Growth, photosynthesis, and gene expression in Chlamydomonas over a range of CO2 concentrations and CO2/O2 ratios: CO2 regulates multiple acclimation states

Abstract

Growth, photosynthesis, and induction of two low CO2-inducible genes of Chlamydomonas reinhardtii Dangeard strain CC125 were quantified in a range of physiologically relevant CO2 and O2 concentrations (5%–0.005% CO2 and 20% or 2% O2) using airlift bioreactors to facilitate the simultaneous measurement of both growth and in situ photosynthetic rates. Within these CO2 concentration ranges, O2 concentrations (20% vs. 2%) had no discernable effect on growth, photosynthetic rate, or induction of the periplasmic carbonic anhydrase (Cah1) and glycolate dehydrogenase (Gdh) genes in wild-type C. reinhardtii. These results failed to support the hypothesis that the CO2/O2 ratio plays any role in signaling for the up-regulation of limiting CO2-induced genes and (or) of the CO2-concentrating mechanism (CCM). The mRNA abundance of the Cah1 and Gdh genes appeared to be regulated in concert, suggesting co-regulation by the same signaling pathway, which, because of a lack of an O2 effect, seems unlikely to involve photorespiration or a photorespiratory metabolite. Instead, it appeared that the CO2 concentration alone was responsible for regulation of limiting CO2 acclimation responses. Based on growth, photosynthesis, and gene expression characteristics, three distinct CO2-regulated physiological states were recognized within the studied parameters, a high CO2 (5%–0.5%) state, a low CO2 (0.4%–0.03%) state, and a very low CO2 (0.01%–0.005%) state. Induction of Cah1 expression and Gdh up-regulation occurred at a CO2 concentration between 0.5% and 0.4% CO2, delineating the high from the low CO2 states. Photosynthetic characteristics also were distinct in the three CO2-regulated physiological states, e.g., the estimated K0.5(CO2) of the high CO2, low CO2, and very low CO2 states were 72, 10, and 0.9 µmol·L–1 CO2, respectively. In addition to a greater photosynthetic CO2 affinity, the very low CO2 state could be distinguished from the low CO2 state by an increased cell-doubling time and a smaller cell size.Key words: algae, Chlamydomonas, CO2, gene expression, induction, photorespiration, photosynthesis.