GSE67971
Diatom acclimation to elevated CO2 via novel gene clusters and cAMP-signaling
Diatoms are responsible for ~40% of marine primary productivity1, fueling the oceanic carbon cycle and contributing to natural carbon sequestration in the deep ocean2. Diatoms rely on energetically expensive carbon concentrating mechanisms (CCMs) to fix carbon efficiently at modern levels of CO23–5. How diatoms may respond over the short and long-term to rising atmospheric CO2 remains an open question. Here we use nitrate-limited chemostats to show that the model diatom Thalassiosira pseudonana rapidly responds to increasing CO2 by differentially expressing gene clusters that regulate transcription and chromosome folding and subsequently reduces transcription of photosynthesis and respiration gene clusters under steady-state elevated CO2. These results suggest that exposure to elevated CO2 first causes a shift in regulation and then a metabolic rearrangement. Genes in one CO2-responsive cluster included CCM and photorespiration genes that share a putative cyclic-AMP responsive cis-regulatory sequence, implying these genes are co-regulated in response to CO2 with cAMP as an intermediate messenger. We verified cAMP-induced down-regulation of CCM gene d-CA3 in nutrient-replete diatom cultures by inhibiting the hydrolysis of cAMP. These results indicate an important role for cAMP in down-regulating CCM and photorespiration genes under elevated CO2 and provide insights into mechanisms of diatom acclimation in response to climate change. Overall design: In steady-state experiments: axenic T. pseudonana cells in four biological replicates (duplicate chemostats x 2 experimental runs) were acclimated to nitrate-limitation at 70% (1.5 day-1) of max growth rate for >10 days (>15 generations) under continuous light of 80 µmol photons·m­-2·s-1. Cell biomass was maintained at ~2 x 105 cells·mL-1 by 10 µM nitrate and carbonate chemistry stabilized to 300, 475 or 800 µatm CO2, verified by pH and DIC measurements. Transition samples and carbonate chemistry were collected daily from chemostat cultures as CO2 levels were increased from ~300-800 µatm at a rate = 0.2 µatm·min-1 over four consecutive days (6 generations) after pre-acclimation to 300 µatm CO2 and nitrate-limitation.