Correspondence
Evelyn Abbott, Department of Integrative Biology, University of Texas at Austin, Austin, TX, USA
Email: evelyn.abbott@utexas.edu
Abstract
In recent years, as sea surface temperature increases, many coral species that used to harbor symbionts of the genus Cladocopiumhave 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 symbionts’ 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.
Introduction
Reef building corals get up to 90% of their energetic requirements for growth and calcification through symbiosis with dinoflagellate algae of the family Symbiodiniaceae (Falkowski et al. 1984). Coral bleaching is the breakdown of this symbiosis, and often occurs when water temperatures exceed a certain threshold. This heat tolerance threshold varies more depending on the genus of symbiont than on the host genetics (Fuller et al., 2020). These symbionts, formerly delineated as clades A-I, have now been divided into six genera (Lajeunesse et al., 2018). In the Great Barrier Reef, the majority of scleractinian corals of the genus Acropora have historically engaged in symbiosis with symbionts of the genus Cladocopium . However, as ocean temperatures continue to rise and bleaching events become more frequent, these corals are becoming colonized by relatively opportunistic, thermotolerant symbionts of the genus Durusdinium .
Symbionts are known to have diverse effects on their coral hosts. Although Durusdinium symbionts confer bleaching resistance, it comes at the cost of reduced growth (Pettay et al., 2015). Other physiological trade-offs have been observed, including reduced fecundity, reduced carbon acquisition (Matthews et al., 2018), reduced calcification (Pettay et al., 2015), and disease susceptibility (Shore-Maggio et al., 2018). Furthermore, it was found that in the Caribbean coral Montastraea cavernosa, Durusdinium dominance is associated with differential expression of stress-related genes in the host: havingDurusdinium appears to stress the host (Cunning et al., 2020).
Most corals only associate with a single symbiont type at a time, with background levels of other symbionts present in host tissues (Baker, 2003). In the case of acroporid corals from the Great Barrier Reef, hosts may harbor Cladocopium symbionts with background levels ofDurusdiunium , or the reverse, although some colonies have been shown to have a more even mixture (Ulstrup et al., 2003). Whether these two symbiont genera interact in the host tissues is presently unknown. Furthermore, as colonization of acroporid corals by Durusdinium becomes more common, it is unknown how harboring two distinct symbiont genera at once impacts both the symbionts and the host.
In this study, we analysed existing gene expression data from two studies with a combined total of 181 Acropora hyacinthus samples (Rose et al., 2015;Barshis et al., 2013). These indo-pacific corals had entirelyCladocopium, entirely Durusdinium , or a mixture of both symbionts. We asked how symbionts respond to symbionts of a different genus within the same host. Initially, we predicted that symbionts would have the most distinct expression patterns depending on whether they are the majority or the minority within the host. We also anticipated that the stress of competition would cause the symbionts to become more virulent towards the host, prioritizing their own proliferation by sequestering more nutrients and translocating fewer photosynthates to the host (Lesser et al., 2013;Baker et al., 2018;Morris et al., 2019). Therefore, we expected that corals hosting mixed symbiont populations would be more susceptible to heat stress and might show elevated expression of generalized stress response genes (Dixon et al., 2020) even under non-stressful temperature. We were surprised to find no support for any of these predictions.
Materials and Methods