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.

A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity

“…Globally, we detected in our scRNA-seq dataset a similar number of genes (31,425) to those seen in S . pistillata bulk RNA-seq studies (30,821) ( Liew et al, 2018 ; Rädecker et al, 2021 ; Figure S1K ), and the aggregated scRNA-seq gene expression levels correlated well with levels measured bulk RNA-seq analyses (Rs = 0.803) ( Figure S1L ).…”

“…For comparison of single-cell RNA-seq versus bulk RNA-seq data, we re-mapped reads from two studies ( Liew et al, 2018 ; Rädecker et al, 2021 ) using the same STAR parameters used to map scRNA-seq reads and we used STAR gene count estimates with the same gene intervals defined for our scRNA-seq analysis for compatibility in the comparison.…”

Marine heatwaves depress metabolic activity and impair cellular acid–base homeostasis in reef‐building corals regardless of bleaching susceptibility

“…Understanding the diversity of coral heat stress responses both within and between species is critical for predicting future coral performance in a changing ocean. While coral bleaching is a dramatic and easily observable heat stress response (Bollati et al, 2020; Putnam et al, 2017), elevated temperatures can also trigger less visible stress responses in the animal host, even if the symbiosis remains intact (Rädecker et al, 2021). All animals have a range of temperatures to which they are adapted, and once exposed to temperatures beyond this optimal range, can activate a suite of heat stress responses and divert energetic investment toward maintenance processes like homeostasis, at the expense of other more immediately expendable processes such as growth and reproduction (Pörtner, 2008).…”

Flexibility in Red Sea Tridacna maxima‐Symbiodiniaceae associations supports environmental niche adaptation

“…Importantly, the physiology of the algal symbionts may modulate the phenotype of their marine invertebrate hosts (Cunning et al, 2015;Howells et al, 2020;Rädecker et al, 2015;Rädecker et al, 2021;Silverstein et al, 2015;Terraneo et al, 2019). As an example, many Durusdinium taxa appear to be relatively stress-tolerant (LaJeunesse et al, 2014), for example, to warm and cold temperature-induced bleaching (Silverstein et al, 2017), and certain specialist Cladocopium taxa are found in the hottest coral-containing waters on Earth (Hume et al, 2016).…”