The Genome of Intoshia linei Affirms Orthonectids as Highly Simplified Spiralians

Abstract

Orthonectids are rare parasites of marine invertebrates [1] that are commonly treated in textbooks as a taxon of uncertain affinity [2]. Trophic forms of orthonectids reside in the tissues of their hosts as multinucleated plasmodia, generating short-lived, worm-like ciliated female and male organisms that exit into the environment for copulation [3]. These ephemeral males and females are composed of just several hundred somatic cells and are deprived of digestive, circulatory, or excretory systems. Since their discovery in the 19(th) century, the orthonectids were described as organisms with no differentiated cell types and considered as part of Mesozoa, a putative link between multicellular animals and their unicellular relatives. More recently, this view was challenged as the new data suggested that orthonectids are animals that became simplified due to their parasitic way of life [3, 4]. Here, we report the genomic sequence of Intoshia linei, one of about 20 known species of orthonectids. The genomic data confirm recent morphological analysis asserting that orthonectids are members of Spiralia and possess muscular and nervous systems [5]. The 43-Mbp genome of I. linei encodes about 9,000 genes and retains those essential for the development and activity of muscular and nervous systems. The simplification of orthonectid body plan is associated with considerable reduction of metazoan developmental genes, leaving what might be viewed as the minimal gene set necessary to retain critical bilaterian features.

The structure of the muscular and nervous systems of the male Intoshialinei (Orthonectida)

“…(Filippova, Purschke, Tzetlin, & Müller, ). Taking together, this may support the annelid affinity of the Orthonectida, also supported by recent molecular phylogenetic analyses (Mikhailov et al, ; Schiffer et al, ).…”

“…It should be emphasized that the sexual individuals of orthonectids are free living and cannot be considered as neotenic larvae. It is also important to note the small size of I. linei genome, which amounts to only 9,000 genes (Mikhailov et al, ). As shown by the genome analysis, the orthonectid simplification is associated with reduction of developmental genes.…”

“…It has been widely accepted that orthonectids lack both, muscular and nervous systems, which was the main rationale for referring them to the most primitive animals together with Porifera and Placozoa (Brusca, Moore, & Shuster, 2016;Caullery, 1961;Ruppert, Fox, & Barnes, 2004;Stunkard, 1954). However, recent analysis of molecular data argues for considering Orthonectida as representatives of Lophotrochozoa (Mikhailov et al, 2016). More specifically, orthonectids appear to be most close to Annelida (Schiffer, Robertson, & Telford, 2018;Slyusarev & Kristensen, 2003;Slyusarev & Starunov, 2016).…”

The phylogenetic position of dicyemid mesozoans offers insights into spiralian evolution

“…Protein sequences of Tribolium castaneum , Drosophila melanogaster , Schistosoma mansoni , and Daphnia pulex were downloaded from the Uniprot database. Protein sequences contributed by the Intoshia linei genome project [17] were downloaded from NCBI BioProject: PRJNA316116. Gene models of Octopus bimaculatus were downloaded from the Octopus Genome website of the Molecular Genomics Unit at OIST [18, 19].…”

Genomics and the animal tree of life: conflicts and future prospects

“…A morphological 'progression rule' was therefore not required any longer, and further cases of simplification of body plans were suggested by molecular data analyses (e.g. Siddall et al 1995;Monteiro et al 2002;Mikhailov et al 2016).…”