The origin of Metazoa: a transition from temporal to spatial cell differentiation

Authors

  • Kirill V. Mikhailov,

    1. Belozersky Institute for Physicochemical Biology, Lomonosov Moscow State University, Moscow, Russian Federation
    2. Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, Moscow, Russian Federation
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  • Anastasiya V. Konstantinova,

    1. Belozersky Institute for Physicochemical Biology, Lomonosov Moscow State University, Moscow, Russian Federation
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  • Mikhail A. Nikitin,

    1. Belozersky Institute for Physicochemical Biology, Lomonosov Moscow State University, Moscow, Russian Federation
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  • Peter V. Troshin,

    1. Membrane Protein Structure Initiative, STFC Daresbury Laboratory, Warrington, Cheshire WA4 4AD, UK
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  • Leonid Yu. Rusin,

    1. Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow 127994, Russian Federation
    2. Faculty of Biology, Lomonosov Moscow State University, Moscow, Russian Federation
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  • Vassily A. Lyubetsky,

    1. Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow 127994, Russian Federation
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  • Yuri V. Panchin,

    1. Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow 127994, Russian Federation
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  • Alexander P. Mylnikov,

    1. Institute for Biology of Inland Waters, Russian Academy of Sciences, Yaroslavskaya oblast, Borok, Russian Federation
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  • Leonid L. Moroz,

    1. The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Boulevard, St. Augustine, FL, USA
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  • Sudhir Kumar,

    1. Center for Evolutionary Functional Genomics, Biodesign Institute, School of Life Sciences, Arizona State University, Tempe, AZ, USA
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  • Vladimir V. Aleoshin

    Corresponding author
    1. Belozersky Institute for Physicochemical Biology, Lomonosov Moscow State University, Moscow, Russian Federation
    • Belozersky Institute for Physicochemical Biology, Lomonosov Moscow State University, Leninskie Gory 1/40, Moscow 119991, Russian Federation.
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  • Dedicated to the 60th year of A. A. Zakhvatkin's Synzoospore hypothesis.

Abstract

For over a century, Haeckel's Gastraea theory remained a dominant theory to explain the origin of multicellular animals. According to this theory, the animal ancestor was a blastula-like colony of uniform cells that gradually evolved cell differentiation. Today, however, genes that typically control metazoan development, cell differentiation, cell-to-cell adhesion, and cell-to-matrix adhesion are found in various unicellular relatives of the Metazoa, which suggests the origin of the genetic programs of cell differentiation and adhesion in the root of the Opisthokonta. Multicellular stages occurring in the complex life cycles of opisthokont protists (mesomycetozoeans and choanoflagellates) never resemble a blastula. Here, we discuss a more realistic scenario of transition to multicellularity through integration of pre-existing transient cell types into the body of an early metazoon, which possessed a complex life cycle with a differentiated sedentary filter-feeding trophic stage and a non-feeding blastula-like larva, the synzoospore. Choanoflagellates are considered as forms with secondarily simplified life cycles.

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