An original mode of symbiosis in open ocean plankton

Abstract

International audienceSymbiotic 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

Diversity and abundance of haptophytes in the East China Sea

“…Until now, all of the sequences affiliated to P. jahnii and P. cordata have been retrieved from latitudes between 10 and 45°. A recent study on the phylogeny of the symbiotic relationship between Phaeocystis and Acantharia demonstrated that genetic distances of symbiont Phaeocystis were significantly correlated to its biogeography, but had no relationship with the host taxonomy (Decelle et al 2012). Overall, our results are consistent with previous studies showing that species of Phaeocystis occurring in polar and non-polar areas are distinct (Schoemann et al 2005, Decelle et al 2012.…”

“…A recent study on the phylogeny of the symbiotic relationship between Phaeocystis and Acantharia demonstrated that genetic distances of symbiont Phaeocystis were significantly correlated to its biogeography, but had no relationship with the host taxonomy (Decelle et al 2012). Overall, our results are consistent with previous studies showing that species of Phaeocystis occurring in polar and non-polar areas are distinct (Schoemann et al 2005, Decelle et al 2012. Few studies have reported blooms of P. jahnii and P. cordata, which may be due to their small size, or may indicate that they cannot form, or seldom form, colonies in the natural environment (Zingone et al 1999, Medlin & Zingone 2007.…”

“…3). A recent study reported that some Phaeocystis have a symbiotic relationship with Acantharia (Decelle et al 2012). The clone libraries from our samples were constructed from < 5 µm size fractions, which may have excluded Acantharia sequences.…”

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

“…Reads of genotype 2 also displayed negative correlations with some nutrients (NO 2 , PO 4 , Si), whereas those of genotype 1 had positive correlations with the depth of the deep chlorophyll maximum. Thus, the correlation patterns between the host, its symbiont and their abiotic environment clearly indicate that the symbiotic partnership predominantly occurs in oligotrophic conditions (typically characterized by deep chlorophyll maximum and low chlorophyll and nutrient concentrations), mirroring the ecology of other known planktonic photosymbioses (Shaked and de Vargas, 2006;Stoecker et al, 2009;Decelle et al, 2012). More specifically, we note that genotype 2 positively correlated with salinity, very likely because of its prevalence in the Mediterranean Sea.…”

“…Many hosts build mineral skeletons of calcium carbonate, silica or strontium sulfate, hence contributing to the biogeochemical cycles of these elements (Bernstein et al, 1987). For instance, the rhizarian Radiolaria and Foraminifera are known to develop obligate photosymbioses in surface waters with diverse eukaryotic microalgae, such as photosynthetic dinoflagellates (for example, Brandtodinium, Pelagodinium) and haptophytes (for example, Phaeocystis) (Gast and Caron, 2001;Shaked and de Vargas, 2006;Decelle et al, 2012;Probert et al, 2014). Some heterotrophic dinoflagellates have also been found to host prasinophyte (Sweeney, 1976) or pelagophyte (Daugbjerg et al, 2013) microalgae.…”