New perspectives on the functioning and evolution of photosymbiosis in plankton: Mutualism or parasitism?

Photosymbiosis is common and widely distributed in plankton and is considered to be beneficial for both partners (mutualism). Such intimate associations involving heterotrophic hosts and microalgal symbionts have been extensively studied in coral reefs, but in the planktonic realm, the ecology and evolution of photosymbioses remain poorly understood. Acantharia (Radiolaria) are ubiquitous and abundant heterotrophic marine protists, many of which host endosymbiotic microalgae. Two types of photosymbiosis involving acantharians have recently been described using molecular techniques: one found in a single acantharian species involving multiple microalgal partners (dinoflagellates and haptophytes), and the other observed in more than 25 acantharian species exclusively living with the haptophyte Phaeocystis. Contrary to most benthic and terrestrial mutualistic symbioses, these symbiotic associations share the common feature of involving symbionts that are abundant in their free-living stage. We propose a hypothetical framework that may explain this original mode of symbiosis, and discuss the ecological and evolutionary implications. We suggest that photosymbiosis in Acantharia, and probably in other planktonic hosts, may not be a mutualistic relationship but rather an “inverted parasitism,” from which only hosts seem to benefit by sequestrating and exploiting microalgal cells. The relatively small population size of microalgae in hospite would prevent reciprocal evolution that can select uncooperative symbionts, therefore making this horizontally-transmitted association stable over evolutionary time. The more we learn about the diversity of life and the structure of genomes, the more it appears that much of the evolution of biodiversity is about the manipulation of other species—to gain resources and, in turn, to avoid being manipulated (John Thompson, 1999).