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First published online November 13, 2009
Journal of Experimental Biology 212, 3892-3900 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.034561

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Cell kinetics of the marine sponge Halisarca caerulea reveal rapid cell turnover and shedding

J. M. De Goeij^1,2,*, A. De Kluijver¹, F. C. Van Duyl¹, J. Vacelet³, R. H. Wijffels⁴, A. F. P. M. De Goeij⁵, J. P. M. Cleutjens⁵ and B. Schutte⁶

¹ Department of Biological Oceanography, Royal Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg, Texel, The Netherlands
² The CARMABI Foundation, Caribbean Research & Management of Biodiversity, PO Box 2090, Willemstad, Curaçao, Netherlands Antilles
³ Centre d'Océanologie de Marseille, Aix-Marseille Université, CNRS UMR 6540 DIMAR, Station Marine d'Endoume, Rue Batterie des Lions, 13007 Marseille, France
⁴ Bioprocess Engineering Group, Wageningen University, PO Box 8129, 6700 EV Wageningen, The Netherlands
⁵ Department of Pathology, Maastricht University, PO Box 616, 6200 MD Maastricht, The Netherlands
⁶ Department of Molecular Cell Biology, Research Institute Growth and Development, Maastricht University, PO Box 616, 6200 MD Maastricht, The Netherlands

^* Author for correspondence (jmdegoeij{at}gmail.com)

Accepted 28 August 2009

This study reveals the peculiar in vivo cell kinetics and cell turnover of the marine sponge Halisarca caerulea under steady-state conditions. The tropical coral reef sponge shows an extremely high proliferation activity, a short cell cycle duration and massive cell shedding. Cell turnover is predominantly confined to a single cell population, i.e. the choanocytes, and in this process apoptosis only plays a minor role. To our knowledge, such fast cell kinetics under steady-state conditions, with high turnover by shedding in the absence of apoptosis, has not been observed previously in any other multicellular organism. The duration of the cell cycle in vivo resembles that of unicellular organisms in culture. Morphological and histochemical studies demonstrate compartmentalization of choanocytes in the sponge tissue, which corresponds well with its remarkable cellular kinetics. Coral reef cavity sponges, like H. caerulea, inhabit low nutrient tropical waters, forcing these organisms to filter large volumes of water and to capture the few nutrients efficiently. Under these oligotrophic conditions, a high cell turnover may be considered as a very useful strategy, preventing permanent damage to the sponge by environmental stress. Halisarca caerulea maintains its body mass and keeps its food uptake system up to date by constantly renewing its filter system. We conclude that studies on cell kinetics and functional morphology provide new and essential information on the growth characteristics and the regulation of sponge growth in vivo as well as in vitro and the role of choanocytes in tissue homeostasis.

Key words: Porifera, cell kinetics, cell cycle, BrdU, shedding, apoptosis

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