Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria.

International audience 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...

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Published in:Genome Biology
Main Authors: Dufresne, Alexis, Ostrowski, Martin, Scanlan, David J., Mazard, Sophie, Palenik, Brian P., Paulsen, Ian T, Tandeau de Marsac, Nicole, Wincker, Patrick, Dossat, Carole, Ferriera, Steve, Johnson, Justin, Post, Anton F., Hess, Wolfgang R., Partensky, Frédéric, Garczarek, Laurence
Other Authors: Ecosystèmes, biodiversité, évolution Rennes (ECOBIO), Université de Rennes (UR)-Institut Ecologie et Environnement - CNRS Ecologie et Environnement (INEE-CNRS), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Observatoire des Sciences de l'Univers de Rennes (OSUR), Université de Rennes (UR)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Rennes 2 (UR2)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Rennes 2 (UR2)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Centre National de la Recherche Scientifique (CNRS), Department of Biological Sciences, Warwick, University of Warwick Coventry, Scripps Institution of Oceanography (SIO - UC San Diego), University of California San Diego (UC San Diego), University of California (UC)-University of California (UC), Department of Chemistry and Biomolecular Sciences, Macquarie University, Collection des Cyanobactéries, Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS), Génomique métabolique (UMR 8030), Genoscope - Centre national de séquençage Evry (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), J Craig Venter Institute, J. Craig Venter Institute, Interuniversity Institute for Marine Science, Hebrew University, Faculty of Biology, Freiburg, University of Freiburg Freiburg, Adaptation et diversité en milieu marin (AD2M), Station biologique de Roscoff Roscoff (SBR), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2008
Subjects:
SEA
Online Access:https://hal.science/hal-00338634
https://hal.science/hal-00338634/document
https://hal.science/hal-00338634/file/gb-2008-9-5-r90.pdf
https://doi.org/10.1186/gb-2008-9-5-r90
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Summary:International audience 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.