The cyanobacterial genome core and the origin of photosynthesis

doi:10.1073/pnas.0605709103

The cyanobacterial genome core and the origin of photosynthesis

*School of Physics, University of Osnabrück, D-49069 Osnabrück, Germany;
^‡A. N. Belozersky Institute of Physico–Chemical Biology, Moscow State University, Moscow 119899, Russia;
^§National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894;
^¶Station Biologique, Unité Mixte de Recherche 7144, Centre National de la Recherche Scientifique et Université Paris 6, BP74, F-29682 Roscoff Cedex, France;
^‖Integrated Genomics, Inc., Chicago, IL 60612; and
**Department of Molecular Genetics and Cell Biology, University of Chicago, 920 East 58th Street, Chicago, IL 60637

Contributed by Robert Haselkorn, July 14, 2006

Abstract

Comparative analysis of 15 complete cyanobacterial genome sequences, including “near minimal” genomes of five strains of Prochlorococcus spp., revealed 1,054 protein families [core cyanobacterial clusters of orthologous groups of proteins (core CyOGs)] encoded in at least 14 of them. The majority of the core CyOGs are involved in central cellular functions that are shared with other bacteria; 50 core CyOGs are specific for cyanobacteria, whereas 84 are exclusively shared by cyanobacteria and plants and/or other plastid-carrying eukaryotes, such as diatoms or apicomplexans. The latter group includes 35 families of uncharacterized proteins, which could also be involved in photosynthesis. Only a few components of cyanobacterial photosynthetic machinery are represented in the genomes of the anoxygenic phototrophic bacteria Chlorobium tepidum, Rhodopseudomonas palustris, Chloroflexus aurantiacus, or Heliobacillus mobilis. These observations, coupled with recent geological data on the properties of the ancient phototrophs, suggest that photosynthesis originated in the cyanobacterial lineage under the selective pressures of UV light and depletion of electron donors. We propose that the first phototrophs were anaerobic ancestors of cyanobacteria (“procyanobacteria”) that conducted anoxygenic photosynthesis using a photosystem I-like reaction center, somewhat similar to the heterocysts of modern filamentous cyanobacteria. From procyanobacteria, photosynthesis spread to other phyla by way of lateral gene transfer.

Footnotes

^†To whom correspondence may be addressed: E-mail: amulkid{at}uos.de, r-haselkorn{at}uchicago.edu, or galperin{at}ncbi.nlm.nih.gov
Author contributions: A.Y.M., E.V.K., and M.Y.G. designed research; A.Y.M., E.V.K., K.S.M., S.L.M., A.S., Y.I.W., A.D., F.P., D.K., and M.Y.G. performed research; H.B., D.K., and M.Y.G. contributed new reagents/analytic tools; A.Y.M., E.V.K., K.S.M., S.L.M., A.S., Y.I.W., A.D., F.P., D.K., R.H., and M.Y.G. analyzed data; and A.Y.M., E.V.K., A.D., F.P., R.H., and M.Y.G. wrote the paper.
Conflict of interest statement: No conflicts declared.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. DQ831217–DQ831236).
Abbreviations::

CyOGs,

cyanobacterial clusters of orthologous groups of proteins;

LGT,

lateral gene transfer;

PSI,

photosystem I;

PSII,

photosystem II;

RC,

reaction center.
Freely available online through the PNAS open access option.