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Impairment of symbiont photosynthesis increases host cell proliferation in the epidermis of the sea anemone Aiptasia pallida

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Abstract

Corals exposed to environmental stresses need to engage appropriate physiological strategies to survive. Here, we examined tissue modifications following algal dysfunction. Aiptasia pallida was exposed during 1 week to 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), the herbicide called diuron. DCMU treatment produced a drastic loss in photosynthetic efficiency and a subsequent diminution of algae density over the following days. Cell proliferation evaluated by measuring the number of cells labeled with a thymidine analogue (EdU) revealed a significant increase in EdU+ cells in the epidermis after 1 week of DCMU incubation and in the gastrodermis at 4 weeks. TUNEL histology showed that the extent of cell death was, however, similar in the epidermis of control and treated specimens. In addition, we noticed a significant effect of DCMU treatment on the density of epidermal mucocytes after 1, 2 and 4 weeks. These results show that inhibition of Symbiodinium photosynthesis in the absence of any known direct effect of DCMU on host cells can induce an increase in epidermal host cell proliferation in both the epidermis and the gastrodermis. While new host gastrodermal cells are likely to promote tissue regeneration in order to recruit new algae, the new host epidermal cells may contribute to tissue adaptation following a decrease in energy income. Some of these new epidermal cells, such as mucocytes, may contribute to an eventual increase in the host heterotrophic ability until restoration of algal autotrophic contribution.

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Abbreviations

CHAR:

Contribution of heterotrophically acquired carbon to daily animal respiration

DCMU:

3-(3,4-Dichlorophenyl)-1,1-dimethylurea

EdU:

5-Ethynyl-2′-deoxyuridine

EdU+:

5-Ethynyl-2′-deoxyuridine positive

F 0 :

Initial fluorescence level

F M :

Maximum fluorescence level

ΦPSII:

Effective photochemical quantum yield

PSII:

Photosystem II

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Acknowledgments

We thank the two anonymous reviewers for their helpful comments and the laboratory of Oceanology (ULg) for the diving PAM. DF is a recipient of a F.R.I.A PhD Studentship. JCP was supported by funding from the F.R.S.-F.N.R.S. (FRFC 2.4.631.09) and from the University of Liège (C-13/22). PAM was funded by ULg C-10/78 Fonds Spéciaux—crédits classiques. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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The authors have declared that no conflict of interest.

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Authors and Affiliations

  1. Ecophysiologie et Physiologie Animale, Département de Biologie, Ecologie et Evolution, Université de Liège, Boulevard du Rectorat 27 (Bat. B22), 4000, Liège, Belgium

    David Fransolet, Stéphane Roberty & Jean-Christophe Plumier

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  1. David Fransolet
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  2. Stéphane Roberty
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  3. Jean-Christophe Plumier
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Correspondence to Jean-Christophe Plumier.

Additional information

Communicated by R. Hill.

David Fransolet and Stéphane Roberty have equally contributed to this article.

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Fransolet, D., Roberty, S. & Plumier, JC. Impairment of symbiont photosynthesis increases host cell proliferation in the epidermis of the sea anemone Aiptasia pallida . Mar Biol 161, 1735–1743 (2014). https://doi.org/10.1007/s00227-014-2455-1

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