Diatom acclimation to elevated CO2 via cAMP signalling and coordinated gene expression

Abstract

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...

The ancestors of diatoms evolved a unique mitochondrial dehydrogenase to oxidize photorespiratory glycolate

“…Consistent with our finding that PtGO1 is a good candidate for the oxidation of photorespiratory glycolate, its expression was recently found to be downregulated in response to elevated CO 2 together with other genes involved in metabolizing photorespiratory glycolate (Hennon et al 2015). An analysis of transcript-level changes after induction of photorespiration in response to silicon starvation in T. pseudonana also indicated coordinately increased levels of the PtGO1 ortholog and other photorespiratory genes (Claquin et al 2002;Smith et al 2016).…”

“…An analysis of transcript-level changes after induction of photorespiration in response to silicon starvation in T. pseudonana also indicated coordinately increased levels of the PtGO1 ortholog and other photorespiratory genes (Claquin et al 2002;Smith et al 2016). In contrast, the PtGO2 homolog did not appear coordinately expressed with other photorespiratory genes (Hennon et al 2015;Smith et al 2016).…”

Ocean acidification of a coastal Antarctic marine microbial community reveals a critical threshold for CO<sub>2</sub> tolerance in phytoplankton productivity

“…Tolerance of CO 2 levels up to ∼ 1000 µatm has often been observed in natural phytoplankton communities in regions exposed to fluctuating CO 2 levels. In these communities, increasing CO 2 often had no effect on primary productivity (Tortell et al, 2000;Tortell and Morel, 2002;Tortell et al, 2008b;Hopkinson et al, 2010;Tanaka et al, 2013;Sommer et al, 2015;Young et al, 2015;Spilling et al, 2016) or growth (Tortell et al, 2008b;Schulz et al, 2013), although an increase in primary production has been observed in some instances (Riebesell, 2004;Tortell et al, 2008b;Egge et al, 2009;Tortell et al, 2010;Hoppe et al, 2013;Holding et al, 2015). These differing responses may be due to differences in community composition, nutrient supply, or ecological adaptations of the phytoplankton community in the region studied.…”

“…It is difficult to extrapolate the response of individual species to natural communities, as monospecific studies exclude interactions among species and trophic levels. Estimates of CO 2 tolerance under laboratory conditions may also be influenced by experimental acclimation periods (Trimborn et al, 2014;Hennon et al, 2015;Torstensson et al, 2015;Li et al, 2017a), differences in experimental conditions (e.g. nutrients, light climate) (Hoppe et al, 2015;Hong et al, 2017;Li et al, 2017b), methods of CO 2 manipulation (Shi et al, 2009;Gattuso et al, 2010), and region-specific environmental adaptations (Schaum et al, 2012).…”

Functional group-specific traits drive phytoplankton dynamics in the oligotrophic ocean

“…Molecular-level tools that can track transcripts, proteins, or even metabolites and biochemicals in a taxon-specific way are increasingly being used in cultures and field populations to track metabolic capacity and physiological responses (16)(17)(18)(19)(20)(21)(22)(23). Molecular assessment of physiology for eukaryotic populations is most tractable in coastal systems with high biomass (17,18); thus, in oligotrophic ocean regions, molecular studies of physiology have typically been limited to the numerically abundant members of the microbial community: picoplankton (cyanobacteria, heterotrophic bacteria, and small picoeukaryotes).…”