title: Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics.
abstract: Dinoflagellates are key species in marine environments, but they remain poorly understood in part because of their large, complex genomes, unique molecular biology, and unresolved in-group relationships. We created a taxonomically representative dataset of dinoflagellate transcriptomes and used this to infer a strongly supported phylogeny to map major morphological and molecular transitions in dinoflagellate evolution. Our results show an early-branching position of Noctiluca, monophyly of thecate (plate-bearing) dinoflagellates, and paraphyly of athecate ones. This represents unambiguous phylogenetic evidence for a single origin of the group's cellulosic theca, which we show coincided with a radiation of cellulases implicated in cell division. By integrating dinoflagellate molecular, fossil, and biogeochemical evidence, we propose a revised model for the evolution of thecal tabulations and suggest that the late acquisition of dinosterol in the group is inconsistent with dinoflagellates being the source of this biomarker in pre-Mesozoic strata. Three distantly related, fundamentally nonphotosynthetic dinoflagellates, Noctiluca, Oxyrrhis, and Dinophysis, contain cryptic plastidial metabolisms and lack alternative cytosolic pathways, suggesting that all free-living dinoflagellates are metabolically dependent on plastids. This finding led us to propose general mechanisms of dependency on plastid organelles in eukaryotes that have lost photosynthesis; it also suggests that the evolutionary origin of bioluminescence in nonphotosynthetic dinoflagellates may be linked to plastidic tetrapyrrole biosynthesis. Finally, we use our phylogenetic framework to show that dinoflagellate nuclei have recruited DNA-binding proteins in three distinct evolutionary waves, which included two independent acquisitions of bacterial histone-like proteins.
authors.affiliation: Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom; janjan.cz@gmail.com.|Biology Department, San Diego State University, San Diego, CA 92182.|Botany Department, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.|Program in Integrated Microbial Diversity, Canadian Institute for Advanced Research, Toronto, ON M5G 1Z8, Canada.
authors.forename: Jan
authors.identifier: 0000-0001-6547-749X
authors.initials: J
authors.lastname: Janouškovec
authors.affiliation: Zoology Department, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
authors.forename: Gregory S
authors.initials: GS
authors.lastname: Gavelis
authors.affiliation: Botany Department, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
authors.forename: Fabien
authors.initials: F
authors.lastname: Burki
authors.affiliation: Botany Department, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
authors.forename: Donna
authors.initials: D
authors.lastname: Dinh
authors.affiliation: Institute for Marine and Environmental Technology, University of Maryland Center for Environmental Sciences, Baltimore, MD 21202.
authors.forename: Tsvetan R
authors.initials: TR
authors.lastname: Bachvaroff
authors.affiliation: Centre for Chromosome Biology, School of Natural Sciences, National University of Ireland, Galway, Ireland.
authors.forename: Sebastian G
authors.initials: SG
authors.lastname: Gornik
authors.affiliation: Shannon Point Marine Center, Western Washington University, Anacortes, WA 98221.
authors.forename: Kelley J
authors.initials: KJ
authors.lastname: Bright
authors.affiliation: Botany Department, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
authors.forename: Behzad
authors.initials: B
authors.lastname: Imanian
authors.affiliation: Shannon Point Marine Center, Western Washington University, Anacortes, WA 98221.
authors.forename: Suzanne L
authors.initials: SL
authors.lastname: Strom
authors.affiliation: Department of Cell Biology and Molecular Genetics and Agricultural Experiment Station, University of Maryland, College Park, MD 20742.
authors.forename: Charles F
authors.identifier: 0000-0001-7854-8584
authors.initials: CF
authors.lastname: Delwiche
authors.affiliation: Department of Biochemistry, University of Cambridge, Cambridge CB2 1QW, United Kingdom.
authors.forename: Ross F
authors.initials: RF
authors.lastname: Waller
authors.affiliation: Bedford Institute of Oceanography, Geological Survey of Canada (Atlantic), Dartmouth, NS B2Y 4A2, Canada.
authors.forename: Robert A
authors.initials: RA
authors.lastname: Fensome
authors.affiliation: Botany Department, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.|Program in Integrated Microbial Diversity, Canadian Institute for Advanced Research, Toronto, ON M5G 1Z8, Canada.|Zoology Department, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
authors.forename: Brian S
authors.initials: BS
authors.lastname: Leander
authors.affiliation: Biology Department, San Diego State University, San Diego, CA 92182.|Program in Integrated Microbial Diversity, Canadian Institute for Advanced Research, Toronto, ON M5G 1Z8, Canada.
authors.forename: Forest L
authors.initials: FL
authors.lastname: Rohwer
authors.affiliation: Botany Department, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
authors.forename: Juan F
authors.initials: JF
authors.lastname: Saldarriaga
mesh_terms: D004141:Dinoflagellida / Q000235:genetics*; D019143:Evolution, Molecular; D010802:Phylogeny; D018087:Plastids; D016053:RNA, Protozoan / Q000235:genetics; D017423:Sequence Analysis, RNA; D059467:Transcriptome
chemical_list: D016053:RNA, Protozoan
keywords: dinoflagellates; dinosterol; phylogeny; plastids; theca