Phylogenetic signature of light and thermal stress for the endosymbiotic dinoflagellates of corals (Family Symbiodiniaceae)

Abstract

Coral reefs around the world have been affected by a climate‐change induced phenomenon known as “coral bleaching,” which is caused by the interaction between high irradiance and elevated seawater temperatures, and involves the mass expulsion of Symbiodiniaceae from anemones, sponges, and corals. The primary drivers of this phenomenon are the inherent genetic variability in the Family Symbiodiniaceae, and the variability in the abiotic environment for variables such as irradiance and temperature. Recent experiments have either disregarded the important interactive role of irradiance or have suggested that photooxidative stress is not a prerequisite for coral bleaching because certain reactive oxygen species (ROS) can be produced in the dark. Here, fluorescent probes are used as proxies for the relative concentration of ROS in different genera of cultured Symbiodiniaceae under varying thermal and light conditions. The results show that taxon‐specific patterns of the concentration of ROS are observed but that all genera tested produced significantly greater amounts of superoxide radicals and hydrogen peroxide, compared to singlet oxygen, when exposed to high light and thermal stress. These results are contextualized in relation to the primary drivers of ROS production and the photo‐physiological basis for differences in ROS production that may then be correlated with symbiont driven coral bleaching.

Temperature transcends partner specificity in the symbiosis establishment of a cnidarian

“…Indeed, we observed a significantly higher abundance of variants associated with Symbiodinium (clade A), Cladocopium (clade C), and Durusdinium (clade D) taxa in anemones that were preexposed to 32°C, but also in heat stressed individuals (that is, Aiptasia reared at 25°C and subsequently subjected to 32°C). Symbiodinium species are known to be more resilient, with lower reactive oxygen species levels and slower deterioration of photosystem (PS) II compared to Breviolum, for example [41,[59][60][61][62]. Surprisingly, despite S. linucheae (A4) being supposedly the most thermally tolerant species tested here (according to [32]), it was barely observed at 32°C; only in few individuals from 25°C and for which it was already present in their initial ITS2 composition.…”

A New “Business as Usual” Climate Scenario and the Stress Response of the Caribbean Coral Montastraea cavernosa

“…Studies that have examined the resistance of corals to predicted changes in OW and OA have resulted in variable results reflecting the interand intraspecific phenotypic plasticity of corals and their Symbiodiniaceae symbionts (Hoadley et al, 2015;Bahr et al, 2016; Castillo et al, 2018;Cole et al, 2018;Davies et al, 2018). For Symbiodiniaceae, the diversity in phenotypic characters related to the stress response is significant (Díaz-Almeyda et al, 2018;Lesser, 2019), and recent studies, including those on M. cavernosa, have shown that "symbiont shuffling" to stresstolerant Symbiodiniaceae (i.e., Durusdinium trenchi [Phylotype D1a]) can occur after exposure to thermal stress (Silverstein et al, 2015(Silverstein et al, , 2017Cunning et al, 2018). The change to, or addition of, D. trenchi symbionts to the Symbiodiniaceae community potentially adds resistance to future thermal perturbation (Silverstein et al, 2015).…”

“…The change to, or addition of, D. trenchi symbionts to the Symbiodiniaceae community potentially adds resistance to future thermal perturbation (Silverstein et al, 2015). While some studies incorporating both long and short-exposures of corals to combined OW and OA conditions have revealed little effect of OA on gene expression or the functional diversity of their Symbiodiniaceae (Baghdasarian et al, 2017;Davies et al, 2018), other studies on the functional responses of corals in response to OW and OA have shown significant effects where OA lowers the thermal response threshold of the coral (e.g., Anthony et al, 2008) when using ecologically relevant irradiances (sensu Lesser, 2019).…”

“…Nonetheless, the production of ROS is inevitable, even in the absence of thermal stress, as it is directly related to pO 2 (Jamieson et al, 1986). As a result, the endosymbiotic Symbiodiniaceae contribute significant amounts of photogenerated O 2 − and H 2 O 2 (Lesser, 1996(Lesser, , 2019Suggett et al, 2008;Saragosti et al, 2010;McGinty et al, 2012), and both host cells (Perez and Weis, 2006) and Symbiodiniaceae also produce nitric oxide (NO • ) (Bouchard and Yamasaki, 2008). Nitric oxide synthase (NOS) activity in corals and sea anemones (Morrall et al, 2000;Trapido-Rosenthal et al, 2005) suggest that NO • production, and subsequently reactive RNS, including the highly reactive peroxynitrite radical (ONOO − ), are produced and are considered important contributors to redox stress and initiation of coral bleaching (Weis, 2008).…”

“…Most severe bleaching occurs in the first 15 m depth on a coral reef (e.g., Baird et al, 2018) where irradiances are high (e.g., Lesser, 2000) and experimental evidence has supported a significant, and interactive, role for solar radiation in the bleaching phenomenon (Lesser et al, 1990;Brown et al, 2002;Bhagooli and Hidaka, 2004;Lesser and Farrell, 2004;Lesser, 2010Lesser, , 2011a. Both the host and dinoflagellate symbionts respond by differential expression of stress genes that include heat shock proteins, enzymatic antioxidants, fluorescent proteins and regulators of apoptosis, autophagy or necrosis (Lesser and Farrell, 2004;Baird et al, 2009;Lesser, 2011a,b), or by switching to symbionts with increased organismal functionality (i.e., temperature compensated photophysiology) under environmental stress (Suggett et al, 2017;Lesser, 2019). One way to identify coral phenotypes resistant to environmental stress is to use molecular markers known to respond to multiple environmental stressors (Downs et al, 2000;Tchernov et al, 2004;Kenkel et al, 2011Kenkel et al, , 2014Jin et al, 2016;Louis et al, 2017).…”