The response of Shewanella oneidensis MR-1 to Cr(III) toxicity differs from that to Cr(VI)

Chromium is a contaminant of concern that is found in drinking water in its soluble, hexavalent form [Cr(VI)] and that is known to be toxic to eukaryotes and prokaryotes. Trivalent chromium [Cr(III)] is thought to be largely harmless due to its low solubility and inability to enter cells. Previous w...

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Main Authors: Dorothy L Parker, Pirmin eBorer, Rizlan eBernier-Latmani
Format: Article
Language:English
Published: Frontiers Media S.A. 2011-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2011.00223/full
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spelling doaj-ef8dcf26846c4576bbcddd609b6eeb962020-11-24T21:28:41ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2011-11-01210.3389/fmicb.2011.0022314359The response of Shewanella oneidensis MR-1 to Cr(III) toxicity differs from that to Cr(VI)Dorothy L Parker0Dorothy L Parker1Pirmin eBorer2Rizlan eBernier-Latmani3Ecole Polytechnique Federale de LausanneScripps Institution of OceanographyEcole Polytechnique Federale de LausanneEcole Polytechnique Federale de LausanneChromium is a contaminant of concern that is found in drinking water in its soluble, hexavalent form [Cr(VI)] and that is known to be toxic to eukaryotes and prokaryotes. Trivalent chromium [Cr(III)] is thought to be largely harmless due to its low solubility and inability to enter cells. Previous work has suggested that Cr(III) may also be toxic to microorganisms but the mechanism remained elusive. In this work, we probe the toxicity of Cr(III) to Shewanella oneidensis MR-1, a bacterium able to reduce Cr(VI) to Cr(III) and compare it to Cr(VI) toxicity. We found evidence for Cr(III) toxicity both under Cr(VI) reducing conditions, during which Cr(III) was generated by the reduction process, and under non-reducing conditions, when Cr(III) was amended exogenously. Interestingly, cells exposed to Cr(III) (200 µM) experienced rapid viability loss as measured by colony-forming units on Luria-Bertani (LB) agar plates. In contrast, they maintained some enzymatic activity and cellular integrity. Cr(VI)-exposed cells exhibited loss of enzymatic activity and cell lysis. The loss of viability of Cr(III)-exposed cells was not due to membrane damage or to enzymatic inhibition but rather appeared to be associated with an abnormal morphology that consisted of chains of membrane-enclosed units of irregular size. Exposure of abnormal cells to growth conditions resulted in membrane damage and cell death, which is consistent with the observed viability loss on LB plates. While Cr(VI) was taken up intracellularly and caused cell lysis, the toxic effect of Cr(III) appeared to be associated with extracellular interactions leading to an ultimately lethal cell morphology.http://journal.frontiersin.org/Journal/10.3389/fmicb.2011.00223/fullcarboxyfluoresceinCcmC mutantchromatepropidium iodidetrivalent chromiumvital staining
collection DOAJ
language English
format Article
sources DOAJ
author Dorothy L Parker
Dorothy L Parker
Pirmin eBorer
Rizlan eBernier-Latmani
spellingShingle Dorothy L Parker
Dorothy L Parker
Pirmin eBorer
Rizlan eBernier-Latmani
The response of Shewanella oneidensis MR-1 to Cr(III) toxicity differs from that to Cr(VI)
Frontiers in Microbiology
carboxyfluorescein
CcmC mutant
chromate
propidium iodide
trivalent chromium
vital staining
author_facet Dorothy L Parker
Dorothy L Parker
Pirmin eBorer
Rizlan eBernier-Latmani
author_sort Dorothy L Parker
title The response of Shewanella oneidensis MR-1 to Cr(III) toxicity differs from that to Cr(VI)
title_short The response of Shewanella oneidensis MR-1 to Cr(III) toxicity differs from that to Cr(VI)
title_full The response of Shewanella oneidensis MR-1 to Cr(III) toxicity differs from that to Cr(VI)
title_fullStr The response of Shewanella oneidensis MR-1 to Cr(III) toxicity differs from that to Cr(VI)
title_full_unstemmed The response of Shewanella oneidensis MR-1 to Cr(III) toxicity differs from that to Cr(VI)
title_sort response of shewanella oneidensis mr-1 to cr(iii) toxicity differs from that to cr(vi)
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2011-11-01
description Chromium is a contaminant of concern that is found in drinking water in its soluble, hexavalent form [Cr(VI)] and that is known to be toxic to eukaryotes and prokaryotes. Trivalent chromium [Cr(III)] is thought to be largely harmless due to its low solubility and inability to enter cells. Previous work has suggested that Cr(III) may also be toxic to microorganisms but the mechanism remained elusive. In this work, we probe the toxicity of Cr(III) to Shewanella oneidensis MR-1, a bacterium able to reduce Cr(VI) to Cr(III) and compare it to Cr(VI) toxicity. We found evidence for Cr(III) toxicity both under Cr(VI) reducing conditions, during which Cr(III) was generated by the reduction process, and under non-reducing conditions, when Cr(III) was amended exogenously. Interestingly, cells exposed to Cr(III) (200 µM) experienced rapid viability loss as measured by colony-forming units on Luria-Bertani (LB) agar plates. In contrast, they maintained some enzymatic activity and cellular integrity. Cr(VI)-exposed cells exhibited loss of enzymatic activity and cell lysis. The loss of viability of Cr(III)-exposed cells was not due to membrane damage or to enzymatic inhibition but rather appeared to be associated with an abnormal morphology that consisted of chains of membrane-enclosed units of irregular size. Exposure of abnormal cells to growth conditions resulted in membrane damage and cell death, which is consistent with the observed viability loss on LB plates. While Cr(VI) was taken up intracellularly and caused cell lysis, the toxic effect of Cr(III) appeared to be associated with extracellular interactions leading to an ultimately lethal cell morphology.
topic carboxyfluorescein
CcmC mutant
chromate
propidium iodide
trivalent chromium
vital staining
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2011.00223/full
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