Codominance of two symbiont genera within the same coral host is associated with elevated symbiont productivity and lower host susceptibility to thermal stress

Abstract

In recent years, as sea surface temperature increases, many coral species that used to harbor symbionts of the genus Cladocopium have become colonized with the thermally tolerant genus, Durusdinium. Here, we asked how the symbionts of one genus react to the presence of another symbiont genus within the same coral host, and what effect this interaction has on the host. We used previously published transcriptomic data from Acropora hyacinthus corals hosting Cladocopium and/or Durusdinium symbionts and looked at gene expression in all three symbiotic partners depending on the relative proportion of the two symbiont genera within the same host. We find that both Cladocopium and Durusdinium change their expression the most when their proportions within the host are nearly equal (the state that we call "codominance"): both genera elevate expression of photosynthesis and ribosomal genes, suggesting increase in photosynthesis and growth (i.e. higher productivity). At the same time, the coral host also elevates production of ribosomes suggesting faster cellular growth, and, when heated, shows less pronounced stress response. These results can be explained in two alternative ways. One explanation is that increased competition between codominant symbionts switches them to the higher productivity mode, which benefits the host, making it more resilient to stress. Alternatively, the symbionts elevated productivity might be not the cause but the consequence of the host being particularly healthy. Under this explanation, rapid growth of the healthy host creates new space, lowering the symbioints competition and thus promoting their growth, which allows for codominance to happen where one genus would otherwise outcompete another. The latter explanation is supported by the fact that codominance is associated with lower symbiont densities, assessed as relative proportions of symbiont reads in the data. Irrespective of the causation direction, the presence of mixed symbiont communities could potentially be used as an instant indicator of coral well-being, which would be a useful tool for coral conservation and restoration.