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., Garczarek, Laurence, Mazard, Sophie, Palenik, Brian P., Paulsen, Ian, T., de Marsac, Nicole Tandeau, Wincker, Patrick, Dossat, Carole, Ferriera, Steve, Johnson, Justin, Post, Anton F., Hess, Wolfgang R., Partensky, Frédéric
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, 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), Collection des Cyanobactéries, Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS), Scripps Institution of Oceanography (SIO - UC San Diego), University of California San Diego (UC San Diego), University of California (UC)-University of California (UC), 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, Albert-Ludwigs-Universität Freiburg = University of Freiburg, ANR-05-BLAN-0122,PHYCOSYN,Evolution, Biosynthèse et Régulation des Phycobilisomes chez les Cyanobactéries Marines du Genre Synechococcus(2005)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2008
Subjects:
SEA
Online Access:https://hal.science/hal-00338634
https://hal.science/hal-00338634v1/document
https://hal.science/hal-00338634v1/file/gb-2008-9-5-r90.pdf
https://doi.org/10.1186/gb-2008-9-5-r90
id ftinraparis:oai:HAL:hal-00338634v1
record_format openpolar
institution Open Polar
collection Institut National de la Recherche Agronomique: ProdINRA
op_collection_id ftinraparis
language English
topic MAXIMUM-LIKELIHOOD
ATLANTIC-OCEAN
NORTH-ATLANTIC
NE ATLANTIC
DIVERSITY
SEA
PROCHLOROCOCCUS ECOTYPES
SYNECHOCOCCUS ECOTYPES
PHYLOGENETIC ANALYSIS
COMMUNITY STRUCTURE
MESH: Gene Transfer
Horizontal
MESH: Genome
Bacterial
MESH: Seawater
MESH: Synechococcus
[SDU.ENVI]Sciences of the Universe [physics]/Continental interfaces
environment
[SDE.MCG]Environmental Sciences/Global Changes
[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology
spellingShingle MAXIMUM-LIKELIHOOD
ATLANTIC-OCEAN
NORTH-ATLANTIC
NE ATLANTIC
DIVERSITY
SEA
PROCHLOROCOCCUS ECOTYPES
SYNECHOCOCCUS ECOTYPES
PHYLOGENETIC ANALYSIS
COMMUNITY STRUCTURE
MESH: Gene Transfer
Horizontal
MESH: Genome
Bacterial
MESH: Seawater
MESH: Synechococcus
[SDU.ENVI]Sciences of the Universe [physics]/Continental interfaces
environment
[SDE.MCG]Environmental Sciences/Global Changes
[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology
Dufresne, Alexis
Ostrowski, Martin
Scanlan, David, J.
Garczarek, Laurence
Mazard, Sophie
Palenik, Brian P.
Paulsen, Ian, T.
de Marsac, Nicole Tandeau
Wincker, Patrick
Dossat, Carole
Ferriera, Steve
Johnson, Justin
Post, Anton F.
Hess, Wolfgang R.
Partensky, Frédéric
Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria.
topic_facet MAXIMUM-LIKELIHOOD
ATLANTIC-OCEAN
NORTH-ATLANTIC
NE ATLANTIC
DIVERSITY
SEA
PROCHLOROCOCCUS ECOTYPES
SYNECHOCOCCUS ECOTYPES
PHYLOGENETIC ANALYSIS
COMMUNITY STRUCTURE
MESH: Gene Transfer
Horizontal
MESH: Genome
Bacterial
MESH: Seawater
MESH: Synechococcus
[SDU.ENVI]Sciences of the Universe [physics]/Continental interfaces
environment
[SDE.MCG]Environmental Sciences/Global Changes
[SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology
description 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.
author2 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
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)
Collection des Cyanobactéries
Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS)
Scripps Institution of Oceanography (SIO - UC San Diego)
University of California San Diego (UC San Diego)
University of California (UC)-University of California (UC)
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
Albert-Ludwigs-Universität Freiburg = University of Freiburg
ANR-05-BLAN-0122,PHYCOSYN,Evolution, Biosynthèse et Régulation des Phycobilisomes chez les Cyanobactéries Marines du Genre Synechococcus(2005)
format Article in Journal/Newspaper
author Dufresne, Alexis
Ostrowski, Martin
Scanlan, David, J.
Garczarek, Laurence
Mazard, Sophie
Palenik, Brian P.
Paulsen, Ian, T.
de Marsac, Nicole Tandeau
Wincker, Patrick
Dossat, Carole
Ferriera, Steve
Johnson, Justin
Post, Anton F.
Hess, Wolfgang R.
Partensky, Frédéric
author_facet Dufresne, Alexis
Ostrowski, Martin
Scanlan, David, J.
Garczarek, Laurence
Mazard, Sophie
Palenik, Brian P.
Paulsen, Ian, T.
de Marsac, Nicole Tandeau
Wincker, Patrick
Dossat, Carole
Ferriera, Steve
Johnson, Justin
Post, Anton F.
Hess, Wolfgang R.
Partensky, Frédéric
author_sort Dufresne, Alexis
title Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria.
title_short Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria.
title_full Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria.
title_fullStr Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria.
title_full_unstemmed Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria.
title_sort unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria.
publisher HAL CCSD
publishDate 2008
url https://hal.science/hal-00338634
https://hal.science/hal-00338634v1/document
https://hal.science/hal-00338634v1/file/gb-2008-9-5-r90.pdf
https://doi.org/10.1186/gb-2008-9-5-r90
genre North Atlantic
genre_facet North Atlantic
op_source ISSN: 1465-6906
EISSN: 1474-760X
Genome Biology
https://hal.science/hal-00338634
Genome Biology, 2008, 9 (5), pp.R90. ⟨10.1186/gb-2008-9-5-r90⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1186/gb-2008-9-5-r90
info:eu-repo/semantics/altIdentifier/pmid/18507822
PUBMED: 18507822
op_rights info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1186/gb-2008-9-5-r90
container_title Genome Biology
container_volume 9
container_issue 5
container_start_page R90
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spelling ftinraparis:oai:HAL:hal-00338634v1 2024-10-13T14:09:33+00:00 Unraveling the genomic mosaic of a ubiquitous genus of marine cyanobacteria. Dufresne, Alexis Ostrowski, Martin Scanlan, David, J. Garczarek, Laurence Mazard, Sophie Palenik, Brian P. Paulsen, Ian, T. de Marsac, Nicole Tandeau Wincker, Patrick Dossat, Carole Ferriera, Steve Johnson, Justin Post, Anton F. Hess, Wolfgang R. Partensky, Frédéric 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 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) Collection des Cyanobactéries Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS) Scripps Institution of Oceanography (SIO - UC San Diego) University of California San Diego (UC San Diego) University of California (UC)-University of California (UC) 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 Albert-Ludwigs-Universität Freiburg = University of Freiburg ANR-05-BLAN-0122,PHYCOSYN,Evolution, Biosynthèse et Régulation des Phycobilisomes chez les Cyanobactéries Marines du Genre Synechococcus(2005) 2008 https://hal.science/hal-00338634 https://hal.science/hal-00338634v1/document https://hal.science/hal-00338634v1/file/gb-2008-9-5-r90.pdf https://doi.org/10.1186/gb-2008-9-5-r90 en eng HAL CCSD BioMed Central info:eu-repo/semantics/altIdentifier/doi/10.1186/gb-2008-9-5-r90 info:eu-repo/semantics/altIdentifier/pmid/18507822 PUBMED: 18507822 info:eu-repo/semantics/OpenAccess ISSN: 1465-6906 EISSN: 1474-760X Genome Biology https://hal.science/hal-00338634 Genome Biology, 2008, 9 (5), pp.R90. ⟨10.1186/gb-2008-9-5-r90⟩ MAXIMUM-LIKELIHOOD ATLANTIC-OCEAN NORTH-ATLANTIC NE ATLANTIC DIVERSITY SEA PROCHLOROCOCCUS ECOTYPES SYNECHOCOCCUS ECOTYPES PHYLOGENETIC ANALYSIS COMMUNITY STRUCTURE MESH: Gene Transfer Horizontal MESH: Genome Bacterial MESH: Seawater MESH: Synechococcus [SDU.ENVI]Sciences of the Universe [physics]/Continental interfaces environment [SDE.MCG]Environmental Sciences/Global Changes [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology info:eu-repo/semantics/article Journal articles 2008 ftinraparis https://doi.org/10.1186/gb-2008-9-5-r90 2024-09-24T14:49:09Z 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. Article in Journal/Newspaper North Atlantic Institut National de la Recherche Agronomique: ProdINRA Genome Biology 9 5 R90