Optimal nutrient exchange and immune responses operate in partner specificity in the cnidarian-dinoflagellate symbiosis

Abstract

The relationship between corals and dinoflagellates of the genus is fundamental to the functioning of coral ecosystems. It has been suggested that reef corals may adapt to climate change by changing their dominant symbiont type to a more thermally tolerant one, although the capacity for such a shift is potentially hindered by the compatibility of different host-symbiont pairings. Here we combined transcriptomic and metabolomic analyses to characterize the molecular, cellular, and physiological processes that underlie this compatibility, with a particular focus on, an opportunistic, thermally tolerant symbiont that flourishes in coral tissues after bleaching events. Symbiont-free individuals of the sea anemone (commonly referred to as Aiptasia), an established model system for the study of the cnidarian-dinoflagellate symbiosis, were colonized with the "normal" (homologous) symbiont and the heterologous Analysis of the host gene and metabolite expression profiles revealed that heterologous symbionts induced an expression pattern intermediate between the typical symbiotic state and the aposymbiotic state. Furthermore, integrated pathway analysis revealed that increased catabolism of fixed carbon stores, metabolic signaling, and immune processes occurred in response to the heterologous symbiont type. Our data suggest that both nutritional provisioning and the immune response induced by the foreign "invader" are important factors in determining the capacity of corals to adapt to climate change through the establishment of novel symbioses.

Role of host genetics and heat‐tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming

“…On the other hand, D. trenchii is associated with depressed calcification that could impact reef accretion (Pettay et al, 2015), as well as altered metabolic and immune activity indicative of suboptimal symbiosis in heterologous hosts (Matthews et al, 2017). Long-term monitoring data at one of the inshore sites sampled here (UKI1, Cheeca Rocks) revealed significantly less bleaching in 2015 versus 2014 despite the fact that 2015 was hotter (Gintert et al, 2018).…”

“…On one hand, colonies dominated by D. trenchii are able to tolerate temperatures 1–2°C warmer than conspecifics hosting other symbiont types, and corals that become dominated by D. trenchii due to a bleaching event do gain increased heat tolerance (Silverstein, Cunning, & Baker, ). On the other hand, D. trenchii is associated with depressed calcification that could impact reef accretion (Pettay et al., ), as well as altered metabolic and immune activity indicative of suboptimal symbiosis in heterologous hosts (Matthews et al., ). Long‐term monitoring data at one of the inshore sites sampled here (UKI1, Cheeca Rocks) revealed significantly less bleaching in 2015 versus 2014 despite the fact that 2015 was hotter (Gintert et al., ).…”

Revealing changes in the microbiome of Symbiodiniaceae under thermal stress

“…) – of course whether this reflects a response of the bacteria to changing health of (and resource provision by) the Symbiodiniaceae, versus a fundamental change in Symbiodiniaceae fitness as a result of heat stress impacts on the bacteria community, or even an independent temperature effect on both, cannot be resolved from this observation alone. In the case of Symbiodiniaceae and their associated bacteria, resolving ‘who influences who’ is extremely important given that both can potentially influence the emergent properties of cultures, for example, reactive oxygen production and quenching (Vardi et al ., ; Goyen et al ., ), nutrient availability (Croft et al ., ; Suggett et al ., ) and metabolite production (Matthews et al ., ; ). Even so, understanding how Symbiodiniaceae associated bacterial communities change with thermal stress is the first step in uncoupling their functional relationship.…”

The past, present, and future of coral heat stress studies

“…A growing understanding of the metabolic hostsymbiont relationship has encouraged the use of methods that allow the measuring of these dynamics, such as metabolomics (Cui et al, 2019;Matthews et al, 2017) or NanoSIMS (Krueger et al, 2018). Recent studies have increasingly been combining coral and Symbiodiniaceae responses in their hypothesis testing.…”