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.
Highlights
Excretory organs are specialized organs that remove toxic metabolic waste products and control water and ion balance in animals based on the principles of ultrafiltration, active transport, and passive transport/diffusion [1]
To identify potential excretory sites in xenacoelomorphs, we examined the expression of the entire set of these candidate excretion-related genes in the acoel Isodiametra pulchra and the nemertodermatid Meara stichopi, which differ in their digestive system composition (I. pulchra has a syncytial, lumenless gut, whereas M. stichopi has an epithelia-lined, cellular gut [49] (S1b Fig)
Our findings suggest that I. pulchra uses different mechanisms for ammonia excretion that are known from nephrozoans; an active ammonia excretion mechanism via Na+/K+[NH4+] ATPase (NKA) through the digestive system, as suggested by in situ hybridization, and a passive vesicular transport mechanism likely mediated by Rhesus, through digestive and likely epidermal tissues
Summary
Excretory organs are specialized organs that remove toxic metabolic waste products and control water and ion balance in animals based on the principles of ultrafiltration, active transport, and passive transport/diffusion [1]. They are only present in Nephrozoa (Deuterostomia + Protostomia) [2] (Fig 1a) and, based on morphological correspondences, can be grouped into two major architectural units: the protonephridia, only found in Protostomia, and the metanephridia, present in both Deuterostomia and Protostomia [3,4]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
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