Photosynthetic Endosymbionts Benefit from Host's Phagotrophy, Including Predation on Potential Competitors

In many endosymbioses, hosts have been shown to benefit from symbiosis, but it remains unclear whether intracellular endosymbionts benefit from their association with hosts [1, 2]. This makes it difficult to determine evolutionary mechanisms underlying cooperative behaviors between hosts and intracellular endosymbionts, such as mutual exchange of vital resources. Here, we investigate the fitness effects of symbiosis on the ciliate host Paramecium bursaria and on the algal endosymbiont Chlorella [3, 4], using experimental microcosms that include the free-living alga Chlamydomonas reinhardtii to mimic ecologically realistic conditions. We demonstrate that both host ciliate and the endosymbiotic algae gain fitness benefits from the symbiosis when another alga C. reinhardtii is present in the system. Specifically, the endosymbiotic Chlorella can grow as the host ciliate feeds and grows on C. reinhardtii, whereas the growth of free-living Chlorella is reduced by its competitor, C. reinhardtii. Thus, we propose that the endosymbiotic algae benefit from the host's phagotrophy, which allows the endosymbiont to access particulate nutrient sources and to indirectly prey on the potential competitors competing with its free-living counterparts. Even though the ecological contexts in which each partner receives its benefits differ, both partners would gain net fitness benefits in an ecological timescale. Thus, the cooperative behaviors can evolve through fitness feedback (partner fidelity feedback) between the host and the endosymbiont, without need for special partner control mechanisms. The proposed ecological and evolutionary mechanisms provide a basis for understanding cooperative resource exchanges in endosymbioses, including many photosynthetic endosymbioses widespread in aquatic ecosystems.