BACKGROUND: Diplonemid flagellates are among the most abundant and species-rich of known marine microeukaryotes, colonizing all habitats, depths, and geographic regions of the world ocean. However, little is known about their genomes, biology, and ecological role. RESULTS: We present the first nuclear genome sequence from a diplonemid, the type species Diplonema papillatum. The ~ 280-Mb genome assembly contains about 32,000 protein-coding genes, likely co-transcribed in groups of up to 100. Gene clusters are separated by long repetitive regions that include numerous transposable elements, which also reside within introns. Analysis of gene-family evolution reveals that the last common diplonemid ancestor underwent considerable metabolic expansion. D. papillatum-specific gains of carbohydrate-degradation capability were apparently acquired via horizontal gene transfer. The predicted breakdown of polysaccharides including pectin and xylan is at odds with reports of peptides being the predominant carbon source of this organism. Secretome analysis together with feeding experiments suggest that D. papillatum is predatory, able to degrade cell walls of live microeukaryotes, macroalgae, and water plants, not only for protoplast feeding but also for metabolizing cell-wall carbohydrates as an energy source. The analysis of environmental barcode samples shows that D. papillatum is confined to temperate coastal waters, presumably acting in bioremediation of eutrophication. CONCLUSIONS: Nuclear genome information will allow systematic functional and cell-biology studies in D. papillatum. It will also serve as a reference for the highly diverse diplonemids and provide a point of comparison for studying gene complement evolution in the sister group of Kinetoplastida, including human-pathogenic taxa.

Architecture et Fonction des Macromolécules Biologiques CNRS Aix Marseille Université Marseille France

Department of Biochemistry and Molecular Biology Institute for Comparative Genomics Dalhousie University Halifax NS Canada

Department of Biochemistry Robert Cedergren Centre for Bioinformatics and Genomics Université de Montréal Montreal QC Canada

Department of Biological Sciences King Abdulaziz University Jeddah Saudi Arabia

Faculty of Science University of Ostrava Ostrava Czech Republic

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic

Laboratory of Molecular Parasitology Graduate School of Life Science and Technology Iryo Sosei University Iwaki City Fukushima Japan

Present address Canadian Centre for Computational Genomics; McGill Genome Centre McGill University Montreal QC Canada

Present address DTU Bioengineering Technical University of Denmark Lyngby Denmark

Present address Environment Climate Change Canada Dorval QC Canada

Present address High Performance Computing Centre Bristol UK

RIKEN Interdisciplinary Theoretical and Mathematical Sciences Program Hirosawa Wako Saitama Japan

School of Biological Sciences University of Bristol Bristol UK

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Ultrastructure and 3D reconstruction of a diplonemid protist (Diplonemea) and its novel membranous organelle

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