Differential antioxidant response between two Symbiodinium species from contrasting environments

Abstract

High sea surface temperature accompanied by high levels of solar irradiance is responsible for the disruption of the symbiosis between cnidarians and their symbiotic dinoflagellates from the genus Symbiodinium. This phenomenon, known as coral bleaching, is one of the major threats affecting coral reefs around the world. Because an important molecular trigger to bleaching appears related to the production of reactive oxygen species (ROS), it is critical to understand the function of the antioxidant network of Symbiodinium species. In this study we investigated the response of two Symbiodinium species, from contrasting environments, to a chemically induced oxidative stress. ROS produced during this oxidative burst reduced photosynthesis by 30 to 50% and significantly decreased the activity of superoxide dismutase. Lipid peroxidation levels and carotenoid concentrations, especially diatoxanthin, confirm that these molecules act as antioxidants and contribute to the stabilization of membrane lipids. The comparative analysis between the two Symbiodinium species allowed us to highlight that Symbiodinium sp. clade A temperate was more tolerant to oxidative stress than the tropical S. kawagutii clade F. These differences are very likely a consequence of adaptation to their natural environment, with the temperate species experiencing conditions of temperature and irradiance much more variable and extreme.

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

“…In contrast, the results reported here ( Fig. 2a-d) support previous studies showing that the quenching of 1 O 2 production at the site of production by carotenoids (Ramel et al 2012;Telfer 2014), is important to maintain 1 O 2 at very low concentrations to prevent damage to PS II, because there is no enzyme-based antioxidant to quench 1 O 2 (Asada 2006;Triantaphylides and Havaux 2009;Pospíšil 2016;Roberty et al 2016). In fact, it has been hypothesized that the production of highly reactive 1 O 2 is suppressed by carotenoids (e.g., Brown et al 1999) at the expense of increased production of other species of ROS because there are specific enzymatic and nonenzymatic antioxidants available to quench those species of ROS (Asada 2006).…”

“…representing multiple phenotypes with different rates of photosynthesis, capacity to photoacclimatize, stress tolerance, and metabolic interchange with their hosts (Iglesias‐Prieto and Trench , ; Banaszak et al ; Robison and Warner ; Reynolds et al ; Hennige et al ; Brading et al ; Buxton et al ; Karim et al ; Warner and Suggett ) can be placed within the context of the revised phylogeny. One of these phenotypic character states, the production of reactive oxygen species (ROS) and the activities of antioxidants such as the enzyme superoxide dismutase (SOD), known to differ among phylotypes in the cladal phylogeny (Suggett et al ; Lesser ; McGinty et al ; Roberty et al , ; Kreuger et al ), can also be re‐examined as it relates to the new phylogeny, and the phenomenon of coral bleaching.…”

“…The result of ROS/RNS production is cellular stress with damage to many cellular components that can initiate coral bleaching caused by apoptosis (Lesser et al 1990;Lesser 1996Lesser , 2006Lesser , 2011Downs et al 2002Downs et al , 2013Lesser and Farrell 2004;Sandeman 2006;Suggett et al 2008;Saragosti et al 2010;Rehman et al 2016). The light dependency (i.e., photosynthetic) of ROS production followed by photosystem II (PSII) dysfunction (e.g., D1 protein damage) and bleaching has been repeatedly shown (Lesser and Shick 1989;Dykens et al 1992;Asada 1994Asada , 2006Lesser and Farrell 2004;Tchernov et al 2004;Smith et al 2005;Lesser 2006Lesser , 2011Suggett et al 2008;Roberty et al 2014Roberty et al , 2015Roberty et al , 2016 as has the recovery of photosynthetic capacity when exposed to exogenous antioxidants (Lesser 1996).…”

Different levels of energetic coupling between photosynthesis and respiration do not determine the occurrence of adaptive responses of Symbiodiniaceae to global warming

“…(Avir) can tolerate a wide range (10–35°C) of temperatures and rapidly fluctuating temperatures, in comparison to other Symbiodiniaceae. This could relate to the species' association to a host – a sea anemone, Anemonia viridis , which inhabits intertidal and sublittoral zones of temperate latitudes (Suggett et al ., 2012; Roberty et al ., 2016) (i.e. areas characterized by relatively wide daily and seasonal changes of temperature conditions, Table 1).…”

Alternative Photosynthetic Electron Transfers and Bleaching Phenotypes Upon Acute Heat Stress in Symbiodinium and Breviolum spp. (Symbiodiniaceae) in Culture

“…Plasticity of the photosynthetic apparatus may involve greater ROS tolerance [i.e., higher constitutive antioxidant defenses or higher ability to upregulate components of the antioxidant network (Krueger et al, 2014;Roberty et al, 2016), larger photoprotective capacities (Robison and Warner, 2006;Warner and Berry-Lowe, 2006), and/or some more efficient electron sinks (Warner and Suggett, 2016)]. Photosynthetic alternative electron flows (AEF) such as electron rerouting toward oxygen or cyclic electron flow (CEF) may essentially contribute to ensure photoprotection by decreasing excitation pressure on photosystems and by providing additional ATP to the cellular metabolism (reviewed in Munekage et al, 2008;Cardol et al, 2010;Johnson et al, 2014).…”