Abstract
ABSTRACTTrichoplax adhaerens is a flat, millimeter-sized marine animal that adheres to surfaces and grazes on algae. Trichoplax displays a repertoire of different feeding behaviors despite the apparent absence of a true nervous system with electrical or chemical synapses. It glides along surfaces to find food, propelled by beating cilia on cells at its ventral surface, and pauses during feeding by arresting ciliary beating. We found that when endomorphin-like peptides are applied to an animal, ciliary beating is arrested, mimicking natural feeding pauses. Antibodies against these neuropeptides label cells that express the neurosecretory proteins and voltage-gated calcium channels implicated in regulated secretion. These cells are embedded in the ventral epithelium, where they comprise only 4% of the total, and are concentrated around the edge of the animal. Each bears a cilium likely to be chemosensory and used to detect algae. Trichoplax pausing during feeding or spontaneously in the absence of food often induce their neighbors to pause as well, even neighbors not in direct contact. Pausing behavior propagates from animal to animal across distances much greater than the signal that diffuses from just one animal, so we presume that the peptides secreted from one animal elicit secretion from nearby animals. Signal amplification by peptide-induced peptide secretion explains how a small number of sensory secretory cells lacking processes and synapses can evoke a wave of peptide secretion across the entire animal to globally arrest ciliary beating and allow pausing during feeding.
Highlights
Placozoans are disk-shaped animals, up to several millimeters in diameter, that adhere to surfaces in littoral zones of tropical and subtropical seas (Schulze, 1883; Grell and Ruthmann, 1991; Schierwater, 2005)
Trichoplax arrests ciliary beating to cease gliding upon contact with algae, demonstrating that it has a sensory system that detects algae coupled to effectors that exert global control over ciliary beating
We discovered that endomorphin-like peptides (ELPs) consistently elicit cessation of gliding accompanied by ciliary arrest, precisely mimicking pauses that occur during feeding, when applied to the ambient seawater surrounding the animals
Summary
Placozoans are disk-shaped animals, up to several millimeters in diameter, that adhere to surfaces in littoral zones of tropical and subtropical seas (Schulze, 1883; Grell and Ruthmann, 1991; Schierwater, 2005). These secretory cells contain the machinery for calcium-regulated secretion, secretory SNARE proteins (syntaxin, synaptobrevin, SNAP-25; Smith et al, 2014) and complexin (Smith et al, 2017), as well as voltage-gated calcium channels (CaV2, CaV3; Senatore et al, 2016; Smith et al, 2017) Their granules label for RFamides (Schuchert, 1993; Smith et al, 2014), a class of neuropeptides that is common in cnidarians and bilaterians and is implicated in the control of ciliary beating (Katsukura et al, 2004; Braubach et al, 2006; Conzelmann et al, 2011). They each bear a single cilium that could be chemosensory and used to detect algae
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