Proteomic Basis of Symbiosis: A Heterologous Partner Fails to Duplicate Homologous Colonization in a Novel Cnidarian– Symbiodiniaceae Mutualism

Abstract

Reef corals and sea anemones form symbioses with unicellular symbiotic dinoflagellates. The molecular circumventions that underlie the successful intracellular colonization of hosts by symbionts are still largely unknown. We conducted proteomic analyses to determine molecular differences of Exaiptasia pallida anemones colonized by physiologically different symbiont species, in comparison with symbiont-free (aposymbiotic) anemones. We compared one homologous species, Symbiodinium linucheae , that is natively associated with the clonal Exaiptasia strain (CC7) to another heterologous species, Durusdinium trenchii , a thermally tolerant species that colonizes numerous coral species. This approach allowed the discovery of a core set of host genes that are differentially regulated as a function of symbiosis regardless of symbiont species. The findings revealed that symbiont colonization at higher densities requires circumvention of the host cellular immunological response, enhancement of ammonium regulation, and suppression of phagocytosis after a host cell in colonized. Furthermore, the heterologous symbionts failed to duplicate the same level of homologous colonization within the host, evidenced by substantially lower symbiont densities. This reduced colonization of D. trenchii correlated with its inability to circumvent key host systems including autophagy-suppressing modulators, cytoskeletal alteration, and isomerase activity. The larger capability of host molecular circumvention by homologous symbionts could be the result of a longer evolutionary history of host/symbiont interactions, which translates into a more finely tuned symbiosis. These findings are of great importance within the context of the response of reef corals to climate change since it has been suggested that coral may acclimatize to ocean warming by changing their dominant symbiont species.

Host Genotypic Effect on Algal Symbiosis Establishment in the Coral Model, the Anemone Exaiptasia diaphana, From the Great Barrier Reef

“…B. minutum density increased further over time, reaching a maximum of 127 ± 2 cells/mm 2 at 30 dpi. These results are congruent with our identification of B. minutum as the homologous symbiont in GBR anemones and are consistent with previous works showing that the homologous symbiont is the most efficient colonizer of other E. diaphana genotypes (Belda-Baillie et al, 2002;Xiang et al, 2013;Gabay et al, 2018Gabay et al, , 2019Parkinson et al, 2018;Medranos et al, 2019;Sproles et al, 2019). Such an affinity profile is not exclusive to anemones, as it has also been reported in several corals (Weis et al, 2001;Rodriguez-Lanetty et al, 2003, 2004Wolfowicz et al, 2016;Lin et al, 2019).…”

“…It is common for E. diaphana to have affinities for heterologous symbionts ( Table 1). For instance, anemone genotype CC7 exhibits high compatibility for the homologous algae of E. diaphana from other regions (Hambleton et al, 2014;Wolfowicz et al, 2016), and the genetic lines of anemones from both Atlantic and Indo-Pacific regions are able to establish symbiosis with members of the Durusdinium genus (Wolfowicz et al, 2016;Gabay et al, 2018;Medranos et al, 2019;Sproles et al, 2019). This matrix of compatibility/incompatibility between hosts and symbionts probably represents an underlying system of genetic match-ups that regulates which partnerships occur in any given region, but the underlying cellular mechanisms are completely unknown.…”

Free‐living and symbiotic lifestyles of a thermotolerant coral endosymbiont display profoundly distinct transcriptomes under both stable and heat stress conditions

“…Whereas multiple investigations have queried the cnidarian host to compare conditions of symbiosis and aposymbiosis (e.g., Kuo, Chen, Lin, & Fang, 2004;Lehnert et al, 2014;Medrano, Merselis, Bellantuono, & Rodriguez-Lanetty, 2019;Oakley et al, 2016;Rodriguez-Lanetty, Phillips, & Weis, 2006), there has been limited inquiry into the changes which take place in Symbiodiniaceae when free-living dinoflagellates switch to an in hospite, endosymbiotic lifestyle. Previous work has included gel-based protein profiling of changes between in hospite and cultured Symbiodiniaceae (Pasaribu et al, 2015;Stochaj & Grossman, 1997).…”

Omics Analysis for Dinoflagellates Biology Research

“…Surprisingly, the expression levels of proteins related to antioxidant or heat stress phenotypes were roughly the same, while proteins involved in protein biosynthesis were highly expressed. Proteomics has also been used to compare the performance of different Symbiodiniaceae species [144,152]. Using LC-MS based proteomics, they compared proteomes of the model sea anemone Exaiptasia pallida colonized by different dinoflagellate symbiont ( B. minutum and Durusdinium trenchii ) [144].…”

“…Results showed that in anemones containing D. trenchii (heterologous symbiont), Niemann-Pick C2 proteins, and glutamine synthetases were lowly expressed, while methionine-synthesizing betaine–homocysteine S-methyltransferases and proteins with predicted oxidative stress response functions were highly expressed when compared with anemones containing B. minutum (homologous symbiont). In another study, the researchers found that high-density symbiotic colonization required avoiding the immune responses of host cells, enhancing ammonium regulation, and inhibiting the phagocytosis of host cells after colonization [152]. iv) Proteins related to toxin biosynthesis were identified in A .…”