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Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria

Alexis Dufresne12, Martin Ostrowski3, David J Scanlan3, Laurence Garczarek1, Sophie Mazard3, Brian P Palenik4, Ian T Paulsen5, Nicole Tandeau de Marsac6, Patrick Wincker7, Carole Dossat7, Steve Ferriera8, Justin Johnson8, Anton F Post9, Wolfgang R Hess10 and Frédéric Partensky1*

Author Affiliations

1 Université Paris 6 and CNRS, UMR 7144, Station Biologique, 29682 Roscoff, France

2 Université Rennes 1, UMR 6553 EcoBio, IFR90/FR2116, CAREN, 35042 Rennes, France

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

4 Scripps Institution of Oceanography, UCSD, San Diego, CA 92093, USA

5 Department of Chemistry and Biomolecular Sciences, Macquarie University, Sydney, NSW, Australia 2109

6 Institut Pasteur, Dépt de Microbiologie, Unité des Cyanobactéries, URA 2172 CNRS, Paris, France

7 Genoscope (CEA) and UMR 8030 CNRS-Genoscope-Université d'Evry, 91057 Evry, France

8 J Craig Venter Institute, Rockville, MD 20850, USA

9 The Interuniversity Institute for Marine Science, Hebrew University, Eilat 88103, Israel

10 University of Freiburg, Faculty of Biology, D-79104 Freiburg, Germany

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Genome Biology 2008, 9:R90  doi:10.1186/gb-2008-9-5-r90

Published: 28 May 2008

Abstract

Background

The picocyanobacterial genus Synechococcus occurs over wide oceanic expanses, having colonized most available niches in the photic zone. Large scale distribution patterns of the different Synechococcus clades (based on 16S rRNA gene markers) suggest the occurrence of two major lifestyles ('opportunists'/'specialists'), corresponding to two distinct broad habitats ('coastal'/'open ocean'). Yet, the genetic basis of niche partitioning is still poorly understood in this ecologically important group.

Results

Here, we compare the genomes of 11 marine Synechococcus isolates, representing 10 distinct lineages. Phylogenies inferred from the core genome allowed us to refine the taxonomic relationships between clades by revealing a clear dichotomy within the main subcluster, reminiscent of the two aforementioned lifestyles. Genome size is strongly correlated with the cumulative lengths of hypervariable regions (or 'islands'). One of these, encompassing most genes encoding the light-harvesting phycobilisome rod complexes, is involved in adaptation to changes in light quality and has clearly been transferred between members of different Synechococcus lineages. Furthermore, we observed that two strains (RS9917 and WH5701) that have similar pigmentation and physiology have an unusually high number of genes in common, given their phylogenetic distance.

Conclusion

We propose that while members of a given marine Synechococcus lineage may have the same broad geographical distribution, local niche occupancy is facilitated by lateral gene transfers, a process in which genomic islands play a key role as a repository for transferred genes. Our work also highlights the need for developing picocyanobacterial systematics based on genome-derived parameters combined with ecological and physiological data.