Diatoms are responsible for ∼40% of marine primary productivity 1 , fuelling the oceanic carbon cycle and contributing to natural carbon sequestration in the deep ocean 2 . Diatoms rely on energetically expensive carbon concentrating mechanisms (CCMs) to fix carbon e ciently at modern levels of CO 2 (refs 3-5). How diatoms may respond over the short and long term to rising atmospheric CO 2 remains an open question. Here we use nitrate-limited chemostats to show that the model diatom Thalassiosira pseudonana rapidly responds to increasing CO 2 by di erentially expressing gene clusters that regulate transcription and chromosome folding, and subsequently reduces transcription of photosynthesis and respiration gene clusters under steady-state elevated CO 2 . These results suggest that exposure to elevated CO 2 first causes a shift in regulation, and then a metabolic rearrangement. Genes in one CO 2 -responsive cluster included CCM and photorespiration genes that share a putative cAMP-responsive cis-regulatory sequence, implying these genes are co-regulated in response to CO 2 , with cAMP as an intermediate messenger.We verified cAMP-induced downregulation of CCM gene δ-CA3 in nutrient-replete diatom cultures by inhibiting the hydrolysis of cAMP. These results indicate an important role for cAMP in downregulating CCM and photorespiration genes under elevated CO 2 and provide insights into mechanisms of diatom acclimation in response to climate change.Burning fossil fuels and land-use change have accelerated CO 2 emissions to the atmosphere by a factor ∼100 above natural levels 6 . About a third of anthropogenic emissions have been absorbed by the oceans 7,8 , increasing dissolved CO 2 and reducing pH (ref. 9). Despite these changes, CO 2 concentrations in surface waters remain below half-saturation for most forms of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) 3 , the central enzyme used to fix carbon. Consequently, marine phytoplankton, including diatoms, rely on carbon concentrating mechanisms (CCMs) to ensure adequate delivery of CO 2 to the Rubisco active site, minimizing the competitive fixation of oxygen 3-5 . The required bicarbonate transporters and carbonic anhydrases of these CCMs concentrate CO 2 against a gradient, which is energetically costly 10 . Downregulation of CCMs as part of acclimation to elevated CO 2 should result in energy savings to the diatom cell and metabolic rearrangement. Here we use nitrate-limited chemostats to simulate in situ nutrient limitation 11 while precisely controlling cell biomass and CO 2 (ref. 12), allowing us to identify potential signalling pathways triggered either by an abrupt transition to increased CO 2 , as might occur during coastal upwelling 13 , or at steady-state exposure to elevated CO 2 , including 800 µatm predicted for 2100 (ref. 14; Fig. 1a,b).Metabolic and regulatory genes were differentially impacted by changes in CO 2 (Fig. 1c). The initial response to an abrupt increase in CO 2 included upregulation of genes required for transcriptional regul...
Sunlight is the dominant control on phytoplankton biosynthetic activity, and darkness deprives them of their primary external energy source. Changes in the biochemical composition of phytoplankton communities over diel light cycles and attendant consequences for carbon and energy flux in environments remain poorly elucidated. Here we use lipidomic data from the North Pacific subtropical gyre to show that biosynthesis of energy-rich triacylglycerols (TAGs) by eukaryotic nanophytoplankton during the day and their subsequent consumption at night drives a large and previously uncharacterized daily carbon cycle. Diel oscillations in TAG concentration comprise 23 ± 11% of primary production by eukaryotic nanophytoplankton representing a global flux of about 2.4 Pg C yr−1. Metatranscriptomic analyses of genes required for TAG biosynthesis indicate that haptophytes and dinoflagellates are active members in TAG production. Estimates suggest that these organisms could contain as much as 40% more calories at sunset than at sunrise due to TAG production.
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