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