Single-Cell Transcriptome Profiling Reveals Mechanisms of Host-Control
and Nutrient Exchange in Acantharea-Phaeocystis Photosymbioses
Microbial eukaryotes (protists) are important contributors to marine
biogeochemistry and play essential roles as both producers and consumers
in marine ecosystems. Among protists, mixotrophs—those that use both
heterotrophy and autotrophy to satisfy their energy requirements—are
especially important to primary production in oligotrophic regions where
nutrient availability is otherwise limiting. For instance, acantharians
accomplish mixotrophy by hosting Phaeocystis spp. as endosymbionts.
Despite their ecological importance, Acantharea-Phaeocystis symbioses
are understudied due to host fragility and inability to survive in
culture. We investigated the evolution and ecological functioning of
these symbioses by sequencing single-cell transcriptomes from sixteen
acantharians. Since hosts harbor multiple Phaeocystis species, we
prepared transcriptomes for the two most common symbiont species
available in culture—P. cordata and P. jahnii—and evaluated
differential gene expression between symbiotic and free-living cells.
Results indicate photosynthesis genes are upregulated in symbiosis for
both symbiont species, suggesting symbionts are photosynthesizing at
elevated rates within hosts. However, biosynthesis and metabolism of
storage carbohydrates and lipids are downregulated in symbiosis,
indicating that extra energy captured through elevated photosynthesis is
not retained. Symbiont gene expression suggests symbionts relinquish
fixed carbon as small organonitrogen compounds, such as amides and amino
acids, while receiving host-supplied nitrogen as urea and ammonium.
Importantly, genes associated with protein kinase signaling pathways
that promote cell proliferation are deactivated in symbionts.
Manipulation of these pathways may prevent symbionts from overgrowing
hosts and therefore represents a key component of maintaining the
symbiosis. This study illuminates mechanisms of host control and
nutrient transfer in an important microbial symbiosis in oligotrophic