An original mode of symbiosis in open ocean plankton

Abstract

Symbiotic relationships are widespread in nature and are fundamental for ecosystem functioning and the evolution of biodiversity. In marine environments, photosymbiosis with microalgae is best known for sustaining benthic coral reef ecosystems. Despite the importance of oceanic microbiota in global ecology and biogeochemical cycles, symbioses are poorly characterized in open ocean plankton. Here, we describe a widespread symbiotic association between Acantharia biomineralizing microorganisms that are abundant grazers in plankton communities, and members of the haptophyte genus Phaeocystis that are cosmopolitan bloom-forming microalgae. Cophylogenetic analyses demonstrate that symbiont biogeography, rather than host taxonomy, is the main determinant of the association. Molecular dating places the origin of this photosymbiosis in the Jurassic (ca. 175 Mya), a period of accentuated marine oligotrophy. Measurements of intracellular dimethylated sulfur indicate that the host likely profits from antioxidant protection provided by the symbionts as an adaptation to life in transparent oligotrophic surface waters. In contrast to terrestrial and marine symbioses characterized to date, the symbiont reported in this association is extremely abundant and ecologically active in its free-living phase. In the vast and barren open ocean, partnership with photosymbionts that have extensive free-living populations is likely an advantageous strategy for hosts that rely on such interactions. Discovery of the Acantharia–Phaeocystis association contrasts with the widely held view that symbionts are specialized organisms that are rare and ecologically passive outside the host