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Chloroplast and oxygen evolution changes in Symbiodinium sp. as a response to latrunculin and butanedione monoxime treatments under various light conditions

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Abstract

The actin cytoskeleton is a dynamic structure that provides an interactive platform for organelles and cellular components. It also serves as track for membranes and vesicles that move via myosin. The actin cytoskeleton of Symbiodinium is a well-organized reticular structure suggestive of multiple membrane interactions, very likely including those of the chloroplast. The Symbiodinium chloroplast membrane network is, in turn, a highly organized structure, suggestive of being under the control of an organizing network. We visualized the chloroplast membranes of cultured Symbiodinium sp. under various light conditions and observed changes dependent on illumination intensity. Since we suspected interaction between these two organelles, and we knew that the Symbiodinium actin cytoskeleton collapses upon treatment with either latrunculin B, an actin microfilament-disrupting agent, or butanedione monoxime, a myosin function inhibitor, we tested the Symbiodinium sp. oxygen evolution in their presence. Upon latrunculin B addition, the oxygen production decreased compared to non-treated cells; however, this was not observed after a 24 h latrunculin treatment. On the contrary, butanedione monoxime treatment caused a non-recoverable dysfunction of the chloroplast causing a severe loss in oxygen production even after long-term exposure. Using electron microscopy, we observed an alteration of the Symbiodinium sp. chloroplast distribution after latrunculin B treatment, with respect to untreated cells. Furthermore, a thorough disorganization of the chloroplast grana was observed after butanedione monoxime treatment. These data suggest that an actomyosin system would be important for chloroplast organization and distribution, and critical for normal photosynthetic function of Symbiodinium sp.

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Abbreviations

BDM:

Butanedione monoxime

CLSM:

Confocal laser scanning microscopy

latB:

Latrunculin B

PBS:

Phosphate-buffered saline

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Acknowledgments

The authors greatly acknowledge Sophie Pagnotta of the CCMA (Centre Commun de Microscopie Appliquée, Université Nice Sophia Antipolis, Microscopy and Imaging platform Côte d’Azur, MICA) and Maëlle Ogier of the PRISM (Platform of Resources in Imaging and Scientific Microscopy, Institut de Biologie Valrose, Université Nice Sophia Antipolis). SBV and PF thank Dr. Pierre-Laurent Merle for his helpful comments on the manuscript. Dr. M.A. Villanueva’s sabbatical visit was supported by a PASPA fellowship from DGAPA-UNAM, México; we also thank the University of Nice Sophia Antipolis for his hosting.

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    Authors and Affiliations

    1. Instituto de Ciencias del Mar y Limnología, Unidad Académica de Sistemas Arrecifales, Universidad Nacional Autónoma de México-UNAM, Prol. Avenida Niños Héroes S/N, 77580, Puerto Morelos, Quintana Roo, México

      Marco A. Villanueva

    2. Faculté des Sciences, Université Nice Sophia Antipolis, UMR 7138 “Evolution Paris Seine”, équipe ‘Symbiose marine’, Parc Valrose, 06103, Nice Cedex 02, France

      Stéphanie Barnay-Verdier, Fabrice Priouzeau & Paola Furla

    3. Université Pierre-et-Marie-Curie, UMR 7138 “Evolution Paris Seine”, 7, quai Saint-Bernard, 75252, Paris Cedex 05, France

      Stéphanie Barnay-Verdier, Fabrice Priouzeau & Paola Furla

    4. CNRS, UMR 7138 “Evolution Paris Seine”, 7, quai Saint-Bernard, 75252, Paris Cedex 05, France

      Stéphanie Barnay-Verdier, Fabrice Priouzeau & Paola Furla

    Authors
    1. Marco A. Villanueva
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    2. Stéphanie Barnay-Verdier
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    3. Fabrice Priouzeau
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    4. Paola Furla
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    Corresponding authors

    Correspondence to Marco A. Villanueva or Paola Furla.

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    This article is dedicated to the loving memory of our beloved young colleague and friend, Dr. Pierre-Laurent Merle, who passed away on February 1, 2015.

    Stéphanie Barnay-Verdier and Fabrice Priouzeau contributed equally to this work.

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    Villanueva, M.A., Barnay-Verdier, S., Priouzeau, F. et al. Chloroplast and oxygen evolution changes in Symbiodinium sp. as a response to latrunculin and butanedione monoxime treatments under various light conditions. Photosynth Res 124, 305–313 (2015). https://doi.org/10.1007/s11120-015-0142-9

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    • DOI: https://doi.org/10.1007/s11120-015-0142-9

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