Ingredients for protist coexistence: competition, endosymbiosis and a pinch of biochemical interactions

Authors

  • Johann P. Müller,

    Corresponding author
    1. UFR Sciences de la Vie, UPMC Univ Paris 06, Paris, France
    2. Laboratoire Bioemco, Ecole Normale Supérieure, Paris, France
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  • Céline Hauzy,

    1. IFM Theory and Modelling, Linköping University, Linköping, Sweden
    2. Université Pierre et Marie Curie, Sorbonne Universités, UMR 7625 Ecologie et Evolution, Paris, France
    3. INRA, USC 2031 Ecologie des Populations et Communautés, Paris, France
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  • Florence D. Hulot

    1. UFR Sciences de la Vie, UPMC Univ Paris 06, Paris, France
    2. Laboratoire d’Ecologie, Systématique & Evolution, UMR 8079, Univ Paris-Sud, Orsay, France
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Correspondence author. E-mail: jmuller@biologie.ens.fr

Summary

1. The interaction between mutualism, facilitation or interference and exploitation competition is of major interest as it may govern species coexistence. However, the interplay of these mechanisms has received little attention. This issue dates back to Gause, who experimentally explored competition using protists as a model [Gause, G.F. (1935) Vérifications expérimentales de la théorie mathématique de la lutte pour la vie. Actualités Scientifiques et Industrielles, 277]. He showed the coexistence of Paramecium caudatum with a potentially allelopathic species, Paramecium bursaria.

2.Paramecium bursaria hosts the green algae Chlorella vulgaris. Therefore, P. bursaria may benefit from carbohydrates synthesised by the algae. Studying endosymbiosis with P. bursaria is possible as it can be freed of its endosymbiont. In addition, C. vulgaris is known to produce allelochemicals, and P. bursaria may benefit also from allelopathic compounds.

3. We designed an experiment to separate the effects of resource exploitation, endosymbiosis and allelopathy and to assess their relative importance for the coexistence of P. bursaria with a competitor that exploits the same resource, bacteria. The experiment was repeated with two competitors, Colpidium striatum or Tetrahymena pyriformis.

4. Results show that the presence of the endosymbiont enables the coexistence of competitors, while its loss leads to competitive exclusion. These results are in agreement with predictions based on resource equilibrium density of monocultures (R*) supporting the idea that P. bursaria’s endosymbiont is a resource provider for its host. When P. bursaria and T. pyriformis coexist, the density of the latter shows large variation that match the effects of culture medium of P. bursaria. Our experiment suggests these effects are because of biochemicals produced in P. bursaria culture.

5. Our results expose the hidden diversity of mechanisms that underlie competitive interactions. They thus support Gauses’s speculation (1935) that allelopathic effects might have been involved in his competition experiments. We discuss how a species engaged both in competition for a resource and in costly interference such as allelopathy may counterbalance these costs with a resource-provider endosymbiont.

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