Acclimation of Chlamydomonas to changing carbon availability

Abstract

Aquatic organisms, including Chlamydomonas reinhardtii, are faced with a variable supply of dissolved inorganic carbon (Ci). Accordingly, C. reinhardtii has the ability to acclimate to the changing Ci supply through a variety of responses, including induction of a CO2 concentrating mechanism (CCM) when Ci is limiting. The CCM uses active Ci uptake to accumulate a high internal concentration of bicarbonate, which is dehydrated by a specific thylakoid carbonic anhydrase to supply CO2, the substrate used in photosynthesis. In addition to the changes demonstrably related to the function of the CCM, C. reinhardtii exhibits several other acclimation responses to limiting Ci, such as changes in cellular organization and induction or upregulation of several genes. A key area currently under investigation is how C. reinhardtii cells recognize the change in Ci or CO2 concentration, and transduce that signal into needed gene expression changes. Mutational analyses are proving very useful for learning more about the CCM and about the acclimation response to changes in Ci availability. Cloning of the gene disrupted in cia5, a mutant apparently unable to acclimate to limiting Ci, has opened opportunities for more rapid progress in understanding the signal transduction pathway. The Cia5 gene appears to encode a transcription factor that may control, either directly or indirectly, much of the gene expression responses to limiting Ci in C. reinhardtii. Several additional new mutants with potential defects in the signal transduction pathway have been isolated, including three new alleles of cia5.

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“…Furthermore, Ci uptake is higher in chloroplasts isolated from low-than from high-CO 2 -grown cells (8). Genes involved in Ci uptake by Chlamydomonas are strongly induced when high-CO 2 -grown cells are transferred to low-CO 2 conditions (12,13,19,20). Mutants in which these genes were impaired required high CO 2 for growth.…”

“…As opposed to CO 2 supply, there is far less information regarding the mechanism of HCO 3 Ϫ uptake in Chlamydomonas. Nevertheless, isolated chloroplasts of Chlamydomonas can accumulate HCO 3 Ϫ to levels higher than could be accounted for by passive diffusion (13). Furthermore, Ci uptake is higher in chloroplasts isolated from low-than from high-CO 2 -grown cells (8).…”

“…The organization of the carboxysomes in prokaryotes and the pyrenoids in eukaryotes, and the presence of membrane mechanisms for inorganic carbon (Ci) uptake, are central to the activity of the CO 2 -concentrating mechanism. The presence of multiple Ci-transporting systems in cyanobacteria has been indicated (17), but little is known about the mechanism of Ci uptake in eukaryotes, such as the green alga Chlamydomonas (13). As in most other photosynthetic organisms examined to date, Chlamydomonas can use either CO 2 or HCO 3 Ϫ or both (13).…”

“…The presence of multiple Ci-transporting systems in cyanobacteria has been indicated (17), but little is known about the mechanism of Ci uptake in eukaryotes, such as the green alga Chlamydomonas (13). As in most other photosynthetic organisms examined to date, Chlamydomonas can use either CO 2 or HCO 3 Ϫ or both (13). Kinetic data based on initial rates of transport are available for Ci uptake in some organisms but difficult to obtain for Chlamydomonas, because the steadystate internal Ci concentration is attained rapidly.…”

An inorganic carbon transport system responsible for acclimation specific to air levels of CO 2 in Chlamydomonas reinhardtii

“…Although initially identified as a probable Ci transport mutant, a recent study reported that the expression profiles of several CO 2 responsive genes in pmp1 differ from those in wild type and suggested that the Pmp1 gene product might regulate the expression of Ci transporter genes (14). Another recent observation regarding pmp1 is its unusual, air-dieing phenotype (15,16): it grows well in either high (5%) or very low (Ͻ200 ppm) CO 2 , but dies in low (air-level) CO 2 (350-450 ppm). This conspicuous phenotype distinguishes pmp1 from most other high CO 2 -requiring mutants and indicates the existence of multiple Ci transport systems in C. reinhardtii corresponding to multiple, CO 2 level-dependent acclimation states.…”