Open Access Research

Diversity and evolution of phycobilisomes in marine Synechococcus spp.: a comparative genomics study

Christophe Six12, Jean-Claude Thomas3, Laurence Garczarek1, Martin Ostrowski4, Alexis Dufresne1, Nicolas Blot1, David J Scanlan4 and Frédéric Partensky1*

Author Affiliations

1 UMR 7144 Université Paris VI and CNRS, Station Biologique, Groupe Plancton Océanique, F-29682 Roscoff cedex, France

2 Mount Allison University, Photosynthetic Molecular Ecophysiology Group, Biology Department, E4L 1G7 Sackville, New Brunswick, Canada

3 UMR 8186 CNRS and Ecole Normale Supérieure, Biologie Moléculaire des Organismes Photosynthétiques, F-75230 Paris, France

4 Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, UK

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Genome Biology 2007, 8:R259  doi:10.1186/gb-2007-8-12-r259

Published: 5 December 2007

Abstract

Background

Marine Synechococcus owe their specific vivid color (ranging from blue-green to orange) to their large extrinsic antenna complexes called phycobilisomes, comprising a central allophycocyanin core and rods of variable phycobiliprotein composition. Three major pigment types can be defined depending on the major phycobiliprotein found in the rods (phycocyanin, phycoerythrin I or phycoerythrin II). Among strains containing both phycoerythrins I and II, four subtypes can be distinguished based on the ratio of the two chromophores bound to these phycobiliproteins. Genomes of eleven marine Synechococcus strains recently became available with one to four strains per pigment type or subtype, allowing an unprecedented comparative genomics study of genes involved in phycobilisome metabolism.

Results

By carefully comparing the Synechococcus genomes, we have retrieved candidate genes potentially required for the synthesis of phycobiliproteins in each pigment type. This includes linker polypeptides, phycobilin lyases and a number of novel genes of uncharacterized function. Interestingly, strains belonging to a given pigment type have similar phycobilisome gene complements and organization, independent of the core genome phylogeny (as assessed using concatenated ribosomal proteins). While phylogenetic trees based on concatenated allophycocyanin protein sequences are congruent with the latter, those based on phycocyanin and phycoerythrin notably differ and match the Synechococcus pigment types.

Conclusion

We conclude that the phycobilisome core has likely evolved together with the core genome, while rods must have evolved independently, possibly by lateral transfer of phycobilisome rod genes or gene clusters between Synechococcus strains, either via viruses or by natural transformation, allowing rapid adaptation to a variety of light niches.