The cellular response to ocean warming in Emiliania huxleyi

Abstract

Marine phytoplankton contribute substantially to the global flux of carbon from the atmosphere to the deep ocean. Sea surface temperatures will inevitably increase in line with global climate change, altering the performance of marine phytoplankton. Differing sensitivities of photosynthesis and respiration to temperature, will likely shift the strength of the future oceanic carbon sink. To further clarify the molecular mechanisms driving these alterations in phytoplankton function, shotgun proteomic analysis was carried out on the globally-occurring coccolithophore Emiliania huxleyi exposed to moderate- (23°C) and elevated- (28°C) warming. Compared to the control (17°C), growth of E. huxleyi increased under elevated temperatures, with higher rates recorded under moderate- relative to elevated- warming. Proteomic analysis revealed a significant modification of the E. huxleyi cellular proteome as temperatures increased: at lower temperature, ribosomal proteins and photosynthetic machinery appeared abundant, as rates of protein translation and photosynthetic performance are restricted by low temperatures. As temperatures increased, evidence of heat stress was observed in the photosystem, characterized by a relative down-regulation of the Photosystem II oxygen evolving complex and ATP synthase. Acclimation to elevated warming (28°C) revealed a substantial alteration to carbon metabolism. Here, E. huxleyi made use of the glyoxylate cycle and succinate metabolism to optimize carbon use, maintain growth and maximize ATP production in heat-damaged mitochondria, enabling cultures to maintain growth at levels significantly higher than those recorded in the control (17°C). Based on the metabolic changes observed, we can predict that warming may benefit photosynthetic carbon fixation by E. huxleyi in the sub-optimal to optimal thermal range. Past the thermal optima, increasing rates of respiration and costs of repair will likely constrain growth, causing a possible decline in the contribution of this species to the oceanic carbon sink depending on the evolvability of these temperature thresholds.

Warming modulates the photosynthetic performance of Thalassiosira pseudonana in response to UV radiation

“…This will have a profound influence on ocean-dwelling organisms, as temperature significantly affects metabolic function and enzyme activity. It is predicted that the distribution and ecology of the components of phytoplankton, including dinoflagellates, diatoms and coccolithophores, would change with ocean warming (Hare et al, 2007;Hallegraeff, 2010;Cabrerizo et al, 2014;Dedman et al, 2023). Ocean warming has also been indicated to intensify stratification (Gao et al, 2019), with the upper mixed layer (UML) becoming shallower, which would influence the degree of exposure of organisms in the UML to photosynthetically active radiation (PAR) and UVR (Häder and Gao, 2015).…”

Gephyrocapsa huxleyi (Emiliania huxleyi) as a model system for coccolithophore biology

“…An exciting development is the application of single-cell RNA-seq, which was used to profile transcriptomes from individual G. huxleyi cells throughout the viral infection cycle (Ku et al, 2020). Proteomic approaches have been used extensively in G. huxleyi to examine, for example, the cellular responses to warming (Dedman et al, 2023) and to identify processes that are affected by nutrient limitation (McKew et al, 2015;Shire & Kustka, 2022). Metabolomic studies have revealed the importance of mannitol as a carbon storage compound in G. huxleyi (Obata et al, 2013) and identified important metabolic differences between life-cycle stages during nutrient starvation (Wordenweber et al, 2018).…”

“…Proteomic approaches have been used extensively in G . huxleyi to examine, for example, the cellular responses to warming (Dedman et al., 2023) and to identify processes that are affected by nutrient limitation (McKew et al., 2015; Shire & Kustka, 2022). Metabolomic studies have revealed the importance of mannitol as a carbon storage compound in G .…”

Variations of polyphenols and carbohydrates of Emiliania huxleyi grown under simulated ocean acidification conditions

“…Microalgae play a key role in marine ecosystems, forming the basis of the marine food chain as they are responsible for almost half of the total primary production (Usher et al, 2014;Dedman et al, 2023). They constitute a potential feedstock because of their valuable metabolites such as pigments, vitamins, proteins, carbohydrates, and lipids with valued fatty acids.…”