Research Article: Ocean acidification modulates expression of genes and physiological performance of a marine diatom

Date Published: February 13, 2017

Publisher: Public Library of Science

Author(s): Yahe Li, Shufang Zhuang, Yaping Wu, Honglin Ren, Fangyi Chen, Xin Lin, Kejian Wang, John Beardall, Kunshan Gao, Adrianna Ianora.

http://doi.org/10.1371/journal.pone.0170970

Abstract

Ocean Acidification (OA) is known to affect various aspects of physiological performances of diatoms, but little is known about the underlining molecular mechanisms involved. Here, we show that in the model diatom Phaeodactylum tricornutum, the expression of key genes associated with photosynthetic light harvesting as well as those encoding Rubisco, carbonic anhydrase, NADH dehydrogenase and nitrite reductase, are modulated by OA (1000 μatm, pHnbs 7.83). Growth and photosynthetic carbon fixation were enhanced by elevated CO2. OA treatment decreased the expression of β-carbonic anhydrase (β-ca), which functions in balancing intracellular carbonate chemistry and the CO2 concentrating mechanism (CCM). The expression of the genes encoding fucoxanthin chlorophyll a/c protein (lhcf type (fcp)), mitochondrial ATP synthase (mtATP), ribulose-1, 5-bisphosphate carboxylase/oxygenase large subunit gene (rbcl) and NADH dehydrogenase subunit 2 (ndh2), were down-regulated during the first four days (< 8 generations) after the cells were transferred from LC (cells grown under ambient air condition; 390 μatm; pHnbs 8.19) to OA conditions, with no significant difference between LC and HC treatments with the time elapsed. The expression of nitrite reductase (nir) was up-regulated by the OA treatment. Additionally, the genes for these proteins (NiR, FCP, mtATP synthase, β-CA) showed diel expression patterns. It appeared that the enhanced photosynthetic and growth rates under OA could be attributed to stimulated nitrogen assimilation, increased CO2 availability or saved energy from down-regulation of the CCM and consequently lowered cost of protein synthesis versus that of non-nitrogenous cell components.

Partial Text

Ocean acidification (OA), expressed in milieu as a decline in pH, is driven by rapid increases in CO2 taken up by the oceans from the atmosphere and is altering marine chemical environments with consequences for marine organisms and the biological CO2 pump [1]. Although intracellular pH levels of both photosynthetic organisms and animals are known to be below that of the bulk seawater pH [2], external pH decline is known to affect the physiology of many marine organisms to different extents [3]. For instance extracellular pH changes can influence the membrane electrochemical potential and enzyme activity [4–6]. Additionally, different and controversial responses of diatoms to OA have been reported [7]. For instance, in the model diatom Phaeodactylum tricornutum, growth and photosynthetic carbon fixation rate were enhanced when cells were acclimated to 1000 μatm CO2 under indoor low light conditions [8–10], but became inhibited under elevated pCO2 levels under fluctuating high sunlight levels [9]. The active CO2 acquisition process, the CO2 concentrating mechanism (CCM), is known to be down-regulated under increased CO2 levels [11], which may increase light stress under high light levels but conversely can enhance the growth of diatoms under low light levels [9]. Consequently, changes in the energy budget of diatoms grown under OA conditions could alter the energy costs for protein synthesis versus that of non-nitrogenous cell components [12, 13]. Photophysiological performance could also be altered, since some microalgae that lack NDH-1 require a plastidial NDH-2 in cyclic electron flow (CEF) to produce extra ATP needed for CO2 fixation [14, 15].

Phytoplankton cells within the upper mixed layers of the oceans are exposed to both increasing pCO2 and higher solar radiation due to enhanced thermal stratification. Interactions of these two key factors are crucial for predictions of the biological consequences of global change in the oceans. Here, we showed for the first time that the marine diatom P. tricornutum under elevated CO2 up-regulated a gene related to nitrogen assimilation while it down-regulated the gene for β-CA, a protein functioning in maintaining CO2 bicarbonate equilibrium, CO2 diffusion to Rubisco and CCMs within cells.

 

Source:

http://doi.org/10.1371/journal.pone.0170970

 

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