The structure and gene repertoire of an ancient red algal plastid genome

Photosynthetic eukaryotes can, according to features of their chloroplasts, be divided into two major groups: the red and the green lineage of plastid evolution. To extend the knowledge about the evolution of the red lineage we have sequenced and analyzed the chloroplast genome (cp-genome) of Cyanid ium caldarium RK1, a unicellular red alga (AF022186). The analysis revealed that this genome shows several unusual structural features, such as a hypo thetical hairpin structure in a gene-free region and absence of large repea t units. We provide evidence that this structural organization of the cp-ge nome of C. caldarium may be that of the most ancient cp-genome so far descr ibed. We also compared the cp-genome of C, caldarium to the other known cp- genomes of the red lineage. The cp-genome of C. caldarium cannot be readily aligned with that of Porphyra purpurea, a multicellular red alga, or Guill ardia theta due to a displacement of a region of the cp-genome. The phyloge netic tree reveals that the secondary endosymbiosis, through which G. theta evolved, took place after the separation of the ancestors of C. caldarium and P. purpurea. We found several genes unique to the cp-genome of C. caldarium. Five of the m seem to be involved in the building of bacterial cell envelopes and may b e responsible for the thermotolerance of the chloroplast of this alga. Two additional genes may play a role in stabilizing the photosynthetic machiner y against salt stress and detoxification of the chloroplast. Thus, these ge nes may be unique to the cp-genome of C. caldarium and may be required for the endurance of the extreme living conditions of this alga.