Heat stress destabilizes symbiotic nutrient cycling in corals

Abstract

Recurrent mass bleaching events are pushing coral reefs worldwide to the brink of ecological collapse. While the symptoms and consequences of this breakdown of the coral-algal symbiosis have been extensively characterized, our understanding of the underlying causes remains incomplete. Here, we investigated the nutrient fluxes and the physiological as well as molecular responses of the widespread coral Stylophora pistillata to heat stress prior to the onset of bleaching to identify processes involved in the breakdown of the coral-algal symbiosis. We show that altered nutrient cycling during heat stress is a primary driver of the functional breakdown of the symbiosis. Heat stress increased the metabolic energy demand of the coral host, which was compensated by the catabolic degradation of amino acids. The resulting shift from net uptake to release of ammonium by the coral holobiont subsequently promoted the growth of algal symbionts and retention of photosynthates. Together, these processes form a feedback loop that will gradually lead to the decoupling of carbon translocation from the symbiont to the host. Energy limitation and altered symbiotic nutrient cycling are thus key factors in the early heat stress response, directly contributing to the breakdown of the coral-algal symbiosis. Interpreting the stability of the coral holobiont in light of its metabolic interactions provides a missing link in our understanding of the environmental drivers of bleaching and may ultimately help uncover fundamental processes underpinning the functioning of endosymbioses in general.

Keywords: coral bleaching; endosymbiosis; metabolic interaction; resource competition; selfish symbiont.

Fig. 1.

State of the coral-algal symbiosis on day 10 of heat stress. (A–C) Corals showed no significant differences in algal symbiont densities or chlorophyll a content and no visual signs of bleaching. (D) Relative release of ROS from freshly isolated symbionts increased during heat stress and correlated with levels of oxidative stress (measured as lipid peroxidation) in the coral host tissue. Bars indicate the mean ± SE. The line displays best-fitting linear regression. The shaded area indicates the 95% confidence intervals. The R² value indicates the amount of variation explained by the linear regression.

Fig. 2.

Regulation of coral host and algal symbiont gene expression on day 10 of heat stress. (A–C) Mean gene expression of significantly differentially expressed key genes in the amino acid metabolism of the coral host. (D) Overview of how highlighted metabolic pathways of the coral host and algal symbiont may interact to alter nutrient cycling in the symbiosis. (E–G) Mean gene expression of significant differentially expressed nitrate (NO₃⁻) assimilation key genes of algal symbionts. Blue arrows indicate a significant down-regulation and red arrows indicate a significant up-regulation of gene expression during heat stress. Lines and error bars indicate mean ± SE. TPM = transcripts per million. For a complete list of differentially expressed genes as well as significant Gene Ontology terms see Dataset S1.

Fig. 3.

Symbiotic assimilation and fate of carbon and nitrogen on day 10 of heat stress. (A) Respiratory carbon consumption of the holobiont derived from oxygen fluxes. Pale bars indicate carbon demand fulfilled by gross photosynthetic production. (B) Assimilation of ¹³C-bicarbonate (H¹³CO₃⁻) into coral host and algal symbiont cells, respectively, based on NanoSIMS imaging (C and D). (E) Net ammonium (NH₄⁺) uptake from seawater by coral fragments. Negative values indicate a net release of NH₄⁺ from the holobiont. (F) Assimilation of ¹⁵NH₄⁺ into coral host and algal symbiont cells, respectively, derived from NanoSIMS imaging (G and H). (I) Net nitrate (NO₃⁻) uptake from seawater by coral fragments. (J) Assimilation of ¹⁵NO₃⁻ into coral host and algal symbiont cells derived from NanoSIMS imaging (K and L). Bars indicate mean ± SE. Asterisks indicated significant differences between treatments. (Scale bars in NanoSIMS images: 5 µm.)

Fig. 4.

Proportion of dividing algal symbiont cells on day 10 of heat stress. NanoSIMS images for ¹²C¹⁴N⁻ were used to quantify the abundance of (A) regular and (B) dividing algal symbiont cells in the coral tissue sections. (C) These data were used to calculate the proportion of dividing cells in the algal symbiont population. Note that this mitotic index likely reflects an underestimation of the true proportion of dividing cells due to the two-dimensional nature of NanoSIMS images. Bars indicate mean ± SE. Asterisks indicated significant differences between treatments. (Scale bars in NanoSIMS images, 5 µm.)

Fig. 5.

Model outlining the dynamic transition between a stable and unstable state of the coral–algal symbiosis based on metabolic interactions between the coral host and its algal symbionts. (A) This model posits that the nutritional status of host and symbionts is passively controlled by a positive and a negative feedback loop arising from the nutrient exchange between the host and its algal symbionts. (B) In a stable state, carbon (C) translocation by algal symbionts fulfils or exceeds the metabolic C demands of the coral host, thereby arresting the symbiosis in a nitrogen (N)-limited state (purple shaded area). Environmental stressors, such as rapid warming, may cause a proportional increase of host C requirements, resulting in a feedback loop imbalance in favor of the positive feedback loop that destabilizes C cycling in the symbiosis. This imbalance will first affect the coral host metabolism resulting in C limitation, while algal symbionts remain N-limited (pink shaded area). If conditions persist, eventually the entire symbiosis shifts towards a C-limited stage (yellow shaded area). Likewise, the rapid proliferation of algal symbionts during the (re)establishment of the symbiosis will accordingly result in a feedback loop imbalance in favor of the negative feedback loop that effectively increases competition for available N between algal symbionts. Thereby, the symbiosis gradually shifts towards an N-limited state in which C translocation and recycling are maximized.