Annelid adult cell type diversity and their pluripotent cellular origins

Abstract

Many annelids can regenerate missing body parts or reproduce asexually, generating all cell types in adult stages. However, the putative adult stem cell populations involved in these processes, and the diversity of cell types generated by them, are still unknown. To address this, we recover 75,218 single cell transcriptomes of the highly regenerative and asexually-reproducing annelid Pristina leidyi. Our results uncover a rich cell type diversity including annelid specific types as well as novel types. Moreover, we characterise transcription factors and gene networks that are expressed specifically in these populations. Finally, we uncover a broadly abundant cluster of putative stem cells with a pluripotent signature. This population expresses well-known stem cell markers such as vasa, piwi and nanos homologues, but also shows heterogeneous expression of differentiated cell markers and their transcription factors. We find conserved expression of pluripotency regulators, including multiple chromatin remodelling and epigenetic factors, in piwi+ cells. Finally, lineage reconstruction analyses reveal computational differentiation trajectories from piwi+ cells to diverse adult types. Our data reveal the cell type diversity of adult annelids by single cell transcriptomics and suggest that a piwi+ cell population with a pluripotent stem cell signature is associated with adult cell type differentiation.

Hooked on zombie worms? Genetic blueprints of bristle formation in Osedax japonicus (Annelida)

“…The third gene we investigated for its potential role in chaetogenesis was NF70, an intermediate filament protein known for its involvement in cytoskeletal processes and previously identified as expressed within the chaetal follicle [35]. Our DGE analysis revealed that NF70's expression levels were relatively constant throughout development, with a notable increase from as early as day 1.…”

“…NF70 was selected for its potential role in chaetogenesis, as suggested by single-cell RNA sequencing results from Ref. [35], which indicated its expression in chaetal sacs. Our phylogenetic analysis of NF70 genes, extracted from public databases, revealed that OjapNF70 clustered with NF70 sequences from other annelids.…”

“…While a set of candidate genes involved in chaetogenesis has been previously proposed [19], they remain unpublished. The increasing availability of single-cell RNA-seq data in annelids [35] enhances the feasibility of screening for genes involved in chaetogenesis and other developmental processes. Our application of in-situ HCR in Osedax demonstrates that this technique is not only effective for confirming gene expression within the follicle but also provides cell-level resolution.…”