Naturally zinc-containing bacteriochlorophyll a ([Zn]-BChl a) protects the photosynthetic apparatus of Acidiphilium rubrum from copper toxicity damage

Abstract

In almost all photosynthetic organisms the photosynthetic pigments chlorophyll and bacteriochlorophyll (BChl) are Mg²⁺ containing complexes, but Mg²⁺ may be exchanged against other metal ions when these are present in toxic concentrations, leading to inactivation of photosynthesis. In this report we studied mechanisms of copper toxicity to the photosynthetic apparatus of Acidiphilium rubrum, an acidophilic purple bacterium that uses Zn²⁺ instead of Mg²⁺ as the central metal in the BChl molecules ([Zn]-BChl) of its reaction centres (RCs) and light harvesting proteins (LH1). We used a combination of in vivo measurements of photosynthetic activity (fast fluorescence and absorption kinetics) together with analysis of metal binding to pigments and pigment-protein complexes by HPLC-ICP-sfMS to monitor the effect of Cu²⁺ on photosynthesis of A. rubrum. Further, we found that its cytoplasmic pH is neutral. We compared these results with those obtained from Rhodospirillum rubrum, a purple bacterium for which we previously reported that the central Mg²⁺ of BChl can be replaced in vivo in the RCs by Cu²⁺ under environmentally realistic Cu²⁺ concentrations, leading to a strong inhibition of photosynthesis. Thus, we observed that A. rubrum is much more resistant to copper toxicity than R. rubrum. Only slight changes of photosynthetic parameters were observed in A. rubrum at copper concentrations that were severely inhibitory in R. rubrum and in A. rubrum no copper complexes of BChl were found. Altogether, the data suggest that [Zn]-BChl protects the photosynthetic apparatus of A. rubrum from detrimental insertion of Cu²⁺ (trans-metallation) into BChl molecules of its RCs.

Keywords: Acidiphilium rubrum; Bacteriochlorophyll; Copper stress; Photosynthetic bacteria; Pigment-protein complexes; Reaction centre; Rhodospirillum rubrum; Trans-metallation.