Different functional traits among closely related algal symbionts dictate stress endurance for vital Indo‐Pacific reef‐building corals

Abstract

Reef-building corals in the genus Porites are one of the most important constituents of Indo-Pacific reefs. Many species within this genus tolerate abnormally warm water and exhibit high specificity for particular kinds of endosymbiotic dinoflagellates that cope with thermal stress better than those living in other corals. Still, during extreme ocean heating, some Porites exhibit differences in their stress tolerance. While corals have different physiological qualities, it remains unknown whether the stability and performance of these mutualisms is influenced by the physiology and genetic relatedness of their symbionts. We investigated two ubiquitous Pacific reef corals, Porites rus and Porites cylindrica, from warmer inshore and cooler offshore reef systems in Palau. While these corals harbored a similar kind of symbiont in the genus Cladocopium (within the ITS2 C15 subclade), rapidly evolving genetic markers revealed evolutionarily diverged lineages corresponding to each Porites species living in each reef habitat. Furthermore, these closely related Cladocopium lineages were differentiated by their densities in host tissues, cell volume, chlorophyll concentration, gross photosynthesis, and photoprotective pathways. When assessed using several physiological proxies, these previously undifferentiated symbionts contrasted in their tolerance to thermal stress. Symbionts within P. cylindrica were relatively unaffected by exposure to 32℃ for 14 days, whereas P. rus colonies lost substantial numbers of photochemically compromised symbionts.Heating reduced the ability of the offshore symbiont associated with P. rus to translocate carbon to the coral. By contrast, high temperatures enhanced symbiont carbon assimilation and delivery to the coral skeleton of inshore P. cylindrica. This study indicates that large physiological differences exist even among closely related symbionts, with significant implications for thermal susceptibility among reef-building Porites.

Cophylogeny and specificity between cryptic coral species (Pocilloporaspp.) at Mo’orea and their symbionts (Symbiodiniaceae)

“…In the past, cophylogeny between corals and their algal symbionts was expected to be rare or absent (Van Oppen and Medina 2020) because many coral species exhibit horizontal transmission (Baird et al 2009), many algal symbiont species exhibit flexibility to associate with different hosts (LaJeunesse et al 2018), and even coral species with vertical transmission can have some degree of horizontal acquisition of symbionts (Quigley et al 2018, 2019). Other coral species, including members from Porites and Montipora , also exhibit vertical transmission and harbor host-specialist species of Cladocopium (Lajeunesse et al 2004; LaJeunesse and Thornhill 2011; Forsman et al 2020; Hoadley et al 2021), but the extent of cophylogeny within these groups remains to be tested. Members of the genus Cladocopium associate with a broad diversity of hosts in addition to corals, including other cnidarians, clams, ciliates, flatworms, foraminifera, and sponges, but can be highly host specialized (LaJeunesse et al 2018).…”

Variation in Coral Thermotolerance Across a Pollution Gradient Erodes as Coral Symbionts Shift to More Heat-Tolerant Genera

“…The qPCR method used in this study to distinguish between Symbiodiniciae genera cannot distinguish among different species of Cladocopium. Therefore, it is possible that we have captured multiple different Cladocopium species, some of which have been shown to promote higher thermotolerance (Hoadley et al, 2021). Also interestingly, even corals that hosted 100% Durusdinium varied in their thermotolerance, indicating that factors other than symbiont community can play a significant role in setting thermotolerance.…”

Building Consensus around the Assessment and Interpretation of Symbiodiniaceae Diversity

“…Budget and logistics permitting, it is recommended to use multiple markers in some situations. For some ITS2 lineages (e.g., Breviolum B1 or Cladocopium C15; Hoadley et al, 2021;Parkinson et al, 2015), available markers that behave as if single copy do not distinguish ecologically relevant variants, but universal primers have yet to be designed for gene regions that capture this variation (e.g., psbA ncr ). Therefore, a marker that behaves as if single copy can first be applied to determine the dominant Symbiodiniaceae genera present to assist in the selection of the correct primer set for a higher resolution marker.…”

“…For example, recent high-throughput approaches for assessing thermal tolerance at the whole coral level (e.g., coral bleaching automated stress systems (CBASS; Voolstra et al, 2020) and single cell levels (Behrendt et al, 2020) have incorporated short thermal challenges followed by stress characterization through the measurement of 1-2 physiological variables such as maximum PSII photochemical efficiency (Fv/Fm) and cell density. While single-phenotype assays can be informative within the context of ecosystem service values (e.g., identifying thermally tolerant corals for nursery propagation; Cunning et al, 2021), identification of functionally distinct Symbiodiniaceae phenotypes will benefit from measuring a broader spectrum of physiological metrics (Hoadley et al, 2021). Phenotypic characterization using multiple photosynthetic metrics can provide some species-specific resolution (Suggett et al, 2015), and the non-invasive nature of chlorophyll a fluorometry lends itself to high-throughput approaches.…”