BACKGROUND: Ascetosporea (Endomyxa, Rhizaria) is a group of unicellular parasites infecting aquatic invertebrates. They are increasingly being recognized as widespread and important in marine environments, causing large annual losses in invertebrate aquaculture. Despite their importance, little molecular data of Ascetosporea exist, with only two genome assemblies published to date. Accordingly, the evolutionary origin of these parasites is unclear, including their phylogenetic position and the genomic adaptations that accompanied the transition from a free-living lifestyle to parasitism. Here, we sequenced and assembled three new ascetosporean genomes, as well as the genome of a closely related amphizoic species, to investigate the phylogeny, origin, and genomic adaptations to parasitism in Ascetosporea. RESULTS: Using a phylogenomic approach, we confirm the monophyly of Ascetosporea and show that Paramyxida group with Mikrocytida, with Haplosporida being sister to both groups. We report that the genomes of these parasites are relatively small (12-36 Mb) and gene-sparse (~ 2300-5200 genes), while containing surprisingly high amounts of non-coding sequence (~ 70-90% of the genomes). Performing gene-tree aware ancestral reconstruction of gene families, we demonstrate extensive gene losses at the origin of parasitism in Ascetosporea, primarily of metabolic functions, and little gene gain except on terminal branches. Finally, we highlight some functional gene classes that have undergone expansions during evolution of the group. CONCLUSIONS: We present important new genomic information from a lineage of enigmatic but important parasites of invertebrates and illuminate some of the genomic innovations accompanying the evolutionary transition to parasitism in this lineage. Our results and data provide a genetic basis for the development of control measures against these parasites.

Centre for Environment Fisheries and Aquaculture Science Weymouth Laboratory Weymouth Dorset DT4 8UB UK

Department of Organismal Biology Uppsala University Norbyv 18D Uppsala SE 752 36 Sweden

Division of Fish Health University of Veterinary Medicine Veterinärplatz 1 Vienna 1210 Austria

Institute of Parasitology Biology Centre of the Czech Academy of Sciences Branišovská 31 České Budějovice 370 05 Czech Republic

Marine Institute Rinville Oranmore H91R673 Ireland

Natural History Museum Science London SW7 5BD UK

Present Address Department of Ecology and Genetics Uppsala University Norbyv 18D Uppsala SE 752 36 Sweden

Present Address Department of Ecology Environment and Plant Sciences Stockholm University Svante Arrhenius 5 20 A Stockholm SE 114 18 Sweden

Present Address Natural History Museum Oslo University Oslo 0562 Norway

Present Address The Royal Swedish Academy of Sciences Stockholm SE 114 18 Sweden

Science for Life Laboratory Uppsala University Uppsala Sweden

Sustainable Aquaculture Futures Biosciences University of Exeter Stocker Road Exeter EX4 4QD UK

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Comparative genomics of Ascetosporea gives new insight into the evolutionary basis for animal parasitism in Rhizaria