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Hidden cell diversity in Placozoa: ultrastructural insights from Hoilungia hongkongensis

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Abstract

From a morphological point of view, placozoans are among the most simple free-living animals. This enigmatic phylum is critical for our understanding of the evolution of animals and their cell types. Their millimeter-sized, disc-like bodies consist of only three cell layers that are shaped by roughly seven major cell types. Placozoans lack muscle cells and neurons but are able to move using their ciliated lower surface and take up food in a highly coordinated manner. Intriguingly, the genome of Trichoplax adhaerens, the founding member of the enigmatic phylum, has disclosed a surprising level of genetic complexity. Moreover, recent molecular and functional investigations have uncovered a much larger, so-far hidden cell-type diversity. Here, we have extended the microanatomical characterization of a recently described placozoan species—Hoilungia hongkongensis. In H. hongkongensis, we recognized the established canonical three-layered placozoan body plan but also came across several morphologically distinct and potentially novel cell types, among them novel gland cells and “shiny spheres”-bearing cells at the upper epithelium. Thus, the diversity of cell types in placozoans is indeed higher than anticipated.

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The data that support the findings of this study are available on https://zenodo.org.

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Acknowledgements

We thank E. Bedoshvili, A. Miroliubov, and V. Starunov for their help in electron microscopy, sample preparation, and advice for SEM protocols.

Funding

This work was supported by the Human Frontiers Science Program (RGP0060/2017) and National Science Foundation (1146575, 1557923, 1548121, and 1645219) grants to L.L.M., Russian Ministry of Science and High Education (agreement 075-15-2020-801) grant to D.R., and the Swiss National Science Foundation (#31003A_182732) grant to D.F. The research reported in this publication was also supported in part by the National Institute of Neurological Disorders and Stroke of the National Institutes of Health under Award Number R01NS114491 (to L.L.M.). M. Eitel received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie grant agreement no 764840.

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Author notes

  1. Daria Y. Romanova, Frédérique Varoqueaux, Dirk Fasshauer, and Leonid L. Moroz contributed equally to this work.

Authors and Affiliations

  1. Department of Fundamental Neurosciences, University of Lausanne, 1005, Lausanne, Switzerland

    Daria Y. Romanova, Frédérique Varoqueaux & Dirk Fasshauer

  2. Cellular Neurobiology of Learning Lab, Institute of Higher Nervous Activity and Neurophysiology, Moscow, 117485, Russia

    Daria Y. Romanova

  3. Department of Computational Biology, University of Lausanne, 1015, Lausanne, Switzerland

    Frédérique Varoqueaux & Dirk Fasshauer

  4. Electron Microscopy Facility, University of Lausanne, Lausanne, Switzerland

    Jean Daraspe

  5. Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow, 119991, Russia

    Mikhail A. Nikitin

  6. Kharkevich Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, 127994, Russia

    Mikhail A. Nikitin

  7. Department of Earth and Environmental Sciences, Paleontology and Geobiology, Ludwig-Maximilians Universität München, Munich, Germany

    Michael Eitel

  8. Whitney Laboratory for Marine Bioscience, University of Florida, St. Augustine, FL, 32080, USA

    Leonid L. Moroz

  9. Departments of Neuroscience and McKnight Brain Institute, University of Florida, Gainesville, FL, 32610, USA

    Leonid L. Moroz

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  1. Daria Y. Romanova
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Contributions

D.Y.R., F.V., D.F., and L.L.M. designed the study; D.Y.R., F.V., J.D., M.A.N., M.E., and L.L.M analyzed the data; D.Y.R., L.L.M, F.V., and D.F. wrote the paper; and all authors reviewed, commented on, and edited the manuscript.

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Correspondence to Daria Y. Romanova, Dirk Fasshauer or Leonid L. Moroz.

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Romanova, D.Y., Varoqueaux, F., Daraspe, J. et al. Hidden cell diversity in Placozoa: ultrastructural insights from Hoilungia hongkongensis. Cell Tissue Res 385, 623–637 (2021). https://doi.org/10.1007/s00441-021-03459-y

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