Active mode of excretion across digestive tissues predates the origin of excretory organs

Abstract

Most bilaterian animals excrete toxic metabolites through specialized organs, such as nephridia and kidneys, which share morphological and functional correspondences. In contrast, excretion in non-nephrozoans is largely unknown, and therefore the reconstruction of ancestral excretory mechanisms is problematic. Here, we investigated the excretory mode of members of the Xenacoelomorpha, the sister group to Nephrozoa, and Cnidaria, the sister group to Bilateria. By combining gene expression, inhibitor experiments, and exposure to varying environmental ammonia conditions, we show that both Xenacoelomorpha and Cnidaria are able to excrete across digestive-associated tissues. However, although the cnidarian Nematostella vectensis seems to use diffusion as its main excretory mode, the two xenacoelomorphs use both active transport and diffusion mechanisms. Based on these results, we propose that digestive-associated tissues functioned as excretory sites before the evolution of specialized organs in nephrozoans. We conclude that the emergence of a compact, multiple-layered bilaterian body plan necessitated the evolution of active transport mechanisms, which were later recruited into the specialized excretory organs.

Acoel single-cell transcriptomics: cell-type analysis of a deep branching bilaterian

“…These cells could be serving the function of both distributing nutrients to other cells and/or, like an excretory system, to filtrate and reabsorb necessary elements while discarding waste. The existence of such an excretory cell type in I. pulchra was previously proposed in Andrikou et al (2019). We looked for the genes tested as excretory markers in that study and found high expression levels of nephrin/kirre and aquaporin b in a large population of these transporter-rich cells, consistent with their hypothesis.…”

“…Since its original description (Smith and Bush 1991), the use of this species in the laboratory has been gaining acceptance because of their easy maintenance and of the availability of different technologies, from in situ and immunochemistry to the gene knockdown using RNAi interference (DeMulder et al 2009;Moreno et al 2010) and transcriptome sequences (Cannon et al 2016;Brauchle et al 2018). Isodiametra pulchra has been instrumental in developing many key studies of the Xenacoelomorpha, for instance: detailed descriptions of stem-like cells (DeMulder et al 2009), the nervous system (Achatz & Martinez 2012), mesoderm (Ladurner et al 2000;Rieger et al 2003; or excretory cells (Andrikou et al 2019).…”

Multiple paedomorphic lineages of soft-substrate burrowing invertebrates: parallels in the origin of Xenocratena and Xenoturbella

“…Notably, while this study had already been completed, a new bilaterian-wide analysis of a 1,173 gene dataset was published and reconfirmed the relationship of Xenoacoelomorpha to Deuterostomia (Ambulacraria) and not as a basal off-shoot of Bilateria [90]. Furthermore, a recent investigation of sperm morphology of Xenoturbella shows close similarities with the sperm of hemichordates [91] and the excretory system of Xenoacoelomorpha (despite the absence of specialized nephridia) shows an active transport mechanism similar to Bilateria and not to Cnidaria [92]. Therefore, this profound duality of the phylogenetic position of Xenoacoelomorpha and homedomain organisation coupled with the model that a soft-substrate environment facilitates paedomorphic evolution (Fig 1) suggest that Xenoacoelomorpha originated from an ancestor that was more complex than modern Xenoturbella, and that this could fill the gap between cnidarian (as unambiguous sister group to bilaterians) [8][9][10][11]89] and bilaterian radiations.…”

A single origin of animal excretory organs

“…The orthologues of the UF-related genes are also present in the potential sister group of Nephrozoa, the xenacoelomorphs, where they are broadly expressed in tissues not related with the excretion process, e.g. in gonads and nervous system (41). This suggests that recruitment of those three genes into formation of excretory filter was an important step in the evolution of specialized excretory organs in Nephrozoa.…”