The ontogeny of choanocyte chambers during metamorphosis in the demosponge Amphimedon queenslandica

Abstract

BackgroundThe aquiferous body plan of poriferans revolves around internal chambers comprised of choanocytes, a cell type structurally similar to choanoflagellates. These choanocyte chambers perform a range of physiological and developmental functions, including the capture of food and the generation of stem cells. Despite the increasing interest for choanocytes as sponge stem cells, there is limited knowledge on the development of choanocyte chambers. Using a combination of cell lineage tracing, antibody staining and EdU labeling, here we examine the development of choanocytes and the chambers they comprise during metamorphosis in the marine demosponge Amphimedon queenslandica.ResultsLineage-tracing experiments show that larval epithelial cells transform into mesenchymal pluripotent stem cells, resembling archeocytes, within 24 h of initiating metamorphosis. By 36 h, some of these labeled archeocyte-like cells have differentiated into choanocytes that will form the first postlarval choanocyte chambers. Non-labeled cells also contribute to these primary choanocyte chambers, consistent with these chambers being a chimera of multiple transdifferentiated larval cell types and not the proliferation of a single choanocyte precursor. Moreover, cell proliferation assays demonstrate that, following the initial formation of choanocyte chambers, chambers grow at least partially by the proliferation of choanocytes within the chamber, although recruitment of individual cells into established chambers also appears to occur. EdU labeling of postlarvae and juveniles reveals that choanocyte chambers are the primary location of cell proliferation during metamorphosis.ConclusionOur results show that multiple larval cell lineages typically contribute to formation of individual choanocyte chambers at metamorphosis, contrary to previous reports in other species that show sponge choanocyte chambers form clonally. Choanocytes in postlarval and juvenile A. queenslandica chambers can also divide, with choanocyte chambers being the primary location of cell proliferation. Interestingly, the level of cell proliferation varies greatly between chambers and appears to be contingent on the size, location and developmental state of the chamber. Small chambers on the periphery of the body tend to possess more dividing cells. As choanocytes can also dedifferentiate into archeocyte-like cells, cell proliferation in chambers may not only contribute to chamber growth and self-renewal but also increase the number of pluripotent archeocytes.

Exploring the bZIP regulatory network in the sponge Amphimedon queenslandica: insights into the ancestral animal regulatory genome

“…At this stage, multiple cells types are identifiable, including two cell types that can transdifferentiate -choanocytes and archeocytes (Sogabe et al, 2016). The expression of multiple A. queenslandica bZIPS in these two sponge stem cells (Funayama, 2013) is consistent with putative conserved roles as master regulators of cellular differentiation and proliferation in animals (Miller, 2009;Shaulian and Karin, 2002;Weirauch and Hughes, 2011).…”

“…The first indications of morphogenesis starts at about 36 hps and by 3 d the functional juvenile body plan is formed Sogabe et al, 2016). At this stage, multiple cells types are identifiable, including two cell types that can transdifferentiate -choanocytes and archeocytes (Sogabe et al, 2016).…”

The characterization of larval homology: transcriptomic insights into the origin and evolution of animal life cycles

“…This enrichment can be rationalized with known prevalence of the cell turnover events (Alexander et al 2014), such as the phagocytosis of apoptosed larval cells during metamorphosis in A. queenslandica (Sogabe et al 2016), that have also been described in other sponge species (Bergquist andGlasglow 1986, Funayama 2013). Additionally, the enrichment of the GO term for vesicle-mediated transport may also reflect histological evidence for the digestion and transport of bacterial cells associated with the maintenance of symbiont communities during metamorphosis via vesicle-mediated phagocytosis (Fieth et al 2016).…”

“…Hadfield et al 2001, Jackson et al 2002, Hadfield 2011, Grasso et al 2011, Ueda et al 2016, and early body plan establishment during metamorphosis (e.g. Woods et al 2004, Williams et al 2009, Sogabe et al 2016, hence GRNs expressed earlier in the life cycle may remain more impervious to evolutionary change.…”

Horizontal gene transfer in the sponge Amphimedon queenslandica

“…In addition, many animals have intracellular bacterial symbionts (Dunning Hotopp et al 2007;Wernegreen 2012;McFall-Ngai et al 2013). Furthermore, many bacterial symbionts are vertically transmitted between generations through reproductive cells (Krueger et al 1996;Moran and Baumann 2000;Webster et al 2010;Fan et al 2012 Sogabe et al 2016), which are pluripotent cells that move throughout the body, are continuously exposed to bacteria, and give rise to oocyte germ cells (Funayama 2010). Therefore, not only are there biological circumstances in which some animals have ample whole bacteria or free and foreign DNA within cells, but because of cell fate specification, an abundant supply of foreign sequences can exist within evolutionarily relevant cells.…”