Proteomic analysis of metabolic pathways supports chloroplast-mitochondria cross-talk in a Cu-limited diatom

Abstract

Diatoms are one of the most successful phytoplankton groups in our oceans, being responsible for over 20% of the Earth’s photosynthetic productivity. Their chimeric genomes have genes derived from red algae, green algae, bacteria and heterotrophs, resulting in multiple isoenzymes targeted to different cellular compartments with the potential for differential regulation under nutrient limitation. The resulting interactions between metabolic pathways are not yet fully understood.We previously showed how acclimation to Cu limitation enhanced susceptibility to overreduction of the photosynthetic electron transport chain and its reorganization to favor photoprotection over light-harvesting in the oceanic diatom Thalassiosira oceanica (Hippmann et al., 2017). In order to understand the overall metabolic changes that help alleviate the stress of Cu limitation, we generated comprehensive proteomic datasets from the diatom Thalassiosira oceanica grown under Cu-limiting and -replete conditions. The datasets were used to identify differentially expressed proteins involved in carbon, nitrogen and oxidative stress-related metabolic pathways and to predict the proteins cellular location.Metabolic pathway analysis showed integrated responses to Cu limitation in diatoms. The up-regulation of ferredoxin (Fdx) was correlated with up-regulation of plastidial Fdx-dependent isoenzymes involved in nitrogen assimilation as well as enzymes involved in glutathione synthesis thus integrating nitrogen uptake and metabolism with photosynthesis and oxidative stress resistance. The differential regulation of glycolytic isoenzymes located in the chloroplast and mitochondria enables them to channel both excess electrons and/or ATP between these compartments. Additional evidence for chloroplast-mitochondrial cross-talk is shown by up-regulation of chloroplast and mitochondrial proteins involved in the proposed malate shunt.One sentence summaryDiatoms adapt to Cu limitation by regulating their large repertoire of isoenzymes to channel electrons away from the chloroplast, enhance nitrogen uptake, and integrate the oxidative stress response. 123

Characterizing the Roles of Biogeochemical Cycling and Ocean Circulation in Regulating Marine Copper Distributions

“…Under Fe-limited conditions, phytoplankton Cu demands increase (Annett et al, 2008;Biswas et al, 2013;Guo et al, 2010;Maldonado et al, 2006;Peers et al, 2005;Peers & Price, 2006). Hence, the high biological utilization of Cu in the Southern Ocean where Fe limitation occurs (Moore et al, 2013;Tagliabue et al, 2017), could be due to the enhanced usage of Cu in marine phytoplankton physiology (Guo et al, 2010(Guo et al, , 2015Hippmann et al, 2017Hippmann et al, , 2020Lelong et al, 2013). In comparison, in the Atlantic, where Fe is abundant, marine phytoplankton may not select Cu, contributing to the substantially weaker biological utilization of Cu in this region.…”

A metabolic, phylogenomic and environmental atlas of diatom plastid transporters from the model species Phaeodactylum

“…Finally, diatoms and their plastid metabolism may act as important bellwethers of environmental and climate change (Spetea et al, 2014). Previous studies have demonstrated that both geochemical factors (e.g., iron and copper concentrations) (Hippmann et al, 2020;Kong and Price, 2021;Turnsěk et al, 2021) alongside physical factors (pH, CO 2 availability, and temperature) (Tong et al, 2021;Zhong et al, 2021) directly influence diatom photosynthetic activity and abundance. Understanding the roles of specific plastid transporters in these responses, such as the production and accumulation of plastid metabolites and compatible ions implicated in stress tolerance (Marchand et al, 2018), and intracellular communication between various subcellular compartments may allow more nuanced prediction of diatom responses to dynamically changing environments (Murik et al, 2019;Hippmann et al, 2020).…”

Physiological adaptation of the diatom Pseudo-nitzschia delicatissima under copper starvation

“…Cu limitation can therefore induce deleterious effects on microalgal cells, such as inhibiting growth rate [9,10], photosynthesis, carbon fixation, respiration [4,14,15]. While some strains can mitigate Cu limitation stress, the research on the physiological adaptations of microalgae to Cu limitation remains scarce.…”