Abstract
Copper is a highly reactive, toxic metal; consequently, transport of this metal within the cell is tightly regulated. Intriguingly, the actinobacterium Kineococcus radiotolerans has been shown to not only accumulate soluble copper to high levels within the cytoplasm, but the phenotype also correlated with enhanced cell growth during chronic exposure to ionizing radiation. This study offers a first glimpse into the physiological and proteomic responses of K. radiotolerans to copper at increasing concentration and distinct growth phases. Aerobic growth rates and biomass yields were similar over a range of Cu(II) concentrations (0–1.5 mM) in complex medium. Copper uptake coincided with active cell growth and intracellular accumulation was positively correlated with Cu(II) concentration in the growth medium (R2 = 0.7). Approximately 40% of protein coding ORFs on the K. radiotolerans genome were differentially expressed in response to the copper treatments imposed. Copper accumulation coincided with increased abundance of proteins involved in oxidative stress and defense, DNA stabilization and repair, and protein turnover. Interestingly, the specific activity of superoxide dismutase was repressed by low to moderate concentrations of copper during exponential growth, and activity was unresponsive to perturbation with paraquot. The biochemical response pathways invoked by sub-lethal copper concentrations are exceptionally complex; though integral cellular functions are preserved, in part, through the coordination of defense enzymes, chaperones, antioxidants and protective osmolytes that likely help maintain cellular redox. This study extends our understanding of the ecology and physiology of this unique actinobacterium that could potentially inspire new biotechnologies in metal recovery and sequestration, and environmental restoration.
Highlights
IntroductionK. radiotolerans is resistant to c-irradiation, prolonged desiccation, and strong oxidants [1,10]; attributes that are consistent with the known ecological distributions of these actinobacteria
Kineococcus radiotolerans was isolated within a shielded cell work area containing highly radioactive nuclear waste at the U.S Department of Energy’s Savannah River Site in Aiken, SC, USA [1]
K. radiotolerans is resistant to c-irradiation, prolonged desiccation, and strong oxidants [1,10]; attributes that are consistent with the known ecological distributions of these actinobacteria
Summary
K. radiotolerans is resistant to c-irradiation, prolonged desiccation, and strong oxidants [1,10]; attributes that are consistent with the known ecological distributions of these actinobacteria. K. radiotolerans was recently shown to and actively accumulate soluble copper within the cytoplasm and more intriguingly, colony formation was stimulated on solid plating medium supplemented with copper (100 mM final concentration) during chronic irradiation [10]. Copper is extremely toxic; cells exert strict homeostatic control over membrane transport and intracellular trafficking [13,14]. Because of its reactivity as a redox active metal capable of participating in Fenton/Haber-Weiss reactions and the inherent toxicity of the metal; free, unbound copper is virtually absent within the cytoplasm of unstressed cells [14]. The intracellular fate of copper within K. radiotolerans has not been determined
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