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Responses of the marine diatom Thalassiosira pseudonana to changes in CO2 concentration: a proteomic approach.

ABSTRACT: The concentration of CO2 in many aquatic systems is variable, often lower than the KM of the primary carboxylating enzyme Rubisco, and in order to photosynthesize efficiently, many algae operate a facultative CO2 concentrating mechanism (CCM). Here we measured the responses of a marine diatom, Thalassiosira pseudonana, to high and low concentrations of CO2 at the level of transcripts, proteins and enzyme activity. Low CO2 caused many metabolic pathways to be remodeled. Carbon acquisition enzymes, primarily carbonic anhydrase, stress, degradation and signaling proteins were more abundant while proteins associated with nitrogen metabolism, energy production and chaperones were less abundant. A protein with similarities to the Ca2+/ calmodulin dependent protein kinase II_association domain, having a chloroplast targeting sequence, was only present at low CO2. This protein might be a specific response to CO2 limitation since a previous study showed that other stresses caused its reduction. The protein sequence was found in other marine diatoms and may play an important role in their response to low CO2 concentration.

SUBMITTER: Clement R

PROVIDER: S-EPMC5299434 | biostudies-literature | 2017 Feb

REPOSITORIES: biostudies-literature

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Responses of the marine diatom Thalassiosira pseudonana to changes in CO2 concentration: a proteomic approach.

Clement Romain R Lignon Sabrina S Mansuelle Pascal P Jensen Erik E Pophillat Matthieu M Lebrun Regine R Denis Yann Y Puppo Carine C Maberly Stephen C SC Gontero Brigitte B

Scientific reports 20170209

The concentration of CO2 in many aquatic systems is variable, often lower than the KM of the primary carboxylating enzyme Rubisco, and in order to photosynthesize efficiently, many algae operate a facultative CO2 concentrating mechanism (CCM). Here we measured the responses of a marine diatom, Thalassiosira pseudonana, to high and low concentrations of CO2 at the level of transcripts, proteins and enzyme activity. Low CO2 caused many metabol ...[more]

PMID: 28181560

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Project description:BackgroundCP12 is a small chloroplast protein that is widespread in various photosynthetic organisms and is an actor of the redox signaling pathway involved in the regulation of the Calvin Benson Bassham (CBB) cycle. The gene encoding this protein is conserved in many diatoms, but the protein has been overlooked in these organisms, despite their ecological importance and their complex and still enigmatic evolutionary background.MethodsA combination of biochemical, bioinformatics and biophysical methods including electrospray ionization-mass spectrometry, circular dichroism, nuclear magnetic resonance spectroscopy and small X ray scattering, was used to characterize a diatom CP12.ResultsHere, we demonstrate that CP12 is expressed in the marine diatom Thalassiosira pseudonana constitutively in dark-treated and in continuous light-treated cells as well as in all growth phases. This CP12 similarly to its homologues in other species has some features of intrinsically disorder protein family: it behaves abnormally under gel electrophoresis and size exclusion chromatography, has a high net charge and a bias amino acid composition. By contrast, unlike other known CP12 proteins that are monomers, this protein is a dimer as suggested by native electrospray ionization-mass spectrometry and small angle X-ray scattering. In addition, small angle X-ray scattering revealed that this CP12 is an elongated cylinder with kinks. Circular dichroism spectra indicated that CP12 has a high content of α-helices, and nuclear magnetic resonance spectroscopy suggested that these helices are unstable and dynamic within a millisecond timescale. Together with in silico predictions, these results suggest that T. pseudonana CP12 has both coiled coil and disordered regions.ConclusionsThese findings bring new insights into the large family of dynamic proteins containing disordered regions, thus increasing the diversity of known CP12 proteins. As it is a protein that is more abundant in many stresses, it is not devoted to one metabolism and in particular, it is not specific to carbon metabolism. This raises questions about the role of this protein in addition to the well-established regulation of the CBB cycle. Choregraphy of metabolism by CP12 proteins in Viridiplantae and Heterokonta. While the monomeric CP12 in Viridiplantae is involved in carbon assimilation, regulating phosphoribulokinase (PRK) and glyceraldehyde-3-phosphate dehydrogenase (GAPDH) through the formation of a ternary complex, in Heterokonta studied so far, the dimeric CP12 is associated with Ferredoxin-NADP reductase (FNR) and GAPDH. The Viridiplantae CP12 can bind metal ions and can be a chaperone, the Heterokonta CP12 is more abundant in all stresses (C, N, Si, P limited conditions) and is not specific to a metabolism. Video Abstract.

Project description:Bacteria-diatom interactions in the ocean are diverse but usually studied in static conditions, which limits our understanding of their importance in marine ecosystems and biogeochemical cycles. Here, we explored the dynamic interactions between an ubiquitous marine bacterium Alteromonas sp. and a diatom Thalassiosira pseudonana under different nutrient conditions. In oligotrophic conditions, minor shifts in nutrients qualitatively altered the interactions from mutualism during early exponential growth to weak parasitism during the late stationary phase. Organic matter-activated Alteromonas chemotactically swam toward, attached on, and dramatically broke down T. pseudonana cells, leading to an aggressive parasitic behavior with a 95% algicidal rate. Meanwhile, inorganic matter-activated T. pseudonana showed amensalism against Alteromonas, resulting in an ephemeral decrease of bacterial abundance by 27%. Interestingly, when both organics and inorganics were sufficient, Alteromonas suppressed diatom growth by inhibiting the cell division, while the surviving T. pseudonana restored proliferation with a significantly smaller cell size inconducive to bacterial attachment, demonstrating an intense competition. The results further indicated that the algicidal effect of Alteromonas was controlled by the cell-specific protease activity and the number of attached bacteria on the diatom cell surface, both of which were related to nutrient conditions. Since the nature and intensity of bacteria-diatom interaction depend on the composition and richness of nutrients, it mechanistically explains the tripartite relationship among bacterial proliferation, nutrient viability, and algal demise during blooms. The algicidal behavior of copiotrophs also potentially enhances the contribution of a microbial carbon pump to carbon sequestration in the ocean. IMPORTANCE As the major producers and consumers, phytoplankton and bacteria play central roles in marine ecosystems and their interactions show great ecological significance. Whether mutualistic or antagonistic, the interaction between certain phytoplankton and bacterial species is usually seen as a derivative of intrinsic physiological properties and rarely changes. This study demonstrated that the interactions between the ubiquitously co-occurring bacteria and diatom, Alteromonas and Thalassiosira pseudonana, varied with nutrient conditions. They overcame hardship together in oligotrophic seawater but showed antagonistic effects against each other under nutrient amendment. The contact-dependent algicidal behavior of Alteromonas based on protease activity solved the paradox among bacterial proliferation, nutrient viability, and algal demise haunting other known non-contact-dependent algicidal processes and might actually trigger the collapse of algal blooms in situ. The chemotactic and swarming movement of Alteromonas might also contribute greatly to the breakdown of "marine snow," which could redirect the carbon sequestration pathway in the ocean.

Dataset Information

Responses of the marine diatom Thalassiosira pseudonana to changes in CO2 concentration: a proteomic approach.

Publications

Responses of the marine diatom Thalassiosira pseudonana to changes in CO<sub>2</sub> concentration: a proteomic approach.

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