Proposed Carbon Dioxide Concentrating Mechanism in Chlamydomonas reinhardtii

Abstract

Aquatic photosynthetic microorganisms account for almost 50% of the world's photosynthesis (19). These organisms face several challenges in acquiring CO 2 from the environment. The first challenge is presented by the properties of ribulose bisphosphate carboxylase-oxygenase (Rubisco). Rubisco is an unusually slow enzyme with a low affinity for CO 2 . At atmospheric levels of CO 2 , Rubisco can function at only about 25% of its catalytic capacity because the concentration of dissolved CO 2 is less than the K m (CO 2 ) of Rubisco and due to the relatively high concentration of O 2 which competes with CO 2 . A second challenge these organisms face is that the diffusion of CO 2 in an aqueous solution is 10,000 times slower than the diffusion of CO 2 in air. Thus, the ability to scavenge CO 2 as quickly as it becomes available is highly advantageous to aquatic photosynthetic organisms. Third, algae often experience significant fluctuations in inorganic carbon (C i ϭ CO 2 ϩ HCO 3 Ϫ ) levels and pH, which change the availability of CO 2 and HCO 3 Ϫ for photosynthesis. At an acidic pH, the vast majority of C i is in the form of CO 2 , while at an alkaline pH,

To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms

“…While there are undoubtedly some CCM systems which function in the absence of a pyrenoid (Raven 1997a,b;Raven et al 2008), we contend that the majority of the significant aquatic global carbon fixation mediated by noncyanobacterial microbes (Raven et al 2008) is mediated by a pyrenoid-based CCM. To date, there are no candidate genes, proteins or specific structures which are thought to comprise a pyrenoid, other than the associated starch sheath (Izumo et al 2007), and internal pyrenoid complement of rubisco (Lacoste-Royal & Gibbs 1987;Vaughn et al 1990;Borkhsenious et al 1998), rubisco activase (McKay et al 1991), nitrate reductase (Okabe & Okada 1990), Calvin cycle enzymes, photosystem I and lumenal carbonic anhydrase-enriched trans-thylakoid lamellae (Villarejo et al 1998;Moroney & Ynalvez 2007). While we are currently undertaking work on a pyrenoid proteome and also investigating the relationship between rubisco structure and function in the chloroplast pyrenoid, our closest guess to the normal pyrenoid structure is some type of aggregation mechanism associated with rubisco, which may be related either to rubisco holoenzyme amino acid residue interactions or some additional plastoskeleton structures.…”

Functional Hybrid Rubisco Enzymes with Plant Small Subunits and Algal Large Subunits

“…Analysis of the Chloroplast Pyrenoid-We wondered whether the poor photosynthetic growth of the SSSO, SSAT, and SSHA hybrid enzyme mutants may result from a loss of the CCM (10). Chlamydomonas mutants that lack the CCM grow poorly, if at all, at air levels of CO 2 but are indistinguishable from wild type with regard to photosynthetic growth at elevated CO 2 , which is a condition when the CCM is normally repressed (74,75).…”

Thylakoid Lumen Carbonic Anhydrase (CAH3) Mutation Suppresses Air-Dier Phenotype of LCIB Mutant in Chlamydomonas reinhardtii

“…Both suppressors have lesions in CAH3, encoding a thylakoid-lumen-located, a-type carbonic anhydrase. The requirement of a thylakoidal CA and an acidic compartment in a functional CCM was first suggested by Pronina and colleagues, and later CAH3 was identified and proposed to catalyze the rapid conversion of HCO 3 2 to CO 2 in the acidic thylakoid lumen, with the CO 2 then diffusing to the pyrenoid to supply elevated substrate CO 2 concentrations for Rubisco (Pronina et al, 1981;Pronina and Semenenko, 1990;Funke et al, 1997;Raven, 1997;Karlsson et al, 1998;Hanson et al, 2003;Moroney and Ynalvez, 2007). Consistent with previous reports (Spalding et al, 1983a;Moroney et al, 1987), the L-CO 2 -acclimated CAH3 single mutant wtsu6, generated in a cross between the suppressed line and wild type, accumulated a very high internal Ci concentration but was unable to use Ci efficiently for photosynthesis.…”

“…Terrestrial C 4 plants have developed a CO 2 -concentrating mechanism (CCM) involving anatomical and biochemical adaptations to accumulate a higher concentration of CO 2 as substrate Rubisco and to suppress oxygenation of ribulose-1,5-bisP, a wasteful side reaction. In contrast, a different type of CCM is induced in the unicellular green microalga Chlamydomonas reinhardtii when the supply of dissolved inorganic carbon (Ci; CO 2 and HCO 3 2 ) for photosynthesis is limited (Beardall and Giordano, 2002;Giordano et al, 2005;Moroney and Ynalvez, 2007;Spalding, 2008). In response to limiting CO 2 , the CCM uses active Ci transport, both at the plasma membrane and the chloroplast envelope, to accumulate a high concentration of HCO 3 2 within the chloroplast (Palmqvist et al, 1988;Sü ltemeyer et al, 1988).…”