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

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.

[1]  T. Reese,et al.  Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses , 2017, Journal of Experimental Biology.

[2]  V. Hartenstein,et al.  Xenacoelomorpha Nervous Systems , 2017 .

[3]  A. Zhuravlev,et al.  First macrobiota biomineralization was environmentally triggered , 2017, Proceedings of the Royal Society B: Biological Sciences.

[4]  M. E. Hahn,et al.  Diversity as Opportunity: Insights from 600 Million Years of AHR Evolution. , 2017, Current opinion in toxicology.

[5]  W. Kristan Early evolution of neurons , 2016, Current Biology.

[6]  D. Erwin Early metazoan life: divergence, environment and ecology , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[7]  T. Reese,et al.  Coordinated Feeding Behavior in Trichoplax, an Animal without Synapses , 2015, PloS one.

[8]  T. Kadowaki,et al.  Evolution of TRP channels inferred by their classification in diverse animal species. , 2015, Molecular phylogenetics and evolution.

[9]  Todd H. Oakley,et al.  The shell-eyes of the chiton Acanthopleura granulata (Mollusca, Polyplacophora) use pheomelanin as a screening pigment , 2014 .

[10]  S. Tamm Formation of the Statolith in the Ctenophore Mnemiopsis leidyi , 2014, The Biological Bulletin.

[11]  C. Winters,et al.  Novel Cell Types, Neurosecretory Cells, and Body Plan of the Early-Diverging Metazoan Trichoplax adhaerens , 2014, Current Biology.

[12]  N. Pivovarova,et al.  Measurement of total calcium in neurons by electron probe X-ray microanalysis. , 2013, Journal of visualized experiments : JoVE.

[13]  P. Martinez,et al.  The nervous system of Isodiametra pulchra (Acoela) with a discussion on the neuroanatomy of the Xenacoelomorpha and its evolutionary implications , 2012, Frontiers in Zoology.

[14]  S. Johnsen,et al.  A Chiton Uses Aragonite Lenses to Form Images , 2011, Current Biology.

[15]  C. Jacobsen,et al.  Carbon K-edge spectra of carbonate minerals. , 2010, Journal of synchrotron radiation.

[16]  Daniel A. Fletcher,et al.  Cell mechanics and the cytoskeleton , 2010, Nature.

[17]  M. Aronova Structural models of “simple” sense organs by the example of the first Metazoa , 2009, Journal of Evolutionary Biochemistry and Physiology.

[18]  L. Staehelin,et al.  Statolith Sedimentation Kinetics and Force Transduction to the Cortical Endoplasmic Reticulum in Gravity-Sensing Arabidopsis Columella Cells[W][OA] , 2009, The Plant Cell Online.

[19]  Nicholas H. Putnam,et al.  The Trichoplax genome and the nature of placozoans , 2008, Nature.

[20]  R. Hill,et al.  Seawater Mg/Ca controls polymorph mineralogy of microbial CaCO3: A potential proxy for calcite‐aragonite seas in Precambrian time , 2008, Geobiology.

[21]  M. Davis,et al.  Protons Act as a Transmitter for Muscle Contraction in C. elegans , 2008, Cell.

[22]  O. Voigt,et al.  Field biology of placozoans (Trichoplax): distribution, diversity, biotic interactions. , 2007, Integrative and comparative biology.

[23]  S. Porter Seawater Chemistry and Early Carbonate Biomineralization , 2007, Science.

[24]  M. Braun,et al.  Gravity‐sensing and gravity‐related signaling pathways in unicellular model systems of protists and plants , 2006 .

[25]  M. Epple,et al.  Calcium sulfate hemihydrate (bassanite) statoliths in the cubozoan Carybdea sp. , 2006 .

[26]  Matthias Epple,et al.  Calcium sulfate hemihydrate is the inorganic mineral in statoliths of Scyphozoan medusae (Cnidaria). , 2005, Dalton transactions.

[27]  A. Knoll Biomineralization and Evolutionary History , 2003 .

[28]  M. Epple,et al.  Calcium sulfate hemihydrate in statoliths of deep-sea medusae , 2002 .

[29]  G. Horváth,et al.  Image formation by bifocal lenses in a trilobite eye? , 2000, Vision Research.

[30]  T. Ueda,et al.  Dynamic patterns in the locomotion and feeding behaviors by the placozoan Trichoplax adhaerence. , 1999, Bio Systems.

[31]  B. Boyan,et al.  A mechanism of adaptation to hypergravity in the statocyst of Aplysia californica , 1996, Hearing Research.

[32]  B. Sperlágh,et al.  Neuronal synthesis, storage and release of ATP , 1996 .

[33]  A. Ruthmann,et al.  The Mesenchyme-Like Layer of the Fiber Cells of Trichoplax adhaerens (Placozoa), a Syncytium , 1995 .

[34]  Richard L. Miller,et al.  Birefringent Granules in Placozoans (Trichoplax adhaerens) , 1994 .

[35]  U. Ehlers Comparative morphology of statocysts in the Plathelminthes and the Xenoturbellida , 1991, Hydrobiologia.

[36]  A. Ruthmann,et al.  The ventral epithelium of Trichoplax adhaerens (Placozoa): Cytoskeletal structures, cell contacts and endocytosis , 1986, Zoomorphology.

[37]  T. Fenchel,et al.  The Structure and Function of Müller Vesicles in Loxodid Ciliates1 , 1986 .

[38]  E. Ferrero,et al.  An Ultrastructural Account of Otoplanid Turbellaria Neuroanatomy II. The statocyst design: evolutionary and functional implications , 1985 .

[39]  U. Ehlers,et al.  Ultrastruktur der Statocyste von Ototyphlonemertes pallida (Keferstein, 1862) (Nemertini) , 1981, Zoomorphology.

[40]  J. Rassat,et al.  Trichoplax adhaerens F.E. Schulze (placozoa) in the scanning electron microscope , 1979, Zoomorphologie.

[41]  H. Nakahara,et al.  An electron microscope study of crystal calcium carbonate formation in the mouse otolith , 1979, The Anatomical record.

[42]  Robert A. Berner,et al.  The role of magnesium in the crystal growth of calcite and aragonite from sea water , 1975 .

[43]  E. Ferrero A Fine Structural Analysis of the Statocyst in Turbellaria Acoela , 1973 .

[44]  R. D. Campbell Statocyst lacking Cilia in the Coelenterate Corymorpha palma , 1972, Nature.

[45]  R. M. Eakin,et al.  Ultrastructure of sensory receptors in ascidian tadpoles , 1970, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[46]  R. Haedrich,et al.  Molecular structure and composition of fish otoliths , 1969 .

[47]  R. Croll,et al.  Trichoplax adhaerens, an enigmatic basal metazoan with potential. , 2014, Methods in molecular biology.

[48]  T. Furuichi,et al.  Mechanosensitive channels are activated by stress in the actin stress fibres, and could be involved in gravity sensing in plants. , 2014, Plant biology.

[49]  P. Masson,et al.  Gravity sensing and signal transduction in vascular plant primary roots. , 2013, American journal of botany.

[50]  M. Toyota,et al.  Gravitropism and mechanical signaling in plants. , 2013, American journal of botany.

[51]  Cronstedtite,et al.  Use of electron-energy loss near-edge fine structure in the study of minerals , 2007 .

[52]  A. Sievers,et al.  Centrifugation causes adaptation of microfilaments Studies on the transport of statoliths in gravity sensingChara rhizoids , 2005, Protoplasma.

[53]  D. Häder,et al.  Gravitational sensory transduction chain in flagellates , 2005 .

[54]  C. L. Singla,et al.  Statocysts of hydromedusae , 2004, Cell and Tissue Research.

[55]  F. Marmo,et al.  Calcite in the statoconia of amphibians: A detailed analysis in the frog Rana esculenta , 2004, Cell and Tissue Research.

[56]  M. Lebert,et al.  Graviperception and gravitaxis in algae. , 2001, Advances in space research : the official journal of the Committee on Space Research.

[57]  K. Rohde,et al.  Ultrastructure of the statocyst in an undescribed species of Luridae (Platyhelminthes: Rhabdocoela: Luridae) , 1993 .

[58]  R. Hanlon,et al.  Strontium is required for statolith development and thus normal swimming behaviour of hatchling cephalopods. , 1989, The Journal of experimental biology.

[59]  B. Budelmann,et al.  Morphological Diversity of Equilibrium Receptor Systems in Aquatic Invertebrates , 1988 .

[60]  T. Barrette,et al.  Calcitic microlenses as part of the photoreceptor system in brittlestars , 2022 .