Structure, organization and expression of cyanobacterial ATP synthase genes

Abstract

The genes encoding the nine polypeptides of the ATP synthase from Synechococcus sp. PCC 6301, a unicellular cyanobacterium, and Anabaena sp. PCC 7120, a filamentous cyanobacterium, have recently been isolated and their sequences determined. These represent the first such sequences available from procaryotic organisms that perform oxygenic photosynthesis. Similar to the organization in chloroplasts, the ATP synthase genes of both cyanobacteria are arranged in two gene clusters which are not closely linked in the chromosome. Three of the genes located in one cluster in cyanobacteria, however, are localized in the nuclear rather than the chloroplast genomes of plants. The cyanobacterial ATP synthase genes are ordered in the same manner as those in the single gene cluster of Escherichia coli. Cyanobacteria contain an additional gene denoted atpG which appears to be a duplicated and diverged from of the atpF gene. The larger cyanobacterial cluster, atp 1, is comprised of eight ATP synthase subunit genes arranged in the order atpI-atpH-atpG-atpF-atpD-atpA-atpC. An overlap between the atpF and atpD gene coding regions observed in Anabaena sp. PCC 7120 is absent in both Synechococcus sp. PCC 6301 and E. coli. The second cluster of genes, atp 2, contains the remaining two ATP synthase genes in the order atpB-atpE. Unlike the situation in many chloroplast genomes, this gene pair does not overlap in either cyanobacterial species. In Anabaena sp. PCC 7120, atp 1 and atp 2 each comprise an operon and the transcription initiation sites for each gene cluster have been identified. The cyanobacterial ATP synthase subunits are much more closely related in sequence to the equivalent polypeptides from chloroplasts than they are to those of E. coli. The similarity in chloroplast and cyanobacterial ATP synthase subunit sequences and gene oreganization argue strongly for an endosymbiotic origin for plant chloroplasts.