Bleaching of the Cnidarian-Dinoflagellate Symbiosis: Aspects of Innate Immunity and the Role of Nitric Oxide
Authors:   , Hawkins Thomas D. 
Published: November 2021

<p>Driven by global warming and the increasing frequency of high temperature anomalies, the collapse of the cnidarian-dinoflagellate symbiosis (known as "bleaching" due to the whitening of host tissues) is contributing to worldwide coral reef decline. Much is known about the consequences of bleaching, but despite over 20 years of effort, we still know little about the physiological mechanisms involved. This is particularly true when explaining the differential susceptibility of coral hosts and their algal partners (genus Symbiodinium) to rising temperatures.  Work carried out over the past 10 years suggests that bleaching may represent an innate immune-like host response to dysfunctional symbionts. This response involves the synthesis of nitric oxide (NO), a signalling molecule widely dispersed throughout the tree of life and implicated in diverse cellular phenomena. However, the source(s) of NO in the cnidarian-dinoflagellate association have been the subject of debate, and almost nothing is known of the capacity for differential NO synthesis among different host species or symbiont types.  The aim of this study was to elucidate the role of NO in the temperature-induced breakdown of the cnidarian-dinoflagellate symbiosis and to assess differences in NO-mediated physiology at the level of both symbiont and host. The specific objectives were (i) to quantify NO synthesis in different types of symbiotic dinoflagellates, (ii) to determine a role for NO in the collapse of the cnidarian-dinoflagellate symbiosis, (iii) to confirm whether NO itself - as opposed to its more reactive derivatives - is capable of mediating cnidarian bleaching, and (iv) to measure the synthesis of NO and the regulation of associated pathways in different reef corals undergoing bleaching.  This thesis demonstrates that both partners of the symbiosis have a capacity for synthesising NO when stimulated by elevated temperature. However, their contributions to NO synthesis in the intact symbiosis may not be equal, as heightened symbiont NO production invariably occurred after that of the host, and at a time when bleaching had already commenced. Closer examination of host-derived NO in the model anemone Aiptasia pulchella revealed that the compound most likely mediates bleaching through apoptotic-like cell death pathways, as either removing NO or inhibiting the activity of an important apoptosis-regulating enzyme could alleviate bleaching. NO's involvement in thermal bleaching also seems to be independent of its conversion to more toxic radicals such as peroxynitrite (ONOO-), which, although present at elevated temperature, had little influence on symbiont loss in A. pulchella. [...]  As is the case in a wide variety of animal-microbe interactions, NO appears to mediate the cnidarian-dinoflagellate symbiosis by influencing the activity of host apoptotic-like pathways. Interestingly, the activation of these host responses at elevated temperature may occur before the dinoflagellate becomes photosynthetically compromised. As such, the model of bleaching as simply a response to symbiont photoinhibition could require modification. Furthermore, the differential sensitivity of symbiont types to NO, coupled with the differential regulation of NO-synthetic and apoptotic pathways in the host, could contribute to corals' varying bleaching susceptibilities.  This thesis provides vital insights into the cell biology of the coral-dinoflagellate symbiosis and the events underpinning its breakdown during temperature stress. It also encourages a greater research emphasis on understanding physiological responses at the level of the coral host as well as during the early stages of a bleaching event.</p>