Regulation, unique gene organization, and unusual primary structure of carbon fixation genes from a marine phycoerythrin-containing cyanobacterium.

Marine phycoerythrin-containing cyanobacteria are major contributors to the overall productivity of the oceans. The present study indicates that the structural genes of the carbon assimilatory system are unusually arranged and possess a unique primary structure compared to previously studied cyanobacteria. Southern blot analyses of Synechococcus sp. strain WH7803 chromosomal DNA digests, using the ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) large subunit gene from Synechococcus sp. strain PCC6301 as a heterologous probe, revealed the presence of a 6.4 kb HindIII fragment that was detectable at only low stringency. Three complete open reading frames (ORFs) were detected within this fragment. Two of these ORFs potentially encode the Synechococcus sp. strain WH7803 rbcL and rbcS genes. The third ORF, situated immediately upstream from rbcL, potentially encodes a homologue of the ccmK gene from Synechococcus sp. strain PCC7942. The deduced amino acid sequences of each of these ORFs are more similar to homologues among the beta/gamma purple bacteria than to existing cyanobacterial homologues and phylogenetic analysis of the Rubisco large and small subunit sequences confirmed an unexpected relationship to sequences from among the beta/gamma purple bacteria. This is the first instance in which the possibility has been considered that an operon encoding three genes involved in carbon fixation may have been laterally transferred from a purple bacterium. Analysis of mRNA extracted from cells grown under diel conditions indicated that rbcL, rbcS and ccmK were regulated at the transcriptional level; specifically Rubisco transcripts were highest during the midday period, decreased at later times during the light period and eventually reached a level where they were all but undetectable during the dark period. Primer extension analysis indicated that the ccmK, rbcL and rbcS genes were co-transcribed.