From cyanobacteria and cyanophages to chloroplasts: the fate of the genomes of oxyphototrophs and the genes encoding photosystem II proteins

New Phytol. 2024 May;242(3):1055-1067. doi: 10.1111/nph.19633. Epub 2024 Mar 5.

Abstract

Chloroplasts are the result of endosymbiosis of cyanobacterial organisms with proto-eukaryotes. The psbA, psbD and psbO genes are present in all oxyphototrophs and encode the D1/D2 proteins of photosystem II (PSII) and PsbO, respectively. PsbO is a peripheral protein that stabilizes the O2-evolving complex in PSII. Of these genes, psbA and psbD remained in the chloroplastic genome, while psbO was transferred to the nucleus. The genomes of selected cyanobacteria, chloroplasts and cyanophages carrying psbA and psbD, respectively, were analysed. The highest density of genes and coding sequences (CDSs) was estimated for the genomes of cyanophages, cyanobacteria and chloroplasts. The synonymous mutation rate (rS) of psbA and psbD in chloroplasts remained almost unchanged and is lower than that of psbO. The results indicate that the decreasing genome size in chloroplasts is more similar to the genome reduction observed in contemporary endosymbiotic organisms than in streamlined genomes of free-living cyanobacteria. The rS of atpA, which encodes the α-subunit of ATP synthase in chloroplasts, suggests that psbA and psbD, and to a lesser extent psbO, are ancient and conservative and arose early in the evolution of oxygenic photosynthesis. The role of cyanophages in the evolution of oxyphototrophs and chloroplastic genomes is discussed.

Keywords: bacteriophages; cyanobacteria; endosymbiosis; evolution; photosynthesis; plastids; viruses.

MeSH terms

  • Chloroplasts / genetics
  • Chloroplasts / metabolism
  • Cyanobacteria* / genetics
  • Cyanobacteria* / metabolism
  • Eukaryota / metabolism
  • Photosynthesis / genetics
  • Photosystem II Protein Complex* / genetics
  • Photosystem II Protein Complex* / metabolism

Substances

  • Photosystem II Protein Complex