Photosymbiosis in Marine Planktonic Protists

Abstract

Some of the most enigmatic components in the plankton are the diverse eukaryotic protists that live in close association with one or more partners. Mutualistic and commensal planktonic interactions are most commonly encountered in the oligotrophic open ocean at tropical and subtropical latitudes. They are functionally and ecologically distinct, and involve a great taxonomic diversity of single-celled partners. Protists like Foraminifera, Radiolaria, dinofl agellates and diatoms can all harbor microalgal symbionts of eukaryotic and prokaryotic origin inside (endosymbiosis) and/or outside (ectosymbiosis) their cytoplasm. Such symbioses (photosymbioses) combine phototrophy, heterotrophy and sometimes dinitrogen (N 2 ) fi xation (reduction of N 2 to ammonium). Symbiotic microorganisms therefore represent an important component of marine ecosystems and play a role in the food web and biogeochemical cycling (e.g., carbon and nitrogen). Despite their important ecological function and early recognition in the late nineteenth century, our knowledge about the diversity, distribution, and metabolic exchanges for many of the photosymbioses remains rudimentary compared with the other marine and terrestrial symbioses. Recent technical advances in single-cell genomics and imaging have greatly improved our understanding about planktonic symbioses. This review aims to present and compare many eukaryote-eukaryote and eukaryote-prokaryote photosymbioses described so far in the open ocean with an emphasis on their ecology and potential function in the ecosystem.

Biology and Ecology of Radiolaria

“…The main symbionts in Acantharia are identifi ed as belonging to the haptophyte genus Phaeocystis (Decelle et al 2012a(Decelle et al , 2015. Using genetic markers, no speciesspecifi c relationship could be revealed and any symbiotic acantharian species can take any Phaeocystis genera as a symbiont.…”

“…Except for colonial Collodaria, radiolarians consume preys by external assimilation of digested material in food vacuoles located in Besides heterotrophic feeding, a signifi cant number of radiolarian species inhabiting the photic zones of the oceans do bear symbiotic microalgae. A variety of associated photosynthetic organisms, including cyanobacteria, prasinophytes, haptophytes, and dinofl agellates have been reported to live in symbiosis with Radiolaria (Anderson 1993 ;Decelle et al 2015 ). The photosymbiont most commonly observed is the dinofl agellate genus Brandtodinium Fig.…”

“…The fate of these swarmers is unknown, and whether they are gametes or not is unclear. The small size of these swarmers together with the lack of chlorophyll fl uorescence demonstrates that symbiotic radiolarians very likely transmit their symbionts horizontally (e.g., de novo acquisition at each host generation, Decelle et al 2015 ).…”

Polymorphic adaptations in metazoans to establish and maintain photosymbioses

“…Photosymbiosis has evolved multiple times in the protist phyla Ciliophora, Foraminifera, Radiolaria, Dinoflagellata and diatoms (Decelle et al, ). Among these, Foraminifera and Radiolaria are skeleton‐building protists who establish photosymbiosis as primary producers of open ocean planktonic communities (Decelle et al, ). Photosymbiotic Foraminifera play a major ecological role contributing to the global carbon cycle and to 25% of carbonate calcium deposits (Langer, Silk & Lipps, ; Erez, ; Lipps & Stanley, ).…”

The symbiotic life ofSymbiodiniumin the open ocean within a new species of calcifying ciliate (Tiarinasp.)

“…Photosymbioses are also pervasive in planktonic ecosystems, especially in tropical and subtropical oligotrophic waters (Taylor, 1982;Stoecker et al, 2009;Decelle et al, 2015), but remain poorly studied compared with benthic ecosystems. Because of their mixotrophic capacity, photosymbiotic protists play a significant dual role as primary producers and predators in pelagic ecosystems (Swanberg and Caron, 1991;Michaels et al, 1995).…”