Heat-Stress and Light-Stress Induce Different Cellular Pathologies in the Symbiotic Dinoflagellate during Coral Bleaching

Abstract

Coral bleaching is a significant contributor to the worldwide degradation of coral reefs and is indicative of the termination of symbiosis between the coral host and its symbiotic algae (dinoflagellate; Symbiodinium sp. complex), usually by expulsion or xenophagy (symbiophagy) of its dinoflagellates. Herein, we provide evidence that during the earliest stages of environmentally induced bleaching, heat stress and light stress generate distinctly different pathomorphological changes in the chloroplasts, while a combined heat- and light-stress exposure induces both pathomorphologies; suggesting that these stressors act on the dinoflagellate by different mechanisms. Within the first 48 hours of a heat stress (32°C) under low-light conditions, heat stress induced decomposition of thylakoid structures before observation of extensive oxidative damage; thus it is the disorganization of the thylakoids that creates the conditions allowing photo-oxidative-stress. Conversely, during the first 48 hours of a light stress (2007 µmoles m−2 s−1 PAR) at 25°C, condensation or fusion of multiple thylakoid lamellae occurred coincidently with levels of oxidative damage products, implying that photo-oxidative stress causes the structural membrane damage within the chloroplasts. Exposure to combined heat- and light-stresses induced both pathomorphologies, confirming that these stressors acted on the dinoflagellate via different mechanisms. Within 72 hours of exposure to heat and/or light stresses, homeostatic processes (e.g., heat-shock protein and anti-oxidant enzyme response) were evident in the remaining intact dinoflagellates, regardless of the initiating stressor. Understanding the sequence of events during bleaching when triggered by different environmental stressors is important for predicting both severity and consequences of coral bleaching.

Differential coral bleaching—Contrasting the activity and response of enzymatic antioxidants in symbiotic partners under thermal stress

“…the applied heating rate in the experimental setup. Low heating rates profoundly delay the physiological response of the coral holobiont (Middlebrook et al, 2010) and the ramping rate of 1°C day -1 used in the current study is considerably slower than in previous studies of antioxidant responses under thermal stress; these applied heating rates ranging from near-instantaneous to 4°C hour -1 (Yakovleva et al, 2004;Richier et al, 2005;Higuchi et al, 2008;Yakovleva et al, 2009;Higuchi et al, 2012;Downs et al, 2013;T. Higuchi and I. Yakovleva, personal communication).…”

“…While our study does not provide any further insights into the wellknown synergistic effects of light and temperature on bleaching physiology (Lesser et al, 1990;Lesser and Farrell, 2004;Downs et al, 2013), because we did not actively manipulate irradiance, it is notable that Day 5 in our experiment had the lowest mean irradiance, highlighting that elevated temperature was the primary stressor to induce the bleaching cascade in this experiment. From an ecological perspective, mass bleaching events, affecting multiple species across latitudinal and depth gradients, are primarily driven by anomalies in temperature rather than light (McWilliams et al, 2005;Sammarco et al, 2006;Eakin et al, 2009).…”

Non-intrusive Assessment of Photosystem II and Photosystem I in Whole Coral Tissues

“…Recent works (Reynolds et al, 2008;Roberty et al, 2014;Aihara et al, 2016) have indicated the possibility that singlet oxygen production is generated when PQ pool is reduced, i.e., the relative size of oxidized PQ pool is smaller (and thus charge recombination in PSII reaction centers is promoted), which may be a primary factor in coral bleaching (Vass, 2012;Rehman et al, 2016). Nevertheless, these effects have to be documented individually in corals, where it is known that there are varied responses to similar acute thermal stress scenarios (Downs et al, 2013;Gardner et al, 2017). It is entirely possible that despite the "Achilles Heel" of a heat sensitive Rubisco, different Symbiodinium types have evolved different strategies to cope with this problem, and that the diversity of these strategies account for the different heat sensitivities of corals to coral bleaching.…”

Respuestas al estrés por calor en los cultivos. I. Aspectos moleculares, bioquímicos y siológicos.

“…En estudios detallados de los simbiontes dinoflagelados de los corales, la descomposición de la estructura de los tilacoides en las primeras 48 h a 32 °C, precedió la aparición de las ROS y la ocurrencia de daño oxidativo severo. Después de 72 h de exposición al calor, se observaron los procesos homeostáticos de síntesis de HSPs y de enzimas anti-oxidantes (Downs et al, 2013). La pérdida de electrolitos varía con la edad de los tejidos, el órgano, el estado de desarrollo y la especie.…”