Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges

Abstract

BackgroundOne of the hallmarks of multicellular organisms is the ability of their cells to trigger responses to the environment in a coordinated manner. In recent years primary cilia have been shown to be present as ‘antennae’ on almost all animal cells, and are involved in cell-to-cell signaling in development and tissue homeostasis; how this sophisticated sensory system arose has been little-studied and its evolution is key to understanding how sensation arose in the Animal Kingdom. Sponges (Porifera), one of the earliest evolving phyla, lack conventional muscles and nerves and yet sense and respond to changes in their fluid environment. Here we demonstrate the presence of non-motile cilia in sponges and studied their role as flow sensors.ResultsDemosponges excrete wastes from their body with a stereotypic series of whole-body contractions using a structure called the osculum to regulate the water-flow through the body. In this study we show that short cilia line the inner epithelium of the sponge osculum. Ultrastructure of the cilia shows an absence of a central pair of microtubules and high speed imaging shows they are non-motile, suggesting they are not involved in generating flow. In other animals non-motile, ‘primary’, cilia are involved in sensation. Here we show that molecules known to block cationic ion channels in primary cilia and which inhibit sensory function in other organisms reduce or eliminate sponge contractions. Removal of the cilia using chloral hydrate, or removal of the whole osculum, also stops the contractions; in all instances the effect is reversible, suggesting that the cilia are involved in sensation. An analysis of sponge transcriptomes shows the presence of several transient receptor potential (TRP) channels including PKD channels known to be involved in sensing changes in flow in other animals. Together these data suggest that cilia in sponge oscula are involved in flow sensation and coordination of simple behaviour.ConclusionsThis is the first evidence of arrays of non-motile cilia in sponge oscula. Our findings provide support for the hypothesis that the cilia are sensory, and if true, the osculum may be considered a sensory organ that is used to coordinate whole animal responses in sponges. Arrays of primary cilia like these could represent the first step in the evolution of sensory and coordination systems in metazoans.

Elements of a ‘nervous system’ in sponges

“…This links both the osculum and the cilia in the osculum with the sneeze behaviour. Furthermore, neomycin sulphate, FM 1-43 and gadolinium all reduce or block the ability of the sponge to carry out a 'sneeze' and the effect is reversible (Ludeman et al, 2014). The fact that cilia appear at the osculum of all sponges studied so far (even hexactinellids), suggests that this is a common sensory organ in Porifera.…”

“…A suite of papers describing the morphology and development of canals, choanocytes and spicules established this as an easy-to-use system (Weissenfels, 1976;Weissenfels and Landschoff, 1977;Weissenfels and Striegler, 1979;Weissenfels, 1980;Weissenfels, 1981;Weissenfels and Hündgen, 1981;Weissenfels, 1982;Weissenfels, 1983;Weissenfels, 1984;Wachtmann et al, 1990;Weissenfels et al, 1990;Weissenfels, 1992). The attractiveness of this model, which was highlighted by Yoko Watanabe through the film 'Life of the freshwater sponge' (Tokyo Film Corporation http://tokyocinema.net/EnglVieo.htm), has led to more recent studies on signalling and coordination of sponge behaviour (Elliott and Leys, 2007;Elliott and Leys, 2010), epithelia Adams, 2010), patterning and most recently, sensory cells (Ludeman et al, 2014). And since freshwater sponges are easily obtained and cultured in Europe, Japan and North America, there is a body of knowledge on the genetics of development (Richelle-Maurer et al, 1998;RichelleMaurer and Van de Vyver, 1999;Nikko et al, 2001;Funayama et al, 2005a;Funayama et al, 2005b;Mohri et al, 2008;Funayama et al, 2010;Holstien et al, 2010;Funayama, 2013) and even the possibility of using RNA interference methods (Rivera et al, 2011).…”

“…Short (4-6 μm long), non-motile, 'primary' cilia have been found to line the inside of oscula in all sponges studied so far by scanning electron microscopy ( Fig. 2A-D) (Nickel, 2010;Ludeman et al, 2014). Primary cilia are found on all cells in vertebrates and many cells in invertebrates, and are involved in sensing gradients of chemicals, light and flow (vibration) via ion channels of the transient receptor potential (TRP) family (Singla and Reiter, 2006).…”

“…2E,F), as do primary cilia in the lateral line of fish and inner-ear hair cells (Ou et al, 2009). The cilium is non motile and lacks a central pair of microtubules (Ludeman et al, 2014;Fig. 2G,H).…”

“…In sponges, primary cilia label with FM 1-43, a steryl dye, and also with a conjugate to the antibiotic neomycin sulphate, both non-specific calcium channel blockers (Ludeman et al, 2014;Fig. 2E,F), as do primary cilia in the lateral line of fish and inner-ear hair cells (Ou et al, 2009).…”