Dicyemid Mesozoans: A Unique Parasitic Lifestyle and a Reduced Genome

Abstract

Dicyemids, previously called "mesozoans" (intermediates between unicellular protozoans and multicellular metazoans), are an enigmatic animal group. They have a highly simplified adult body, comprising only ∼30 cells, and they have a unique parasitic lifestyle. Recently, dicyemids were shown to be spiralians, with affinities to the Platyhelminthes. In order to understand molecular mechanisms involved in evolution of this odd animal, we sequenced the genome of Dicyema japonicum and a reference transcriptome assembly using mixed-stage samples. The D. japonicum genome features a high proportion of repetitive sequences that account for 49% of the genome. The dicyemid genome is reduced to ∼67.5 Mb with 5,012 protein-coding genes. Only four Hox genes exist in the genome, with no clustering. Gene distribution in KEGG pathways shows that D. japonicum has fewer genes in most pathways. Instead of eliminating entire critical metabolic pathways, parasitic lineages likely simplify pathways by eliminating pathway-specific genes, while genes with fundamental functions may be retained in multiple pathways. In principle, parasites can stand to lose genes that are unnecessary, in order to conserve energy. However, whether retained genes in incomplete pathways serve intermediate functions and how parasites overcome the physiological needs served by lost genes, remain to be investigated in future studies.

Keywords: dicyemids; genome; mesozoan; reduction; unique parasite.

Fig. 1.

—The mesozoan, Dicyema japonicum, with a unique life cycle. (A) Life cycle of dicyemids. See the text for details. AG, agamete; AN, axial cell nucleus; AX, axial cell; C, calotte; DI, developing infusoriform embryo; DV, developing vermiform embryo; E, epidermal cell; IN, infusorigen; MP, metapolar cell; PP, propolar cell; Adapted and modified from Furuya and Tsuneki 2003. (B) Dicyemida is a member of Spiralia.

Fig. 2.

—A pipeline for sequencing and de novo assembly of the Dicyema japonicum genome. Sequencing data generated by Illumina and PacBio sequencing platforms were first assembled separately. Then the two data sets were merged into a final assembly for downstream analyses. See Materials and Methods for details.

Fig. 3.

—Genomic and genic reduction in Dicyema japonicum. (A–D) Comparisons of genomic characteristics among nonparasitic and parasitic spiralians. (A) The genome size, (B) gene number, (C) intron size, and (D) percentage of repeats in the genome. Genomic information of compared taxa was obtained from published sources: brachiopods (Luo et al. 2015); limpets, polychaetes, and leeches (Simakov et al. 2013); blood flukes (Berriman et al. 2009); tapeworms (Berriman et al. 2009); and orthonectids (Mikhailov et al. 2016). (E) Venn diagram of dicyemid orthologous groups shared with other spiralians. Gene models of D. japonicum present 2,958 gene clusters, including 313 lineage-specific clusters. (F) Matrix of shared gene clusters among selected spiralians and ecdysozoans. Dicyemids share fewer gene clusters with orthonectids than with platyhelminths and lophotrochozoans. In general, parasitic spiralians share fewer gene clusters with nonparasitic spiralians.

Fig. 4.

—Dicyema japonicum contains four putative unclustered Hox genes. (A) A phylogenetic tree inferred from the homeobox domain using the maximum likelihood method, showing the presence of four Hox genes (blue bolds) in the D. japonicum genome. (B) Hox gene synteny in selected bilaterians. The scattered, unclustered Hox gene structure occurs in three parasitic spiralian lineages. The black block in Branchiostoma represents the rest of the posterior Hox genes. Double slashes signify noncontinuous linkage between two genes.

Fig. 5.

—Reduction of genes associated with biological pathways in parasites. (A) Numbers of conserved pathways in bilaterian species. (B) A heatmap showing the number of genes involved in conserved pathways to compare them among selected bilaterian species. Although parasitic lineages possess only 5% fewer conserved KEGG pathways than nonparasitic lineages (A), parasites in general have fewer genes in each of the KEGG pathways than nonparasitic species (B). Dicyema japonicum exhibits the fewest genes among all parasites.