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MBE Advance Access originally published online on July 13, 2005
Molecular Biology and Evolution 2005 22(11):2179-2189; doi:10.1093/molbev/msi216
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Published by Oxford University Press 2005.

Research Article

Protein Interactions Limit the Rate of Evolution of Photosynthetic Genes in Cyanobacteria

Tuo Shi*, Thomas S. Bibby*, Lin Jiang*, Andrew J. Irwin*,1 and Paul G. Falkowski*,{dagger}

* Environmental Biophysics and Molecular Ecology Program, Institute of Marine and Coastal Sciences, Rutgers University; and {dagger} Department of Geological Sciences, Rutgers University

E-mail: falko{at}imcs.rutgers.edu.

Using a bioinformatic approach, we analyzed the correspondence in genetic distance matrices between all possible pairwise combinations of 82 photosynthetic genes in 10 species of cyanobacteria. Our analysis reveals significant correlations between proteins linked in a conserved gene order and between structurally identified interacting protein scaffolds that coordinate the binding of cofactors involved in photosynthetic electron transport. Analyses of amino acid substitution rates suggest that the tempo of evolution of genes encoding core metabolic processes in the photosynthetic apparatus is highly constrained by protein-protein, protein-lipid, and protein-cofactor interactions (collectively called "protein interactions"). These interactions are critical for energy transduction, primary charge separation, and electron transport and effectively act as an internal selection pressure governing the conservation of clusters of photosynthetic genes in oxygenic prokaryotic photoautotrophs. Consequently, although several proteins within the photosynthetic apparatus are biophysically and physiologically inefficient, selection has not significantly altered the genes encoding these essential proteins over billions of years of evolution. In effect, these core proteins have become "frozen metabolic accidents."

Key Words: cyanobacteria • photosynthesis • coevolution • bioinformatics • gene order • protein-protein interactions


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