title: An Early-Branching Freshwater Cyanobacterium at the Origin of Plastids.
abstract: Photosynthesis evolved in eukaryotes by the endosymbiosis of a cyanobacterium, the future plastid, within a heterotrophic host. This primary endosymbiosis occurred in the ancestor of Archaeplastida, a eukaryotic supergroup that includes glaucophytes, red algae, green algae, and land plants [1-4]. However, although the endosymbiotic origin of plastids from a single cyanobacterial ancestor is firmly established, the nature of that ancestor remains controversial: plastids have been proposed to derive from either early- or late-branching cyanobacterial lineages [5-11]. To solve this issue, we carried out phylogenomic and supernetwork analyses of the most comprehensive dataset analyzed so far including plastid-encoded proteins and nucleus-encoded proteins of plastid origin resulting from endosymbiotic gene transfer (EGT) of primary photosynthetic eukaryotes, as well as wide-ranging genome data from cyanobacteria, including novel lineages. Our analyses strongly support that plastids evolved from deep-branching cyanobacteria and that the present-day closest cultured relative of primary plastids is Gloeomargarita lithophora. This species belongs to a recently discovered cyanobacterial lineage widespread in freshwater microbialites and microbial mats [12, 13]. The ecological distribution of this lineage sheds new light on the environmental conditions where the emergence of photosynthetic eukaryotes occurred, most likely in a terrestrial-freshwater setting. The fact that glaucophytes, the first archaeplastid lineage to diverge, are exclusively found in freshwater ecosystems reinforces this hypothesis. Therefore, not only did plastids emerge early within cyanobacteria, but the first photosynthetic eukaryotes most likely evolved in terrestrial-freshwater settings, not in oceans as commonly thought.
authors.affiliation: Unité d'Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud/Paris-Saclay, AgroParisTech, 91400 Orsay, France.
authors.forename: Rafael I
authors.initials: RI
authors.lastname: Ponce-Toledo
authors.affiliation: Unité d'Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud/Paris-Saclay, AgroParisTech, 91400 Orsay, France.
authors.forename: Philippe
authors.initials: P
authors.lastname: Deschamps
authors.affiliation: Unité d'Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud/Paris-Saclay, AgroParisTech, 91400 Orsay, France.
authors.forename: Purificación
authors.initials: P
authors.lastname: López-García
authors.affiliation: Institut de Génétique et Microbiologie, CNRS UMR 8621, Université Paris-Sud/Paris-Saclay, 91405 Orsay, France.
authors.forename: Yvan
authors.initials: Y
authors.lastname: Zivanovic
authors.affiliation: Institut de Minéralogie, de Physique des Matériaux, et de Cosmochimie, Sorbonne Universités, UPMC Université Paris 06, CNRS UMR 7590, Muséum National d'Histoire Naturelle, IRD UMR 206, 75005 Paris, France.
authors.forename: Karim
authors.initials: K
authors.lastname: Benzerara
authors.affiliation: Unité d'Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud/Paris-Saclay, AgroParisTech, 91400 Orsay, France. Electronic address: david.moreira@u-psud.fr.
authors.forename: David
authors.initials: D
authors.lastname: Moreira
mesh_terms: D005075:Biological Evolution; D000458:Cyanobacteria / Q000145:classification* / Q000235:genetics / Q000302:isolation & purification; D056890:Eukaryota / Q000166:cytology*; D005618:Fresh Water / Q000382:microbiology*; D053263:Gene Regulatory Networks; D010788:Photosynthesis; D010802:Phylogeny; D018087:Plastids / Q000235:genetics* / Q000502:physiology; D013559:Symbiosis
keywords: chloroplasts; cyanobacteria; evolution; molecular phylogeny; phylogenomics; plastids