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Open Access Research article

Copper tolerance mediated by polyphosphate degradation and low-affinity inorganic phosphate transport system in Escherichia coli

Mariana Grillo-Puertas1, Lici Ariane Schurig-Briccio12, Luisa Rodríguez-Montelongo1, María Regina Rintoul1 and Viviana Andrea Rapisarda1*

Author Affiliations

1 Instituto Superior de Investigaciones Biológicas, INSIBIO (CONICET-UNT) and Instituto de Química Biológica “Dr Bernabé Bloj”, Facultad de Bioquímica, Química y Farmacia (UNT), Chacabuco 461 CP T4000ILI, Tucumán, Argentina

2 Present address: Department of Biochemistry, University of Illinois, Urbana IL61801, USA

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BMC Microbiology 2014, 14:72  doi:10.1186/1471-2180-14-72

Published: 19 March 2014

Abstract

Background

Metal tolerance in bacteria has been related to polyP in a model in which heavy metals stimulate the polymer hydrolysis, forming metal-phosphate complexes that are exported. As previously described in our laboratory, Escherichia coli cells grown in media containing a phosphate concentration >37 mM maintained an unusually high polyphosphate (polyP) level in stationary phase. The aim of the present work was to evaluate the influence of polyP levels as the involvement of low-affinity inorganic phosphate transport (Pit) system in E. coli copper tolerance.

Results

PolyP levels were modulated by the media phosphate concentration and/or using mutants in polyP metabolism. Stationary phase wild-type cells grown in high phosphate medium were significantly more tolerant to copper than those grown in sufficient phosphate medium. Copper addition to tolerant cells induced polyP degradation by PPX (an exopolyphosphatase), phosphate efflux and membrane polarization. ppkppx (unable to synthesize/degrade polyP), ppx (unable to degrade polyP) and Pit system mutants were highly sensitive to metal even in high phosphate media. In exponential phase, CopA and polyP-Pit system would act simultaneously to detoxify the metal or one could be sufficient to safeguard the absence of the other.

Conclusions

Our results support a mechanism for copper detoxification in exponential and stationary phases of E. coli, involving Pit system and degradation of polyP. Data reflect the importance of the environmental phosphate concentration in the regulation of the microbial physiological state.

Keywords:
Escherichia coli; Copper tolerance; Stationary phase; Polyphosphate; Inorganic phosphate