Distinction of Cell Types in Dicyema japonicum (Phylum Dicyemida) by Expression Patterns of 16 Genes

Ogino, Kazutoyo; Tsuneki, Kazuhiko; Furuya, Hidetaka

doi:10.1645/ge-2472.1

“…In situ hybridisations for 16 diverse genes in different life stages of Dicyema sp. suggested the presence of multiple different cell types, providing further support for the idea of a complex ancestor of mesozoan members, followed by extreme simplification of body organisation (Ogino et al, 2011).…”

Section: Introductionmentioning

confidence: 73%

The mitochondrial genomes of the mesozoansIntoshia linei,Dicyemasp. andDicyema japonicum

Robertson

¹

,

Schiffer

²

,

Telford

³

2018

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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 unique gene order. The data we have analysed 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 of 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.

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“…A mixed life-stage sample of Dicyema japonicum was collected from urine in renal sacs of the host, Octopus vulgaris , and washed several times with artificial seawater [13]. The sample was homogenized in TRIzol Reagent (Ambion, #15596026), and RNA was extracted using the phenol-chloroform method, after which it was further purified with a QIAGEN RNeasy Micro Kit (QIAGEN, #74004).…”

Section: Methodsmentioning

confidence: 99%

The phylogenetic position of dicyemid mesozoans offers insights into spiralian evolution

Lu

¹

,

Kanda

²

,

Satoh

³

et al. 2017

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BackgroundObtaining phylogenomic data for enigmatic taxa is essential to achieve a better understanding of animal evolution. Dicyemids have long fascinated biologists because of their highly simplified body organization, but their life-cycles remain poorly known. Based on the discovery of the dicyemid DoxC gene, which encodes a spiralian peptide, it has been proposed that dicyemids are members of the Spiralia. Other studies have suggested that dicyemids may have closer affinities to mollusks and annelids. However, the phylogenetic position of dicyemids has remained a matter of debate, leading to an ambiguous picture of spiralian evolution.ResultsIn the present study, newly sequenced transcriptomic data from Dicyema japonicum were complemented with published transcriptomic data or predicted gene models from 29 spiralian, ecdysozoan, and deuterostome species, generating a dataset (Dataset 1) for phylogenomic analyses, which contains 348 orthologs and 58,124 amino acids. In addition to this dataset, to eliminate systematic errors, two additional sub-datasets were created by removing compositionally heterogeneous or rapidly evolving sites and orthologs from Dataset 1, which may cause compositional heterogeneity and long-branch attraction artifacts. Maximum likelihood and Bayesian inference analyses both placed Dicyema japonicum (Dicyemida) in a clade with Intoshia linei (Orthonectida) with strong statistical support. Furthermore, maximum likelihood analyses placed the Dicyemida + Orthonectida clade within the Gastrotricha, while in Bayesian inference analyses, this clade is sister group to the clade of Gastrotricha + Platyhelminthes.ConclusionsWhichever the case, in all analyses, Dicyemida, Orthonectida, Gastrotricha, and Platyhelminthes constitute a monophyletic group that is a sister group to the clade of Mollusca + Annelida. Based on present phylogenomic analyses, dicyemids display close affinity to orthonectids, and they may share a common ancestor with gastrotrichs and platyhelminths, rather than with mollusks and annelids. Regarding spiralian phylogeny, the Gnathifera forms the sister group to the Rouphozoa and Lophotrochozoa, as has been suggested by previous studies; thus our analysis supports the traditional acoeloid–planuloid hypothesis of a nearly microscopic, non-coelomate common ancestor of spiralians.

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“…In situ hybridisations for 16 diverse genes in different life stages of Dicyema sp. suggested the presence of multiple different cell types, and provided further support for the idea of a complex ancestor of mesozoan members, followed by extreme simplification of body organisation (Ogino et al, 2011). Two significant contributions for understanding the evolutionary history of the Mesozoa are the recent publication of the nuclear genome of Intoshia linei, which represents one of approximately 20 species of this genus, and a transcriptome of Dicyema japonicum (Lu et al, 2017;Mikhailov et al, 2016).…”

Section: Introductionmentioning

confidence: 81%

The mitochondrial genomes of the mesozoansIntoshia linei, Dicyemasp., andDicyema japonicum

Robertson

¹

,

Schiffer

²

,

Telford

³

2018

Preprint

0

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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. Mitochondrial genomes; mitochondrial mini-circles; MesozoaAll rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint . http://dx.doi.org/10.1101/282285 doi: bioRxiv preprint first posted online Mar. 14, 2018; Key Findings• We 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.• We 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.• We find that the cox1 gene from dicyemids has a series of four conserved in-frame deletions which appear to be unique to this group.

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Distinction of Cell Types in Dicyema japonicum (Phylum Dicyemida) by Expression Patterns of 16 Genes

Cited by 9 publications

References 26 publications

The mitochondrial genomes of the mesozoansIntoshia linei,Dicyemasp. andDicyema japonicum

The mitochondrial genomes of the mesozoansIntoshia linei,Dicyemasp. andDicyema japonicum

The phylogenetic position of dicyemid mesozoans offers insights into spiralian evolution

The mitochondrial genomes of the mesozoansIntoshia linei, Dicyemasp., andDicyema japonicum

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