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Iron and Copper Act Synergistically To Delay Anaerobic Growth of Bacteria

Bird, Lina J. and Coleman, Maureen L. and Newman, Dianne K. (2013) Iron and Copper Act Synergistically To Delay Anaerobic Growth of Bacteria. Applied and Environmental Microbiology, 79 (12). pp. 3619-3627. ISSN 0099-2240. PMCID PMC3675935. http://resolver.caltech.edu/CaltechAUTHORS:20130709-082907927

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Abstract

Transition metals are known to cause toxic effects through their interaction with oxygen, but toxicity under anoxic conditions is poorly understood. Here we investigated the effects of iron (Fe) and copper (Cu) on the anaerobic growth and gene expression of the purple phototrophic bacterium Rhodopseudomonas palustris TIE-1. We found that Fe(II) and Cu(II) act synergistically to delay anaerobic growth at environmentally relevant metal concentrations. Cu(I) and Cu(II) had similar effects both alone and in the presence of ascorbate, a Cu(II) reductant, indicating that reduction of Cu(II) to Cu(I) by Fe(II) is not sufficient to explain the growth inhibition. Addition of Cu(II) increased the toxicity of Co(II) and Ni(II); in contrast, Ni(II) toxicity was diminished in the presence of Fe(II). The synergistic anaerobic toxicity of Fe(II) and Cu(II) was also observed for Escherichia coli MG1655, Shewanella oneidensis MR-1, and Rhodobacter capsulatus SB1003. Gene expression analyses for R. palustris identified three regulatory genes that respond to Cu(II) and not to Fe(II): homologs of cueR and cusR, two known proteobacterial copper homeostasis regulators, and csoR, a copper regulator recently identified in Mycobacterium tuberculosis. Two P-type ATPase efflux pumps, along with an F_oF_1 ATP synthase, were also upregulated by Cu(II) but not by Fe(II). An Escherichia coli mutant deficient in copA, cus, and cueO showed a smaller synergistic effect, indicating that iron might interfere with one or more of the copper homeostasis systems. Our results suggest that interactive effects of transition metals on microbial physiology may be widespread under anoxic conditions, although the molecular mechanisms remain to be more fully elucidated.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1128/AEM.03944-12DOIArticle
http://aem.asm.org/content/79/12/3619PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3675935/PubMed CentralArticle
ORCID:
AuthorORCID
Newman, Dianne K.0000-0003-1647-1918
Additional Information:© 2013 American Society for Microbiology. Received 6 January 2013 Accepted 27 March 2013. Published ahead of print 5 April 2013. We thank Nathan F. Dalleska (Caltech Environmental Analysis Center) for obtaining the ICP-MS data, Vijaya Kumar and Igor Antoshechkin (Caltech Millard and Muriel Jacobs Genetics and Genomics Laboratory) for microarray preparation, and Jim Imlay (UIUC) for helpful discussion and for E. coli strains. The Howard Hughes Medical Institute (HHMI) supported this work. D.K.N. is an HHMI Investigator.
Funders:
Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
PubMed Central ID:PMC3675935
Record Number:CaltechAUTHORS:20130709-082907927
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20130709-082907927
Official Citation:Iron and Copper Act Synergistically To Delay Anaerobic Growth of Bacteria Lina J. Bird, Maureen L. Coleman, and Dianne K. Newman Appl. Environ. Microbiol. June 2013 79:12 3619-3627; published ahead of print 5 April 2013, doi:10.1128/AEM.03944-12
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:39259
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:16 Jul 2013 23:15
Last Modified:24 Oct 2017 16:19

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