Abstract
Gastrotrichs—’hairy bellies’—are microscopic free-living animals inhabiting marine and freshwater habitats. Based on morphological and early molecular analyses, gastrotrichs were placed close to nematodes, but recent phylogenomic analyses have suggested their close relationship to flatworms (Platyhelminthes) within Spiralia. Small non-coding RNA data on e.g., microRNAs (miRNAs) and PIWI-interacting RNAs (piRNA) may help to resolve this long-standing question. MiRNAs are short post-transcriptional gene regulators that together with piRNAs play key roles in development. In a ‘multi-omics’ approach we here used small-RNA sequencing, available transcriptome and genomic data to unravel the miRNA- and piRNA complements along with the RNAi (RNA interference) protein machinery of Lepidodermella squamata (Gastrotricha, Chaetonotida). We identified 52 miRNA genes representing 35 highly conserved miRNA families specific to Eumetazoa, Bilateria, Protostomia, and Spiralia, respectively, with overall high similarities to platyhelminth miRNA complements. In addition, we found four large piRNA clusters that also resemble flatworm piRNAs but not those earlier described for nematodes. Congruently, transcriptomic annotation revealed that the Lepidodermella protein machinery is highly similar to flatworms, too. Taken together, miRNA, piRNA, and protein data support a close relationship of gastrotrichs and flatworms.
Highlights
The Gastrotricha is an animal taxon with hitherto around 700 described species that are divided into the two main clades Macrodasyida and Chaetonotida [1,2,3]
The analyses revealed that the genome of L. squamata encodes an extensive small RNA repertoire of bona fide miRNAs and PIWI-interacting RNAs (piRNA), as well as the full miRNA & piRNA biogenesis and RNA interference (RNAi) protein machinery
Forty-six L. squamata miRNAs that belonged to 35 conserved families and 6 miRNAs with yet undescribed seed sequences were identified, all of them fulfilling the latest criteria for miRNA annotation [36]
Summary
The Gastrotricha is an animal taxon with hitherto around 700 described species that are divided into the two main clades Macrodasyida and Chaetonotida [1,2,3]. In contrast to short interfering RNAs (siRNAs), responsible for RNA interference (RNAi), and PIWI-interacting RNAs (piRNAs), responsible for genome integrity [25,26], miRNAs are deeply conserved in metazoans Their continuous addition to genomes during evolution has often been correlated with increasing morphological complexity and number of cell-types in a given organism [27,28,29,30]. Information on the presence of the RNAi pathway and small RNAs in gastrotrichs is lacking, but several studies have reported on miRNAs, piRNA, and the RNAi protein machinery in flatworms [40,42,43,44,45,46]. The comparison of miRNAs, and of piRNAs and RNAi protein machinery, to those of flatworms and nematodes together supports a close relationship of gastrotrichs to flatworms and not to nematodes
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