The ventral epithelium of Trichoplax adhaerens deploys in distinct patterns cells that secrete digestive enzymes, mucus or diverse neuropeptides

Tatiana D Mayorova; Katherine Hammar; Christine A Winters; Thomas S Reese; Carolyn L Smith

doi:10.1242/bio.045674

The ventral epithelium of Trichoplax adhaerens deploys in distinct patterns cells that secrete digestive enzymes, mucus or diverse neuropeptides

Biol Open. 2019 Aug 9;8(8):bio045674. doi: 10.1242/bio.045674.

Authors

Tatiana D Mayorova¹, Katherine Hammar², Christine A Winters³, Thomas S Reese³, Carolyn L Smith⁴

Affiliations

¹ Laboratory of Neurobiology, National Institute of Neurological Disorders and Stroke, National Institutes of Health, 49 Convent Drive, Bethesda, MD 20892, USA mayorova@wsbs-msu.ru tatiana.mayorova@nih.gov.
² Central Microscopy Facility, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA.
³ Laboratory of Neurobiology, National Institute of Neurological Disorders and Stroke, National Institutes of Health, 49 Convent Drive, Bethesda, MD 20892, USA.
⁴ Light Imaging Facility, National Institute of Neurological Disorders and Stroke, National Institutes of Health, 35 Convent Drive, Bethesda, MD 20892, USA.

Abstract

The disk-shaped millimeter-sized marine animal, Trichoplax adhaerens, is notable because of its small number of cell types and primitive mode of feeding. It glides on substrates propelled by beating cilia on its lower surface and periodically pauses to feed on underlying microorganisms, which it digests externally. Here, a combination of advanced electron and light microscopic techniques are used to take a closer look at its secretory cell types and their roles in locomotion and feeding. We identify digestive enzymes in lipophils, a cell type implicated in external digestion and distributed uniformly throughout the ventral epithelium except for a narrow zone near its edge. We find three morphologically distinct types of gland cell. The most prevalent contains and secretes mucus, which is shown to be involved in adhesion and gliding. Half of the mucocytes are arrayed in a tight row around the edge of the ventral epithelium while the rest are scattered further inside, in the region containing lipophils. The secretory granules in mucocytes at the edge label with an antibody against a neuropeptide that was reported to arrest ciliary beating during feeding. A second type of gland cell is arrayed in a narrow row just inside the row of mucocytes while a third is located more centrally. Our maps of the positions of the structurally distinct secretory cell types provide a foundation for further characterization of the multiple peptidergic cell types in Trichoplax and the microscopic techniques we introduce provide tools for carrying out these studies.

Keywords: Digestive system evolution; Gland cell; Mucus; Nervous system evolution; Neuropeptide; Placozoa.