Schiffer, P. | bioRxiv Science

bioRxiv2018

The mitochondrial genomes of the mesozoans Intoshia linei, Dicyema sp., and Dicyema japonicum

The Dicyemida and Orthonectida are two groups of tiny, simple, vermiform parasites that have historically been united in a group named the Mesozoa. Both Dicyemida and Orthonectida have just two cell layers and appear to lack any defined tissues. They were initially thought to be evolutionary intermediates between protozoans and metazoans but more recent analyses indicate that they are protostomian metazoans that have undergone secondary simplification from a complex ancestor. Here we describe the first almost complete mitochondrial genome sequence from an orthonectid, Intoshia linei, and describe nine and eight mitochondrial protein-coding genes from Dicyema sp. and Dicyema japonicum, respectively. The 14,247 base pair long I. linei sequence has typical metazoan gene content, but is exceptionally AT-rich, and has a divergent gene order compared to other metazoans. The data we present from the Dicyemida provide very limited support for the suggestion that dicyemid mitochondrial genes are found on discrete mini-circles, as opposed to the large circular mitochondrial genomes that are typical across the Metazoa. The cox1 gene from dicyemid species has a series of conserved in-frame deletions that is unique to this lineage. Using cox1 genes from across the genus Dicyema, we report the first internal phylogeny of this group.\n\nKey FindingsO_LIWe report the first almost-complete mitochondrial genome from an orthonectid parasite, Intoshia linei, including 12 protein-coding genes; 20 tRNAs and putative sequences for large and small subunit rRNAs. We find that the I. linei mitochondrial genome is exceptionally AT-rich and has a novel gene order compared to other published metazoan mitochondrial genomes. These findings are indicative of the rapid rate of evolution that has occurred in the I. linei mitochondrial genome.\nC_LIO_LIWe also report nine and eight protein-coding genes, respectively, from the dicyemid species Dicyema sp. and Dicyema japonicum, and use the cox1 genes from both species for phylogenetic inference of the internal phylogeny of the dicyemids.\nC_LIO_LIWe find that the cox1 gene from dicyemids has a series of four conserved in-frame deletions which appear to be unique to this group.\nC_LI

evolutionary biology↗

bioRxiv2017

Molecular data from Orthonectid worms show they are highly degenerate members of phylum Annelida not phylum Mesozoa.

SummaryThe Mesozoa are a group of tiny, extremely simple, vermiform endoparasites of various marine animals (Fig. 1). There are two recognised groups within the Mesozoa: the Orthonectida (Fig. 1a,b; with a few hundred cells including a nervous system made up of just 10 cells [1]) and the Dicyemids (Fig. 1c; with at most 42 cells [2]). They are classic Problematica [3] - the name Mesozoa suggests an evolutionary position intermediate between Protozoa and Metazoa (animals) [4] and implies their simplicity is a primitive state, but molecular data have shown they are members of Lophotrochozoa within Bilateria [5-8] which would mean they derive from a more complex ancestor. Their precise phylogenetic affinities remain uncertain, however, and ascertaining this is complicated by the very fast evolution observed in genes from both groups, leading to the common systematic error of Long Branch Attraction (LBA) [9]. Here we use mitochondrial and nuclear gene sequence data, and show beyond doubt that both dicyemids and orthonectids are members of the Lophotrochozoa. Carefully addressing the effects of systematic errors due to unequal rates of evolution, we show that the phylum Mesozoa is polyphyletic. While the precise position of dicyemids remains unresolved within Lophotrochozoa, we unequivocally identify orthonectids as members of the phylum Annelida. This result reveals one of the most extreme cases of body plan simplification in the animal kingdom; our finding makes sense of an annelid-like cuticle in orthonectids [1] and suggests the circular muscle cells repeated along their body [10] may be segmental in origin.\n\nO_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=71 SRC=\"FIGDIR/small/235549_fig1.gif\" ALT=\"Figure 1\">\nView larger version (22K):\norg.highwire.dtl.DTLVardef@76ca5org.highwire.dtl.DTLVardef@16df6eaorg.highwire.dtl.DTLVardef@6da877org.highwire.dtl.DTLVardef@14f3056_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOFig. 1:C_FLOATNO The mesozoans Intoshia variabili and Dicyema typus A. Differential Interference contrast micrograph of an Intoshia variabili female showing repeated bands of ciliated cells. Picture G. Slyusarev (St Petersburg State University, Russia).\n\nB. Confocal image of a phalloidin stained female specimen of Intoshia linei reveals repeated set of circular muscles. Picture G. Slyusarev (St Petersburg State Univ.).\n\nC. Rhombogen stage of a dicyemid (Dicyema typus from the Octopus) adapted from Hyman L.H. The Invertebrates: Protozoa through Ctenophora McGraw-Hill, New York 1940(19). Anterior to right in all images.\n\nC_FIG

evolutionary biology↗