Symbiodinium photosymbiosis in the open ocean

Symbiosis is central to the ecology of many ecosystems. The close relationship that occurs with a photosynthetic partner is defined as photosymbiosis, which has led to many eukaryotic lineages acquiring transient and even sometimes permanent photosynthesis. This type of symbiosis is common in both marine and freshwater ecosystems and it understood to be mutualistic. Symbiodinium is known to be one of the most common photosynthetic symbiont in marine environments. The genus Symbiodinium is genetically diverse and has evolved into nine different clades (A to I), which all have distinct physiological capacities, spatial distribution and host spectra. Despite several photosynthetic dinoflagellate taxa being identified as common symbionts in oceanic plankton, to date Symbiodinium, which is a common symbiont is coastal waters, has not been found in symbiosis in pelagic plankton. Ciliates are known to acquire phototrophy through photosymbiosis with eukaryotic or prokaryotic microalgal cells, benthic ciliates Maristentor dinoferus and Euplotes uncinatus host Symbiodinium endosymbionts in coral reefs and some Oligotrichida ciliates associate with prasinophytes in estuarine environments. Photosymbiotic ciliates have been found almost exclusive in coastal or benthic habitats. This study used a combination of microscopy and molecular tools to characterize a novel pelagic photosymbiosis between a calcifying ciliate host and Symbiodinium endosymbionts. By using the worldwide Tara Oceans expedition samples and metabarcoding data set allowed for the study of global specificity, biogeography and ecology.

Consistent microscopy observations on multiple specimens, systematic PCR detection of Symbiodinium within the ciliate and the geographic distribution in surface oceans together provide evidence in favour of a long-term mutualistic symbiosis. The study identified and characterised a novel widespread photosymbiosis between the dinoflagellate Symbiodinium and an undescribed calcifying ciliate. This newly described relationship is relevant not only because the host is previously unknown, but also because the occurrence of Symbiodinium as a pelagic symbiont was unknown, despite it being one of the most extensively studied microalgal genera. Within Symbiodinium clade A it was revealed that 8 subclade types are endemic to pelagic waters as they have not previously been reported in benthic coastal habitats. The selective pressures within the pelagic realm have generated these host specializations and may have created distinct ecological niches as well as the diversification of Symbiodinium.  This symbiosis likely plays many biogeochemical roles in pelagic ecosystems through contribution to primary productivity and calcium cycling. As the cilia-bearing host has the ability to actively move through the environment, unlike the ‘passive’ photosymbiotic rhizarian Radiolaria and Foraminifera, may indicate a chemotactic behaviour for finding symbiotic partners, suitable light conditions, and food or nutrient patches. The benefits to Tiarina sp. can be understood through the metabolic capacities of Symbiodinium in reef ecosystems, these likely include the benefits of a significant source of carbon, nitrogen, phosphate and other key nutrients for growth which would have otherwise been limited in the open ocean. Another benefit may also be the possibility that Symbiodinium plays a crucial role in the calcification of the ciliate’s skeleton (similar to scleractinian corals) and in protection from ultraviolet radiation. Clade A has been known to produce a significant amount of UV-absorbing amino acids which explains why it would be the clade that is represented in the transparent open ocean waters.

Future studies should aim to add to the understanding the nature, ecological role and life cycle of this novel photosymbiosis, and explore the possibility that other Symbiodinium clades can be found in the open ocean. Also in future automatic and in situ imaging techniques could be used to properly quantify this interaction, thus determining its ecological impact to the environment.

Reviewed Paper: Mordret, S., Romac, S., Henry, N., Colin, S., Carmichael, M., Berney, C., Audic, S., Richter, D., Pochon, X., de Vargas, C. and Decelle, J. (2015). The symbiotic life of Symbiodinium in the open ocean within a new species of calcifying ciliate (Tiarina sp.). The ISME Journal, 10(6), pp.1424-1436.