Storage Compound Accumulation in Diatoms as Response to Elevated CO2 Concentration

Abstract

Accumulation of reserve compounds (i.e., lipids and chrysolaminarin) in diatoms depends on the environmental conditions, and is often triggered by stress conditions, such as nutrient limitation. Manipulation of CO2 supply can also be used to improve both lipids and carbohydrates accumulation. Given the high diversity among diatoms, we studied the two marine model diatoms—Thalassiosira pseudonana and Phaeodactylum tricornutum, a freshwater diatom, Asterionella formosa, and Navicula pelliculosa—found in fresh- and sea-water environments. We measured the accumulation of reserve compounds and the activity of enzymes involved in carbon metabolism in these diatoms grown at high and atmospheric CO2. We observed that biomass and lipid accumulation in cells grown at high CO2 differ among the diatoms. Lipid accumulation increased only in P. tricornutum and N. pelliculosa grown in seawater in response to elevated CO2. Moreover, accumulation of lipids was also accompanied by an increased activity of the enzymes tested. However, lipid accumulation and enzyme activity decreased in N. pelliculosa cultured in fresh water. Chrysolaminarin accumulation was also affected by CO2 concentration; however, there was no clear relation with lipids accumulation. Our results are relevant to understand better the ecological role of the environment in the diatom adaptation to CO2 and the mechanisms underpinning the production of storage compounds considering diatom diversity.

Regulation of Carbon Metabolism by Environmental Conditions: A Perspective From Diatoms and Other Chromalveolates

“…The chloroplastic phosphoglycerate kinase belonging to the CBB cycle, catalyzes the ATP-Mg 2+ -dependent phosphorylation of 3-phosphoglycerate (3-PGA) to 1,3-bisphosphoglycerate, in a reversible reaction and was redox-regulated in P. tricornutum ( Belen Bosco et al, 2012 ). However, in our hands, PGK was not redox-regulated, as was also the case in T. pseudonana , in Navicula pelliculosa grown with sea water and fresh water medium and in a freshwater diatom, A. formosa ( Jensen et al, 2019b ). In contrast to the Viridiplantae, two enzymes that are unique to the CBB were not redox regulated ( Michels et al, 2005 ; Maberly et al, 2010 ; Jensen et al, 2017 ).…”

“…Metabolism enzymes, as well as enzymes responsible for pigment synthesis and indirectly in light capture (Figure 4), were less abundant, while enzymes involved in reactive oxygen species (ROS) defence increased in order to avoid accumulation of ROS that might occur when energy is in excess. The increased activity of pyruvate kinase (Figure 4), observed in T. pseudonana seems to be shared by other diatoms, as it was observed in many diatoms from freshwater to seawater species grown under high CO 2 (20,000 ppm) vs. atmospheric CO 2 (400 ppm) (Jensen et al, 2019b). In addition, a modification of gene expression has been described that allows synthesis of either PEP or pyruvate under carbon shortage, indicating that pyruvate is an important hub in these organisms (Heydarizadeh et al, 2017;Heydarizadeh et al, 2019) (Figure 4).…”

“…Physiological and genomic data are available for the response of some chromalveolates, especially diatoms, to light and CO 2 . (Wei et al, 2019) and T. pseudonana (Clement et al, 2017b;Jensen et al, 2019b). Cyclic AMP (cAMP) is a general [CO 2 ] signalling molecule that regulates gene expression (Ohno et al, 2012;Hennon et al, 2015;Young and Morel, 2015).…”

“…In contrast however, a ferredoxin-NADP reductase (FNR)-GAPDH-CP12 complex has been found in A. formosa ( Mekhalfi et al, 2014 ). For the chloroplastic GAPDH, the regulation is more complex as discussed above in the pH regulation section, but in many diatoms, this enzyme seems to be redox regulated ( Maberly et al, 2010 ; Mekhalfi et al, 2012 ; Mekhalfi et al, 2014 ; Jensen et al, 2019b ).…”

“…Like other algae, diatoms exhibit a range of responses to varying CO 2 concentration, including effects on photophysiology, rate of photosynthesis and growth, chemical and pigment composition, and community species composition, but there are large species- and context-specific variations in the magnitude and sign of response ( Boelen et al, 2011 ; Torstensson et al, 2012 ; Gao and Campbell, 2014 ; Dutkiewicz et al, 2015 ; Bach and Taucher, 2019 ; Jensen et al, 2019b ). At the ocean surface, the air-equilibrium concentration of CO 2 ( Dickson, 2010 ) varies between 5 and 25 µM depending on temperature ( Raven, 1994 ; Tortell, 2000 ; Kim et al, 2006 ; Matsuda et al, 2011 ; Maberly and Gontero, 2017 ).…”