Host starvation andin hospitedegradation of algal symbionts shape the heat stress response of theCassiopea-Symbiodiniaceae symbiosis

Abstract

Global warming is causing large-scale disruption of cnidarian-Symbiodiniaceae symbioses fundamental to major marine ecosystems, such as coral reefs. However, the mechanisms by which heat stress perturbs these symbiotic partnerships remain poorly understood. In this context, the upside-down jellyfishCassiopeahas emerged as a powerful experimental model system. We combined a controlled heat stress experiment with isotope labeling and correlative SEM-NanoSIMS imaging to show that host starvation is a central component in the chain of events that ultimately leads to the collapse of theCassiopeaholobiont. Heat stress caused an increase in catabolic activity and a depletion of carbon reserves in the unfed host, concurrent with a reduction in the supply of photosynthates from its algal symbionts. This state of host starvation was accompanied by pronouncedin hospitedegradation of algal symbionts, which may be a distinct feature of the heat stress response ofCassiopeaInterestingly, this loss of symbionts by degradation was to a large extent concealed by body shrinkage of the starving animals, resulting in what could be referred to as 'invisible' bleaching. Overall, our study highlights the importance of the nutritional status in the heat stress response of theCassiopeaholobiont. Compared with other symbiotic cnidarians, the large mesoglea ofCassiopea, with its structural sugar and protein content, may constitute an energy reservoir capable of delaying starvation. It seems plausible that this anatomical feature at least partly contributes to the relatively high stress tolerance of these animals in our warming oceans.

Light exposure induces phenotypic plasticity of the upside-down jellyfishCassiopeaand its endosymbiotic dinoflagellates

“…Despite relative stability, medusa size is still considered a strong indicator of environmental conditions. For example, populations of smaller medusae after long periods of elevated water temperatures can indicate ‘invisible bleaching’ where jellyfish shrink, as a result of the loss of endosymbiotic Symbiodiniaceae (Morejón-Arrojo et al, 2024; Toullec et al, 2023).…”

“…In our experiment, we show that growth is affected by the light (and covarying water temperature), as evident by the significantly larger medusae observed under ambient light conditions (Figure 3B). Given the 'invisible bleaching' hypothesis of (Toullec et al, 2023)), if Cassiopea sp. individuals were heat stressed in our experiment, we would expect medusae to shrink.…”

Blue appendages and temperature acclimation increase survival during acute heat stress in the upside-down jellyfish,Cassiopea xamachana

“…Among marine cnidarians, Cassiopea appears to be uniquely capable of thriving in a range of environmental conditions (Purcell, 2012; Toullec et al, 2023). Specifically, C. andromeda exhibits exceptional tolerance to repeated, intense (26 – 34 °C) heat stress episodes (Banha et al, 2020; Béziat & Kunzmann, 2022).…”