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

Abstract

Mass coral bleaching due to thermal stress represents a major threat to the integrity and functioning of coral reefs. Thermal thresholds vary, however, between corals, partly as a result of the specific type of endosymbiotic dinoflagellate (Symbiodinium sp.) they harbour. The production of reactive oxygen species (ROS) in corals under thermal and light stress has been recognised as one mechanism that can lead to cellular damage and the loss of their symbiont population (Oxidative Theory of Coral Bleaching). Here, we compared the response of symbiont and host enzymatic antioxidants in the coral species Acropora millepora and Montipora digitata at 28°C and 33°C. A. millepora at 33°C showed a decrease in photochemical efficiency of photosystem II (PSII) and increase in maximum midday excitation pressure on PSII, with subsequent bleaching (declining photosynthetic pigment and symbiont density). M. digitata exhibited no bleaching response and photochemical changes in its symbionts were minor. The symbiont antioxidant enzymes superoxide dismutase, ascorbate peroxidase, and catalase peroxidase showed no significant upregulation to elevated temperatures in either coral, while only catalase was significantly elevated in both coral hosts at 33°C. Increased host catalase activity in the susceptible coral after 5 days at 33°C was independent of antioxidant responses in the symbiont and preceded significant declines in PSII photochemical efficiencies. This finding suggests a potential decoupling of host redox mechanisms from symbiont photophysiology and raises questions about the importance of symbiont-derived ROS in initiating coral bleaching.

Species-specific control of external superoxide levels by the coral holobiont during a natural bleaching event

“…Yet non- Symbiodinium sources of superoxide at the coral surface are also likely to contribute indirectly to external hydrogen peroxide concentrations, since the dismutation of superoxide produces hydrogen peroxide. Regardless of the ability of Symbiodinium to generate ROS within coral tissues, however, recent evidence has demonstrated a lack of correspondence between coral host and Symbiodinium redox metabolism during bleaching conditions, suggesting that Symbiodinium -derived ROS may not be the ultimate trigger of coral bleaching5354.…”

Elevated Temperature and Allelopathy Impact Coral Recruitment

“…Lipopeptides have been previously shown to induce ROS formation (and concomitant apoptosis) in mammalian cell lines [62,63]. It is probable that similar damage may be occurring in coral larvae when exposed to microcolin A [64]. If blooms of cyanobacteria increase in size and frequency with increased ocean temperatures as predicted [61,65,66], they could greatly increase sublethal stress and larval mortality during coral recruitment.…”

Warm-preconditioning protects against acute heat-induced respiratory dysfunction and delays bleaching in a symbiotic sea anemone

“…However, we observed no corresponding increases in host SOD activity, suggesting that (a) no O 2 − -driven oxidative challenge arose, and/or (b) constitutive SOD abundance was sufficiently protective. The first possibility raises questions about the fate of electrons transferred to CoQ, if not to generate O 2 − or H 2 O (the latter through CCO activity), while the second raises doubts about the implied necessity for superoxide accumulation to drive cnidarian bleaching (Lesser, 2006;Hawkins et al, 2015;Krueger et al, 2015;Agostini et al, 2016). Here, any excess O 2 − was probably consumed by other antioxidant systems, including the reduced CoQ pool (Ernster and Forsmark-Andrée, 1993;Jin et al, 2016).…”

“…Consequently, bleaching can occur via host and Symbiodinium cell necrosis (Dunn et al, 2004), apoptosis (Dunn et al, 2007;Tchernov et al, 2011; and/or host cell autophagy (Dunn et al, 2007;Downs et al, 2009). However, the roles of host and Symbiodinium in initiating the cellular bleaching cascade are being reconsidered (Ralph et al, 2001;Downs et al, 2009;Paxton et al, 2013;Krueger et al, 2015;Lutz et al, 2015). For example, recent work reported heat stress-induced host mitochondrial degradation independent of Symbiodinium dysfunction (Dunn et al, 2012;Lutz et al, 2015).…”