The highly toxic oxyanion tellurite (TeO 3 2− ) enters the phototrophic bacterium Rhodobacter capsulatus via an as yet uncharacterized monocarboxylate transport system

Abstract

The facultative phototroph Rhodobacter capsulatus takes up the highly toxic oxyanion tellurite when grown under both photosynthetic and respiratory growth conditions. Previous works on Escherichia coli and R. capsulatus suggested that tellurite uptake occurred through a phosphate transporter. Here we present evidences indicating that tellurite enters R. capsulatus cells via a monocarboxylate transport system. Indeed, intracellular accumulation of tellurite was inhibited by the addition of monocarboxylates such as pyruvate, lactate and acetate, but not by dicarboxylates like malate or succinate. Acetate was the strongest tellurite uptake antagonist and this effect was concentration dependent, being already evident at 1 microM acetate. Conversely, tellurite at 100 microM was able to restrict the acetate entry into the cells. Both tellurite and acetate uptakes were energy dependent processes, since they were abolished by the protonophore FCCP and by the respiratory electron transport inhibitor KCN. Interestingly, cells grown on acetate, lactate or pyruvate showed a high level resistance to tellurite, whereas cells grown on malate or succinate proved to be very sensitive to the oxyanion. Taking these data together, we propose that: (a) tellurite enters R. capsulatus cells via an as yet uncharacterized monocarboxylate(s) transporter, (b) competition between acetate and tellurite results in a much higher level of tolerance against the oxyanion and (c) the toxic action of tellurite at the cytosolic level is significantly restricted by preventing tellurite uptake.

Acetate Permease (ActP) Is Responsible for Tellurite (TeO 3 2− ) Uptake and Resistance in Cells of the Facultative Phototroph Rhodobacter capsulatus

“…The link between tellurite uptake and toxicity in bacterial cells has been previously discussed in a limited number of reports (2,3,7). In Escherichia coli, it was shown that mutations in a phosphate transport system confer a high level of resistance to tellurite and that the oxyanion competes very efficiently for 32 P i transport (7).…”

“…Finally, in the phototrophic species Rhodobacter capsulatus it was suggested that a phosphate transporter might also be responsible for tellurite uptake (3). This hypothesis has recently been questioned because of the extremely high concentration of P i needed to significantly inhibit tellurite uptake (2). Conversely, acetate was found to decrease the uptake of tellurite, when present at concentrations as low as 1 M (2).…”

“…Conversely, acetate was found to decrease the uptake of tellurite, when present at concentrations as low as 1 M (2). This finding, along with the fact that lactate and pyruvate, but not malate and succinate, act similarly as competitors of tellurite uptake, led to the proposal that, in R. capsulatus, the oxyanion enters the cell via a monocarboxylate transport system (2).…”

Fructose increases the resistance of Rhodobacter capsulatus to the toxic oxyanion tellurite through repression of acetate permease (ActP)

“…Little is known concerning the biochemical interaction between microbial cells and tellurite although it has been suggested that tellurite exerts its toxic action in the cytoplasmic compartment by triggering an increase in the generation of reactive oxygen species (Borsetti et al 2005;Pérez et al 2007). This implies that the uptake of the oxyanion by the cell is a prerequisite for the full development of its toxicity although the link between tellurite uptake and toxicity in bacterial cells has only been investigated in a limited number of reports (Borghese et al 2008;Borsetti et al 2003;Tomás and Kay 1986;Turner et al 2007;Turner et al 1995).…”

“…Notably, photosynthetic-anaerobically grown cells show a very high minimal inhibitory concentration (MIC) for tellurite ([800 lM) while dark-aerobically grown cells show an extremely low MIC for tellurite (%8 lM) (Borghese et al 2004). It was shown that intermediates of the TCA cycle such as malate, succinate or fumarate, when used as growth carbon sources, make the cells very sensitive to tellurite; conversely, other metabolites such as pyruvate or acetate drastically increase the MIC for the oxyanion by competing with tellurite for the same entry port (Borghese et al 2008), which has been identified as an acetate permease (ActP) (Borghese and Zannoni 2010).…”