Cells containing aragonite crystals mediate responses to gravity in Trichoplax adhaerens (Placozoa), an animal lacking neurons and synapses.

Tatiana D Mayorova,Thomas S Reese,Natalia B Pivovarova,Maria A Aronova,Christine A Winters,Katherine Hammar,Carolyn L Smith,Richard D Leapman,Robert E. Steele

doi:10.1371/journal.pone.0190905

Abstract

Trichoplax adhaerens has only six cell types. The function as well as the structure of crystal cells, the least numerous cell type, presented an enigma. Crystal cells are arrayed around the perimeter of the animal and each contains a birefringent crystal. Crystal cells resemble lithocytes in other animals so we looked for evidence they are gravity sensors. Confocal microscopy showed that their cup-shaped nuclei are oriented toward the edge of the animal, and that the crystal shifts downward under the influence of gravity. Some animals spontaneously lack crystal cells and these animals behaved differently upon being tilted vertically than animals with a typical number of crystal cells. EM revealed crystal cell contacts with fiber cells and epithelial cells but these contacts lacked features of synapses. EM spectroscopic analyses showed that crystals consist of the aragonite form of calcium carbonate. We thus provide behavioral evidence that Trichoplax are able to sense gravity, and that crystal cells are likely to be their gravity receptors. Moreover, because placozoans are thought to have evolved during Ediacaran or Cryogenian eras associated with aragonite seas, and their crystals are made of aragonite, they may have acquired gravity sensors during this early era.

Highlights

Trichoplax adhaerens, a member of the ancient phylum Placozoa, inhabits warm oceans where it adheres to and feeds upon biofilms [1,2]
Lipophil cells, which are distributed throughout the ventral epithelium, release enzymes externally that lyse the algae, and the lysate is endocytosed by the ventral epithelial cells [7]
We analyzed crystal cells by serial section standard errors of mean (SEM) to understand the three-dimensional arrangement of the intracellular crystal with respect to other organelles

Summary

Introduction

Trichoplax adhaerens, a member of the ancient phylum Placozoa, inhabits warm oceans where it adheres to and feeds upon biofilms [1,2]. Fiber cells are not represented on the surface of the animal, but lie in a space between the ventral and thin dorsal epithelia, where they give rise to long branching processes that contact other cells [4,6,8]. The least prevalent type, reside in the space between the ventral and dorsal epithelia but, unlike fiber cells, occur only in a narrow band ~20 μm from edge of the animal. The crystal is surrounded by mitochondria but the cytoplasm in the rest of the crystal cell is remarkably clear of organelles [4,9].

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Results

Conclusion