title: Cyanobacterial symbionts diverged in the late Cretaceous towards lineage-specific nitrogen fixation factories in single-celled phytoplankton.
abstract: The unicellular cyanobacterium UCYN-A, one of the major contributors to nitrogen fixation in the open ocean, lives in symbiosis with single-celled phytoplankton. UCYN-A includes several closely related lineages whose partner fidelity, genome-wide expression and time of evolutionary divergence remain to be resolved. Here we detect and distinguish UCYN-A1 and UCYN-A2 lineages in symbiosis with two distinct prymnesiophyte partners in the South Atlantic Ocean. Both symbiotic systems are lineage specific and differ in the number of UCYN-A cells involved. Our analyses infer a streamlined genome expression towards nitrogen fixation in both UCYN-A lineages. Comparative genomics reveal a strong purifying selection in UCYN-A1 and UCYN-A2 with a diversification process ∼91 Myr ago, in the late Cretaceous, after the low-nutrient regime period occurred during the Jurassic. These findings suggest that UCYN-A diversified in a co-evolutionary process, wherein their prymnesiophyte partners acted as a barrier driving an allopatric speciation of extant UCYN-A lineages.
authors.affiliation: Department of Marine Biology and Oceanography, Institut de Ciències del Mar (ICM), CSIC, Pg. Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain.
authors.forename: Francisco M
authors.initials: FM
authors.lastname: Cornejo-Castillo
authors.affiliation: Department of Marine Biology and Oceanography, Institut de Ciències del Mar (ICM), CSIC, Pg. Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain.
authors.forename: Ana M
authors.initials: AM
authors.lastname: Cabello
authors.affiliation: Department of Marine Biology and Oceanography, Institut de Ciències del Mar (ICM), CSIC, Pg. Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain.
authors.forename: Guillem
authors.identifier: http://orcid.org/0000-0002-9786-1493
authors.initials: G
authors.lastname: Salazar
authors.affiliation: School of Geographical Sciences, University of Bristol, Bristol BS8 1SS, UK.
authors.forename: Patricia
authors.initials: P
authors.lastname: Sánchez-Baracaldo
authors.affiliation: Department of Microbiology and Immunology, Rega Institute KU Leuven, Herestraat 49, 3000 Leuven, Belgium.|VIB Center for the Biology of Disease, VIB, Herestraat 49, 3000 Leuven, Belgium.|Department of Applied Biological Sciences (DBIT), Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium.
authors.forename: Gipsi
authors.initials: G
authors.lastname: Lima-Mendez
authors.affiliation: Aix Marseille Université CNRS IGS UMR 7256, 13288 Marseille, France.
authors.forename: Pascal
authors.initials: P
authors.lastname: Hingamp
authors.affiliation: CEA-Institut de Génomique, Genoscope, Centre National de Séquençage, 2 rue Gaston Crémieux, CP5706, F-91057 Evry, France.
authors.forename: Adriana
authors.initials: A
authors.lastname: Alberti
authors.affiliation: European Molecular Biology Laboratory, Structural and Computational Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany.
authors.forename: Shinichi
authors.identifier: http://orcid.org/0000-0003-3065-0314
authors.initials: S
authors.lastname: Sunagawa
authors.affiliation: European Molecular Biology Laboratory, Structural and Computational Biology Unit, Meyerhofstrasse 1, 69117 Heidelberg, Germany.|Max-Delbrück-Centre for Molecular Medicine, 13092 Berlin, Germany.
authors.forename: Peer
authors.initials: P
authors.lastname: Bork
authors.affiliation: CNRS, UMR 7144, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France.|Sorbonne Universités, UPMC Université Paris 06, UMR 7144, Station Biologique de Roscoff, Place Georges Teissier, 29680 Roscoff, France.
authors.forename: Colomban
authors.initials: C
authors.lastname: de Vargas
authors.affiliation: Department of Microbiology and Immunology, Rega Institute KU Leuven, Herestraat 49, 3000 Leuven, Belgium.|VIB Center for the Biology of Disease, VIB, Herestraat 49, 3000 Leuven, Belgium.|Department of Applied Biological Sciences (DBIT), Vrije Universiteit Brussel, Pleinlaan 2, 1050 Brussels, Belgium.
authors.forename: Jeroen
authors.initials: J
authors.lastname: Raes
authors.affiliation: Ecole Normale Supérieure, PSL Research University, Institut de Biologie de l'Ecole Normale Supérieure (IBENS), CNRS UMR 8197, INSERM U1024, 46 rue d'Ulm, F-75005 Paris, France.
authors.forename: Chris
authors.initials: C
authors.lastname: Bowler
authors.affiliation: CEA-Institut de Génomique, Genoscope, Centre National de Séquençage, 2 rue Gaston Crémieux, CP5706, F-91057 Evry, France.|Université d'Evry, UMR 8030, CP5706 Evry, France.|Centre National de la Recherche Scientifique (CNRS), UMR 8030, CP5706 Evry, France.
authors.forename: Patrick
authors.initials: P
authors.lastname: Wincker
authors.affiliation: Department of Ocean Sciences, University of California, Santa Cruz, California 95064, USA.
authors.forename: Jonathan P
authors.initials: JP
authors.lastname: Zehr
authors.affiliation: Department of Marine Biology and Oceanography, Institut de Ciències del Mar (ICM), CSIC, Pg. Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain.
authors.forename: Josep M
authors.initials: JM
authors.lastname: Gasol
authors.affiliation: Department of Marine Biology and Oceanography, Institut de Ciències del Mar (ICM), CSIC, Pg. Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain.
authors.forename: Ramon
authors.initials: R
authors.lastname: Massana
authors.affiliation: Department of Marine Biology and Oceanography, Institut de Ciències del Mar (ICM), CSIC, Pg. Marítim de la Barceloneta 37-49, 08003 Barcelona, Spain.
authors.forename: Silvia G
authors.initials: SG
authors.lastname: Acinas
mesh_terms: D001267:Atlantic Ocean; D005075:Biological Evolution; D000458:Cyanobacteria / Q000235:genetics*; D023281:Genomics; D058087:Haptophyta / Q000235:genetics*; D009586:Nitrogen Fixation; D010839:Phytoplankton / Q000235:genetics*; D012623:Seawater / Q000382:microbiology*; D013559:Symbiosis