. Ag+ inhibition of these respiratory complexes was also observed in Escherichia coli, but not in Bacillus subtilis. IMPORTANCE The use of metal ions represents a serious threat to the environment and to all living organisms because of the acute toxicity of these ions. Nowadays, silver nanoparticles are one of the most widely used nanoparticles in various industrial and health applications. The antimicrobial effect of nanoparticles is in part related to the released Ag+ ions and their ability to interact with bacterial membranes. Here, we identify, both in vitro and in vivo, specific targets of Ag+ ions within the membrane of bacteria. This include complexes involved in photosynthesis, but also complexes involved in respiration.Reem TambosiSylviane LiotenbergMarie-Line BourbonAnne-Soisig SteunouMarion BabotAnne DurandNouari KebailiSoufian OuchaneAmerican Society for Microbiologyarticlechlorophyllcoppermembrane complexesmetal homeostasisphotosynthesisrespirationMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	chlorophyll copper membrane complexes metal homeostasis photosynthesis respiration Microbiology QR1-502
spellingShingle	chlorophyll copper membrane complexes metal homeostasis photosynthesis respiration Microbiology QR1-502 Reem Tambosi Sylviane Liotenberg Marie-Line Bourbon Anne-Soisig Steunou Marion Babot Anne Durand Nouari Kebaili Soufian Ouchane Silver and Copper Acute Effects on Membrane Proteins and Impact on Photosynthetic and Respiratory Complexes in Bacteria
description	ABSTRACT Silver (Ag+) and copper (Cu+) ions have been used for centuries in industry, as well as antimicrobial agents in agriculture and health care. Nowadays, Ag+ is also widely used in the field of nanotechnology. Yet, the underlying mechanisms driving toxicity of Ag+ ions in vivo are poorly characterized. It is well known that exposure to excess metal impairs the photosynthetic apparatus of plants and algae. Here, we show that the light-harvesting complex II (LH2) is the primary target of Ag+ and Cu+ exposure in the purple bacterium Rubrivivax gelatinosus. Ag+ and Cu+ specifically inactivate the 800-nm absorbing bacteriochlorophyll a (B800), while Ni2+ or Cd2+ treatment had no effect. This was further supported by analyses of CuSO4- or AgNO3-treated membrane proteins. Indeed, this treatment induced changes in the LH2 absorption spectrum related to the disruption of the interaction of B800 molecules with the LH2 protein. This caused the release of B800 molecules and subsequently impacted the spectral properties of the carotenoids within the 850-nm absorbing LH2. Moreover, previous studies have suggested that Ag+ can affect the respiratory chain in mitochondria and bacteria. Our data demonstrated that exposure to Ag+, both in vivo and in vitro, caused a decrease of cytochrome c oxidase and succinate dehydrogenase activities. Ag+ inhibition of these respiratory complexes was also observed in Escherichia coli, but not in Bacillus subtilis. IMPORTANCE The use of metal ions represents a serious threat to the environment and to all living organisms because of the acute toxicity of these ions. Nowadays, silver nanoparticles are one of the most widely used nanoparticles in various industrial and health applications. The antimicrobial effect of nanoparticles is in part related to the released Ag+ ions and their ability to interact with bacterial membranes. Here, we identify, both in vitro and in vivo, specific targets of Ag+ ions within the membrane of bacteria. This include complexes involved in photosynthesis, but also complexes involved in respiration.
format	article
author	Reem Tambosi Sylviane Liotenberg Marie-Line Bourbon Anne-Soisig Steunou Marion Babot Anne Durand Nouari Kebaili Soufian Ouchane
author_facet	Reem Tambosi Sylviane Liotenberg Marie-Line Bourbon Anne-Soisig Steunou Marion Babot Anne Durand Nouari Kebaili Soufian Ouchane
author_sort	Reem Tambosi
title	Silver and Copper Acute Effects on Membrane Proteins and Impact on Photosynthetic and Respiratory Complexes in Bacteria
title_short	Silver and Copper Acute Effects on Membrane Proteins and Impact on Photosynthetic and Respiratory Complexes in Bacteria
title_full	Silver and Copper Acute Effects on Membrane Proteins and Impact on Photosynthetic and Respiratory Complexes in Bacteria
title_fullStr	Silver and Copper Acute Effects on Membrane Proteins and Impact on Photosynthetic and Respiratory Complexes in Bacteria
title_full_unstemmed	Silver and Copper Acute Effects on Membrane Proteins and Impact on Photosynthetic and Respiratory Complexes in Bacteria
title_sort	silver and copper acute effects on membrane proteins and impact on photosynthetic and respiratory complexes in bacteria
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/3ddb1587a0784c57ad925def426005fc
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Silver and Copper Acute Effects on Membrane Proteins and Impact on Photosynthetic and Respiratory Complexes in Bacteria

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