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Oxidative stress tolerance is manganese (Mn²⁺) regulated in Streptococcus gordonii

Oral Microbiology Unit, Department of Oral and Dental Science, University of Bristol Dental School, Lower Maudlin Street, Bristol BS1 2LY, UK¹
Department of Pharmacy and Pharmacology, University of Bath, Bath BA2 7AY, UK²

Author for correspondence: Howard F. Jenkinson. Tel: +44 117 928 4358. Fax: +44 117 928 4313. e-mail: howard.jenkinson{at}bris.ac.uk

The Sca permease in the oral bacterium Streptococcus gordonii is a member of a family of ATP-binding cassette (ABC)-type transporters for manganese (Mn²⁺) and related cations that are associated with streptococcal virulence in a number of infection models. Since Mn²⁺ has a protective function against oxidative damage in a variety of bacteria, we have investigated the role of Sca permease in oxidative stress tolerance in Streptococcus gordonii. A single Mn²⁺-dependent superoxide dismutase (SOD), encoded by sodA, is expressed by S. gordonii and was >10-fold up-regulated under oxidative stress conditions. Inactivation of sodA resulted in increased susceptibility of S. gordonii cells to growth inhibition by dioxygen (O₂), and to killing by paraquat (a superoxide anion generator) and by hydrogen peroxide (H₂O₂). Expression of thiol peroxidase, encoded by the tpx gene located immediately downstream of the scaCBA operon, was also up-regulated under oxidative conditions. Inactivation of tpx led to increased susceptibility of cells to H₂O₂, but not to O₂ or paraquat. In low-Mn²⁺ medium (0·01 µM Mn²⁺) sodA and tpx genes were transcriptionally down-regulated, SOD activity was reduced and cells were more sensitive to growth inhibition by O₂. A Sca permease-deficient (scaC) mutant showed further reduced SOD activity and hypersensitivity to O₂ in medium containing <0·1 µM Mn²⁺. These results demonstrate that the Sca (Mn²⁺) permease in S. gordonii is essential for protection against oxidative stress.

Keywords: manganese transport, oral streptococci, peroxide, reactive oxygen species

Abbreviations: NBT, nitro-blue tetrazolium; ROS, reactive oxygen species; SOD, superoxide dismutase

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