title: The symbiotic life of Symbiodinium in the open ocean within a new species of calcifying ciliate (Tiarina sp.).
abstract: Symbiotic partnerships between heterotrophic hosts and intracellular microalgae are common in tropical and subtropical oligotrophic waters of benthic and pelagic marine habitats. The iconic example is the photosynthetic dinoflagellate genus Symbiodinium that establishes mutualistic symbioses with a wide diversity of benthic hosts, sustaining highly biodiverse reef ecosystems worldwide. Paradoxically, although various species of photosynthetic dinoflagellates are prevalent eukaryotic symbionts in pelagic waters, Symbiodinium has not yet been reported in symbiosis within oceanic plankton, despite its high propensity for the symbiotic lifestyle. Here we report a new pelagic photosymbiosis between a calcifying ciliate host and the microalga Symbiodinium in surface ocean waters. Confocal and scanning electron microscopy, together with an 18S rDNA-based phylogeny, showed that the host is a new ciliate species closely related to Tiarina fusus (Colepidae). Phylogenetic analyses of the endosymbionts based on the 28S rDNA gene revealed multiple novel closely related Symbiodinium clade A genotypes. A haplotype network using the high-resolution internal transcribed spacer-2 marker showed that these genotypes form eight divergent, biogeographically structured, subclade types that do not seem to associate with any benthic hosts. Ecological analyses using the Tara Oceans metabarcoding data set (V9 region of the 18S rDNA) and contextual oceanographic parameters showed a global distribution of the symbiotic partnership in nutrient-poor surface waters. The discovery of the symbiotic life of Symbiodinium in the open ocean provides new insights into the ecology and evolution of this pivotal microalga and raises new hypotheses about coastal pelagic connectivity.
authors.affiliation: EPEP-Evolution des Protistes et des Ecosystèmes Pélagiques-team, Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Roscoff, France.|CNRS, UMR 7144, Station Biologique de Roscoff, Roscoff, France.
authors.forename: Solenn
authors.initials: S
authors.lastname: Mordret
authors.affiliation: EPEP-Evolution des Protistes et des Ecosystèmes Pélagiques-team, Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Roscoff, France.|CNRS, UMR 7144, Station Biologique de Roscoff, Roscoff, France.
authors.forename: Sarah
authors.initials: S
authors.lastname: Romac
authors.affiliation: EPEP-Evolution des Protistes et des Ecosystèmes Pélagiques-team, Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Roscoff, France.|CNRS, UMR 7144, Station Biologique de Roscoff, Roscoff, France.
authors.forename: Nicolas
authors.initials: N
authors.lastname: Henry
authors.affiliation: EPEP-Evolution des Protistes et des Ecosystèmes Pélagiques-team, Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Roscoff, France.|CNRS, UMR 7144, Station Biologique de Roscoff, Roscoff, France.
authors.forename: Sébastien
authors.initials: S
authors.lastname: Colin
authors.affiliation: EPEP-Evolution des Protistes et des Ecosystèmes Pélagiques-team, Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Roscoff, France.|CNRS, UMR 7144, Station Biologique de Roscoff, Roscoff, France.
authors.forename: Margaux
authors.initials: M
authors.lastname: Carmichael
authors.affiliation: EPEP-Evolution des Protistes et des Ecosystèmes Pélagiques-team, Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Roscoff, France.|CNRS, UMR 7144, Station Biologique de Roscoff, Roscoff, France.
authors.forename: Cédric
authors.initials: C
authors.lastname: Berney
authors.affiliation: EPEP-Evolution des Protistes et des Ecosystèmes Pélagiques-team, Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Roscoff, France.|CNRS, UMR 7144, Station Biologique de Roscoff, Roscoff, France.
authors.forename: Stéphane
authors.initials: S
authors.lastname: Audic
authors.affiliation: EPEP-Evolution des Protistes et des Ecosystèmes Pélagiques-team, Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Roscoff, France.|CNRS, UMR 7144, Station Biologique de Roscoff, Roscoff, France.
authors.forename: Daniel J
authors.initials: DJ
authors.lastname: Richter
authors.affiliation: Coastal and Freshwater Group, Cawthron Institute, Nelson, New Zealand.|Institute of Marine Science, University of Auckland, Auckland, New Zealand.
authors.forename: Xavier
authors.initials: X
authors.lastname: Pochon
authors.affiliation: EPEP-Evolution des Protistes et des Ecosystèmes Pélagiques-team, Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Roscoff, France.|CNRS, UMR 7144, Station Biologique de Roscoff, Roscoff, France.
authors.forename: Colomban
authors.initials: C
authors.lastname: de Vargas
authors.affiliation: EPEP-Evolution des Protistes et des Ecosystèmes Pélagiques-team, Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, Roscoff, France.|CNRS, UMR 7144, Station Biologique de Roscoff, Roscoff, France.
authors.forename: Johan
authors.initials: J
authors.lastname: Decelle
mesh_terms: D000818:Animals; D044822:Biodiversity; D005075:Biological Evolution; D016798:Ciliophora / Q000235:genetics* / Q000502:physiology; D058893:DNA Barcoding, Taxonomic; D004275:DNA, Ribosomal / Q000737:chemistry / Q000235:genetics; D004141:Dinoflagellida / Q000235:genetics* / Q000502:physiology; D004463:Ecology; D017753:Ecosystem; D005838:Genotype; D005843:Geography; D006239:Haplotypes; D056186:Metagenomics; D009792:Oceans and Seas; D010802:Phylogeny; D013559:Symbiosis
chemical_list: D004275:DNA, Ribosomal