Short-Term Thermal Acclimation Modifies the Metabolic Condition of the Coral Holobiont

Abstract

The nutritional symbiosis between coral hosts and photosynthetic dinoflagellates is fundamental to the functioning of coral reefs. Rising seawater temperatures destabilize this relationship, resulting in drastic declines in world-wide coral cover. Thermal history is thought to play an important role in shaping a coral's response to subsequent thermal stress. Here, we exposed Pocillopora damicornis to two thermal acclimation regimes (ambient vs. warm) and compared the effect that acclimation had on the coral holobiont's response to a subsequent seven day heat stress event. We conducted daily physiological measurements at the holobiont level (gross photosynthesis, respiration, host protein content, symbiont density and chlorophyll content) throughout the heating event, as well as cellular-level imaging of 13 C-bicarbonate and 15 N-nitrate assimilation (using NanoSIMS) at the end of the heat stress event. Thermal acclimation history had a negligible effect on the measurements conducted at the holobiont level during the heat stress event. No differences were observed in the O 2 -budget between ambient and warm-acclimated corals and only small fluctuations in host protein, symbiont density and chlorophyll content were detected. In contrast, this lack of differential response, was not mirrored at the cellular level. Warm-acclimated corals had substantially higher 13 C enrichment in the host gastrodermis and lipid bodies, but significantly lower 15 N-nitrate assimilation in the symbionts and the host tissue layers, relative to the ambient-acclimated corals. We discuss potential reasons for the disconnect that occurred between symbiont bicarbonate and nitrate assimilation (in the absence of photosynthetic breakdown) in the warm-acclimated corals. We suggest this represents either a shift in nitrogen utilization, or supply limitation by the host. Our findings raise several interesting hypotheses regarding the role that nitrogen metabolism plays in thermal stress, which will warrant further investigation if we are to understand the acclimatization capacity of the coral holobiont.

A method to disentangle and quantify host anabolic turnover in photosymbiotic holobionts with subcellular resolution

“…Labelling patterns produced by [1-13 C]-pyruvate. When photosynthesis was active, [1-13 C]-pyruvate produced 13 C-labelling patterns qualitatively similar to those previously observed in corals exposed to 13 C-labelled bicarbonate in seawater, with preferential accumulation in the pyrenoid and starch granules of the dinoflagellates, and translocated 13 C-labelled lipids in the coral host tissue 10,13,15 (Fig. 1a).…”

“…In organisms hosting photosynthesizing symbionts, both the 13 CO 2 produced as a by-product of the formation of the Acetyl-CoA complex (C-position 1) and during the TCA cycle (C-positions 2 and 3) can be assimilated by the symbionts. Photosynthates that are labelled in 13 C and translocated back to the host tissue then make it impossible to obtain a measure of pure host-cell anabolic turnover. This problem of photosynthate translocation can be avoided either by conducting experiments in the dark and/or by blocking photosynthesis, rendering it impossible for translocated photosynthates to contribute to 13 Cenrichment in the host tissue.…”

“…To date, it has not been possible to investigate the anabolic performance of the coral host tissue without the translocation of photosynthates from the symbiont algae population. Here we demonstrate this capability using pyruvate-labelled with 13 C in specific C-positions within the molecule. This method is not only applicable to corals, but can be used to study a wide range of organisms that host photosynthesizing symbionts: e.g., bivalves, gastropods, jellyfish, sea anemones, hydrozoans, soft corals, foraminifera, sponges, and worms.…”

“…Corals are meta-organisms (so-called holobionts 6 ) that host a dynamic population of bacteria, archaea, viruses and photosynthetic dinoflagellate algae (family: Symbiodiniaceae) 7 . The flux of metabolites between the host and its symbionts has been the subject of numerous studies using stable isotope labelling combined with either bulk tissue analyses 8,9 or correlative imaging [10][11][12][13][14][15] . However, these previous studies have generally focused on the photosynthetic performance of the algae and the metabolic interactions between host and symbiont population.…”

Trophic ecology of shallow and deep reef-building corals

“…Reduced nitrate assimilation by the host and symbionts has been observed in thermally acclimated corals, which may represent nitrogen limitation by the host or a change in nitrogen cycling (Gibbin et al 2018). Nitrogen limitation is capable of inducing lipid synthesis in symbionts (Weng et al 2014), and increased C:N of symbionts from all three species could be due to increased lipid synthesis, nitrogen limitation, or both (Table 3.1).…”