Transitional traits determine the acclimation characteristics of the coccolithophore Chrysotila dentata to ocean warming and acidification

Abstract

Ocean warming and acidification interactively affect the coccolithophore physiology and drives major biogeochemical changes. While numerous studies investigated coccolithophore under short-term conditions, knowledge on how different transitional periods over long-exposure could influence the element, macromolecular and metabolic changes for its acclimation are largely unknown. We cultured the coccolithophore Chrysotila dentata, (culture generations of 1st, 10th, and 20th) under present (lowtemperature low-carbon-dioxide [LTLC]) and projected (high-temperature high-carbon-dioxide [HTHC]) ocean conditions. We examined elemental and macromolecular component changes and sequenced a transcriptome. We found that with long-exposure, most physiological responses in HTHC cells decreased when compared with those in LTLC, however, HTHC cell physiology showed constant elevation between each generation. Specifically, compared to 1st generation, the 20th generation HTHC cells showed increases in quota carbon (Qc:29%), nitrogen (Q N :101%), and subsequent changes in C:N-ratio (68%). We observed higher lipid accumulation than carbohydrates within HTHC cells under long-exposure, suggesting that lipids were used as an alternative energy source for cellular acclimation. Protein biosynthesis pathways increased their efficiency during long-term HTHC condition, indicating that cells produced more proteins than required to initiate acclimation. Our findings suggest that the coccolithophore resilience increased between the 1st-10th generation to initiate the acclimation process under ocean warming and acidifying conditions.

The cellular response to ocean warming in Emiliania huxleyi

“…Many of these components were also significantly raised under moderate warming compared to the control. Similar findings have been reported during proteomic analysis of the marine diatom, Skeletonema dohrnii , as well as during transcriptomic analyses on coccolithophore, prymnesiophyte and dinoflagellate taxa in response to warming combined with acidification ( Cheng et al, 2022 ; Liang et al, 2023 ; Thangaraj et al, 2023 ; Zhang et al, 2023 ). In E. huxleyi , this process appears fuelled by an increase in acetyl-CoA production via pyruvate and acetoacetyl CoA, catalyzed by the pyruvate dehydrogenase complex and acetyl-CoA acetyltransferase (R1FQ80), each significantly up-regulated in the elevated warming treatment relative to the control ( q ≤ 0.01).…”

“…In E. huxleyi , this process appears fuelled by an increase in acetyl-CoA production via pyruvate and acetoacetyl CoA, catalyzed by the pyruvate dehydrogenase complex and acetyl-CoA acetyltransferase (R1FQ80), each significantly up-regulated in the elevated warming treatment relative to the control ( q ≤ 0.01). Expression of the latter has previously been recorded to increase in the coccolithophore Chrysotila dentata following exposure to combined warming and acidification treatments ( Thangaraj et al, 2023 ).…”

“…It has been reported that under stress conditions coccolithophores utilize lipids as an alternative energy reserve and source of carbon for cellular metabolism ( Fernandez et al, 1994 ; Thangaraj et al, 2023 ). The enzyme, glycerol-3-phosphate dehydrogenase plays a key role linking carbohydrate and lipid metabolism by converting dihydroxyacetone phosphate produced by the action of triosephosphate isomerase to L-glycerol-3-phosphate ( Yao et al, 2014 ).…”

“…Abundance of enoyl-CoA hydratase, which catalyses the second step of the FA beta-oxidation pathway, was significantly increased under both moderate- (1.22 FC) and elevated- (1.05 FC) warming ( q ≤ 0.01). Transcripts related to this protein were also significantly up-regulated in C. dentata exposed to warming and acidification ( Thangaraj et al, 2023 ). An increase in FA biosynthesis in the two warming treatments relative to the control is largely expected given their higher energy surplus, indicated by higher rates of growth.…”

“…Advances in omics technologies have broadened our ability to consider the impact of environmental perturbations upon biota. A number of transcriptome studies have been carried out to examine the molecular pathways most impacted by temperature in marine phytoplankton at the gene expression level, often in conjunction with an additional environmental stressors such as ocean acidification ( Thangaraj and Sun, 2021 ; Jin et al, 2022 ; Liang et al, 2023 ; Thangaraj et al, 2023 ; Zhang et al, 2023 ). Proteomic analysis, the examination of organismal response at the individual protein scale, can enhance our understanding of the metabolic response.…”