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...
Prochlorococcus is a globally important marine cyanobacterium that lacks the gene catalase and relies on 'helper' bacteria such as Alteromonas to remove reactive oxygen species. Increasing atmospheric CO decreases the need for carbon concentrating mechanisms and photorespiration in phytoplankton, potentially altering their metabolism and microbial interactions even when carbon is not limiting growth. Here, Prochlorococcus (VOL4, MIT9312) was co-cultured with Alteromonas (strain EZ55) under ambient (400 p.p.m.) and elevated CO (800 p.p.m.). Under elevated CO, Prochlorococcus had a significantly longer lag phase and greater apparent die-offs after transfers suggesting an increase in oxidative stress. Whole-transcriptome analysis of Prochlorococcus revealed decreased expression of the carbon fixation operon, including carboxysome subunits, corresponding with significantly fewer carboxysome structures observed by electron microscopy. Prochlorococcus co-culture responsive gene 1 had significantly increased expression in elevated CO, potentially indicating a shift in the microbial interaction. Transcriptome analysis of Alteromonas in co-culture with Prochlorococcus revealed decreased expression of the catalase gene, known to be critical in relieving oxidative stress in Prochlorococcus by removing hydrogen peroxide. The decrease in catalase gene expression was corroborated by a significant ~6-fold decrease in removal rates of hydrogen peroxide from co-cultures. These data suggest Prochlorococcus may be more vulnerable to oxidative stress under elevated CO in part from a decrease in ecosystem services provided by heterotrophs like Alteromonas. This work highlights the importance of considering microbial interactions in the context of a changing ocean.The ISME Journal advance online publication, 31 October 2017; doi:10.1038/ismej.2017.189.
SeaFlow is an underway flow cytometer that provides continuous shipboard observations of the abundance and optical properties of small phytoplankton (<5 μm in equivalent spherical diameter, ESD). Here we present data sets consisting of SeaFlow-based cell abundance, forward light scatter, and pigment fluorescence of individual cells, as well as derived estimates of ESD and cellular carbon content of picophytoplankton, which includes the cyanobacteria Prochlorococcus, Synechococcus and small-sized Crocosphaera (<5 μm ESD), and picophytoplankton and nanophytoplankton (2–5 μm ESD). Data were collected in surface waters (≈5 m depth) from 27 oceanographic cruises carried out in the Northeast Pacific Ocean between 2010 and 2018. Thirteen cruises provide high spatial resolution (≈1 km) measurements across 32,500 km of the Northeast Pacific Ocean and 14 near-monthly cruises beginning in 2015 provide seasonal distributions at the long-term sampling site (Station ALOHA) of the Hawaii Ocean Time-Series. These data sets expand our knowledge of the current spatial and temporal distributions of picophytoplankton in the surface ocean.
Diatoms are responsible for a large proportion of global carbon fixation, with the possibility that they may fix more carbon under future levels of high CO2 . To determine how increased CO2 concentrations impact the physiology of the diatom Thalassiosira pseudonana Hasle et Heimdal, nitrate-limited chemostats were used to acclimate cells to a recent past (333 ± 6 μatm) and two projected future concentrations (476 ± 18 μatm, 816 ± 35 μatm) of CO2 . Samples were harvested under steady-state growth conditions after either an abrupt (15-16 generations) or a longer acclimation process (33-57 generations) to increased CO2 concentrations. The use of un-bubbled chemostat cultures allowed us to calculate the uptake ratio of dissolved inorganic carbon relative to dissolved inorganic nitrogen (DIC:DIN), which was strongly correlated with fCO2 in the shorter acclimations but not in the longer acclimations. Both CO2 treatment and acclimation time significantly affected the DIC:DIN uptake ratio. Chlorophyll a per cell decreased under elevated CO2 and the rates of photosynthesis and respiration decreased significantly under higher levels of CO2 . These results suggest that T. pseudonana shifts carbon and energy fluxes in response to high CO2 and that acclimation time has a strong effect on the physiological response.
Anthropogenic CO 2 emissions are perturbing the global carbon cycle more rapidly than at any time in the last 66 million years (Zeebe et al., 2016). A key component of the natural carbon cycle is coccolithophores, which modify oceanic dissolved inorganic carbon and alkalinity inventories through photosynthetic carbon fixation and the biogenic production of calcium carbonate plates (Balch et al., 1992). These eukaryotic algae are abundant and widely distributed throughout the global oceans today (
With rising atmospheric CO2, phytoplankton face shifts in ocean chemistry including increased dissolved CO2 and acidification that will likely influence the relative competitive fitness of different phytoplankton taxa. Here we compared the physiological and gene expression responses of six species of phytoplankton including a diatom, a raphidophyte, two haptophytes, and two dinoflagellates to ambient (~400 ppm) and elevated (~800 ppm) CO2. Dinoflagellates had significantly slower growth rates and higher, yet variable, chlorophyll a per cell under elevated CO2. The other phytoplankton tended to have increased growth rates and/or decreased chlorophyll a per cell. Carbon and nitrogen partitioning of cells shifted under elevated CO2 in some species, indicating potential changes in energy fluxes due to changes in carbon concentrating mechanisms (CCM) or photorespiration. Consistent with these phenotypic changes, gene set enrichment analyses revealed shifts in energy, carbon and nitrogen metabolic pathways, though with limited overlap between species in the genes and pathways involved. Similarly, gene expression responses across species revealed few conserved CO2-responsive genes within CCM and photorespiration categories, and a survey of available transcriptomes found high diversity in biophysical CCM and photorespiration expressed gene complements between and within the four phyla represented by these species. The few genes that displayed similar responses to CO2 across phyla were from understudied gene families, making them targets for further research to uncover the mechanisms of phytoplankton acclimation to elevated CO2. These results underscore that eukaryotic phytoplankton have diverse gene complements and gene expression responses to CO2 perturbations and highlight the value of cross-phyla comparisons for identifying gene families that respond to environmental change.
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