The organization and sequence of the genes for ATP synthase subunits in the cyanobacterium Synechococcus 6301 : Support for an endosymbiotic origin of chloroplasts

Abstract

The nucleotide sequence has been determined of two regions of DNA cloned from the cyanobacterium Synechococcus 6301. The larger, 8890 base-pairs in length, contains a cluster of seven genes for subunits of ATP synthase. The order of the genes is a:c:b′:b:δ:α:γ, b′ being a duplicated and diverged form of b. As in the Escherichia coli unc operon, the a gene is preceded by a gene for a small hydrophobic and basic protein. The hydrophobic profile of the potential gene product suggests that its secondary structure is similar to the uncI protein. The smaller DNA fragment, 4737 base-pairs in length, is separated from the larger by at least 15 × 10 3 base-pairs of DNA. It contains a cluster of two genes encoding ATP synthase subunits β and ɛ. Both clusters of ATP synthase genes are preceded by sequences resembling the −10 (Pribnow) ☐ of E. coli promoters and are followed by sequences able to form stable stem-loop structures that might serve to terminate transcription. These features and the small intergenic non-coding sequences suggest that the clusters are operons, for which the names atp1 and atp2 are proposed. The order of genes within the two clusters is very similar to the gene order in the E. coli unc operon. However, it is most closely related to the arrangement of genes for ATP synthase subunits a:c:b:αandβ:ɛ in two clusters in pea chloroplast DNA. This close relationship between chloroplasts and the cyanobacterium is also evident from comparisons of the sequences of ATP synthase subunits; the Synechococcus proteins are much more closely related to chloroplast homologues than to those in other bacteria or in mitochondria. It is further supported by the cyanobacterial b and b′ proteins which, in common with their chloroplast counterpart, subunit I, have extra amino-terminal extensions relative to the E. coli b protein. This extension is known to be removed by post-translational processing in the chloroplast, but its function is obscure. It also seems likely that the cyanobacterial and chloroplast ATP synthases have important similarities in subunit composition. For example, the presence of two related genes, b and b′, in the cyanobacterium suggests that its ATP synthase is a complex of nine polypeptides, and that it may have single copies of related b and b′ proteins rather than two copies of identical b subunits as found in the E. coli enzyme. Existing data on chloroplast enzymes are compatible with a similar structure. Thus, these similarities between the ATP synthase genes and the proteins they encode in Synechococcus and in chloroplasts are strong molecular evidence that cyanobacteria and chloroplasts have a common origin, and support an endosymbiotic origin for the organelle.