New insights into the body plan of Trichoplax adhaerens

Neurons are highly specialized for fast information transfer that takes place in the form of vesicular neurotransmitter release at specialized junctions, the chemical synapses. Synapses evolved early in animal evolution, and relatively simple nervous systems can be found in early branching animals, such as jellyfish. By contrast, sponges or placozoans appear not to be equipped with bona fide synapses. In a previous study, we had discovered that choanoflagellates, a group of mostly single-celled eukaryotes that is thought to be the closest known sister group to animals, already possess a primordial secretion machinery that may have served as a starting point for the evolution of the more complex machinery found in animals, in particular in vertebrates.

We now wanted to take a closer look at the very early stage of the development of the neuronal secretory apparatus by studying the placozoan Trichoplax adhaerens, an organism positioned near the root of the animal tree. Trichoplax is a simple, free-living marine animal that glides on cilia to find and ingest algae in shallow seas. The millimeter-sized animal has been described as having only four cell types that form two sheets around a more loosely packed interior. Its simple, three-layered organization, seemingly lacking muscles or nerves, sparked a debate about the evolutionary origins of metazoans soon after its first descriptions in the late nineteenth century by Franz Eilhard Schulze. Trichoplax adhaerens was largely forgotten until investigations were started again in the 1970´s by Karl Gottlieb Grell, who made the first electron microscopic observations.

Sequencing of its genome has revealed that Trichoplax has a remarkable set of the genes that control cell differentiation and cell-cell communication in more complex animals, including vertebrates. Lately, new sequence information has repeatedly shaken the metazoan Tree of Life, although no consensus about the branching order of basic metazoans has yet been reached. This is not a surprise as the different branches (i.e. Bilateria and the four non-bilaterian phyla Porifera, Placozoa, Ctenophora, and Cnidaria) diverged hundreds of millions of years ago.

While much is known about Trichoplax´s genome, much less was known about its structure, mainly because of its adverse reaction to the canonical preparation for electron and immunofluorescence microscopy.  In collaboration with Thomas S. Reese and Carolyn L. Smith from the NIH (Bethesda, MD, USA) and the laboratory of Bernd Schierwater (ITZ, Hannover, Germany), we overcame this problem by using high-pressure freezing techniques. Our paper on Novel Cell Types, Neurosecretory Cells and Body Plan of the Early-Diverging Metazoan, Trichoplax adhaerens provides extensive new structural information about this remarkable animal. Using confocal and electron microscopy, we provide a comprehensive catalogue of the different cell types, their numbers, and their locations in Trichoplax. Our study shows that Trichoplax has a well-organized body plan with specialized cells deployed at specific locations to serve the needs of the animal. However, while the role of the two epithelial cell types are obvious, some of the cell types of Trichoplax, for instance the two new cell types, lipophils and crystal cells, discovered by us, are rather unusual, rendering it difficult to assign them a clear role. Interestingly, we found that neuronal proteins are expressed in gland cells, suggesting that these cells have a neurosecretory function that might control the locomotor and feeding behavior of Trichoplax. As gland cells do not appear to form synapses, they seem to constitute an ancestral rather than a derived and simplified version of a neuronal cell. We hope that our morphological analysis will nurture further investigations in Trichoplax.

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