Physiological response of Symbiodiniaceae to thermal stress: Reactive oxygen species, photosynthesis, and relative cell size

Abstract

This study investigates the physiological response to heat stress of three genetically different Symbiodiniaceae strains isolated from the scleractinian coral Mussismilia braziliensis, endemic of the Abrolhos Bank, Brazil. Cultures of two Symbiodinium sp. and one Cladocopium sp. were exposed to a stepwise increase in temperature (2°C every second day) ranging from 26°C (modal temperature in Abrolhos) to 32°C (just above the maximum temperature registered in Abrolhos during the third global bleaching event—TGBE). After the cultures reached their final testing temperature, reactive oxygen species (ROS) production, single cell attributes (relative cell size and chlorophyll fluorescence), and photosynthetic efficiency (effective (Y(II)) and maximum (Fv/Fm) quantum yields) were measured within 4 h and 72 h. Non-photochemical coefficient (NPQ) was estimated based on fluorescence values. Population average ROS production was variable across strains and exposure times, reaching up a 2-fold increase at 32°C in one of the Symbiodinium sp. strains. A marked intrapopulation difference was observed in ROS production, with 5 to 25% of the cells producing up to 10 times more than the population average, highlighting the importance of single cell approaches to assess population physiology. Average cell size increases at higher temperatures, likely resulting from cell cycle arrest, whereas chlorophyll fluorescence decreased, especially in 4 h, indicating a photoacclimation response. The conditions tested do not seem to have elicited loss of photosynthetic efficiency nor the activation of non-photochemical mechanisms in the cells. Our results unveiled a generalized thermotolerance in three Symbiodiniaceae strains originated from Abrolhos’ corals. Inter and intra-specific variability could be detected, likely reflecting the genetic differences among the strains.

Diversity of lipid profiles of Symbiodiniaceae under temperature and nutrient stress

“…Over-abundance of ROS under temperature stress can result in photosystem damage and alterations to thylakoid membranes, lipid peroxidation, and an increase in the abundance of oxidized lipids generated by free radicals (Botana et al, 2022;Xing et al, 2022;Amario et al, 2023). Here, there was an increased relative abundance of oxidized phosphatidylinositol (OxPI) across all Symbiodiniaceae species grown at 31°C (Figure 8; Supplementary Table 24).…”

“…Unsaturated fatty acids are more susceptible to ROS attack than saturated fatty acids (Bacellar and Baptista, 2019), therefore, increased saturation of membrane-bound fatty acids can serve to maintain microalgal cell stability during heat stress (Los and Murata, 2004). ROS accumulation has been shown with increased temperature in Cladocopium sp (McGinty et al, 2012) and D. trenchii (Scharfenstein et al, 2023), and higher abundance of ROS has also been linked to increases in cell size (Lima et al, 2022;Amario et al, 2023). Indeed, D. trenchii and C. goreaui (HM & HW) cell sizes increased when grown at 31°C (Figure 3) in this study, indicating potential cellular swelling prior to cell cycle arrest and necrosis as a result of heat stress (Dunn et al, 2004).…”

Multi-Chemical Omics Analysis of the Symbiodiniaceae Durusdinium trenchii under Heat Stress

“…This inositol stereoisomer is suspected to protect cellular structures from reactive oxidizers [ 63 ]. Under high temperatures, Symbiodiniaceae have been observed to increase production and accumulation of reactive oxygen species (ROS) due to heat-induced damage to the photosynthetic apparatus [ 64 ], thus this profile change is further evidence for the role of inositol as a cellular protectant from stress in Symbiodiniaceae.…”

A microfluidic microalgae detection system for cellular physiological response based on an object detection algorithm

“…Variations in factors such as temperature, light exposure, pH, and salinity can accelerate the bleaching or death of cells, affecting their symbiotic relationship with the host and resulting in widespread coral bleaching. 23–26 Especially at this stage, the anthropogenic discharge of industrial wastewater exacerbates changes in marine environments, which is undeniably detrimental to environmentally sensitive algae. Current assays, nevertheless, are mostly performed at the population level, measuring values averaged across all algal cells, thereby overlooking the potential stress-resistant individual cells within the samples.…”