The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae

Abstract

Eukaryotic microalgae have developed CO2concentrating mechanisms to maximise the concentration of CO2 at the active site of Rubisco in response to the low CO2 concentrations in the external aquatic medium. In these organisms, the modes of inorganic carbon (Ci) uptake are diverse, ranging from diffusive CO2 uptake to the active transport of HCO3 -and CO2 and many have an external carbonic anhydrase to facilitate HCO3- use. There is unequivocal evidence for the mechanisms of Ci uptake in only about 25 species of microalgae of the chlorophyte, haptophyte, rhodophyte, diatom, and eustigmatophyte groups. Most of these species take up both CO2 and HCO3-, but the rates of uptake of each of these substrates varies with the algal species. A few species take up only one of the two forms of Ci, an adaptation that is not necessarily correlated with their ecological distribution. Evidence is presented for the active uptake of HCO3- and CO2 in two marine haptophytes,Isochrysis galbana Parke and Dicrateria inornata Parke, and for active transport of CO2 but lack of HCO3- uptake in two marine dinoflagellates, Amphidinium carteraeHulburt and Heterocapsa oceanica Stein.

Characterization of diurnal photosynthetic rhythms in the marine diatom Skeletonema costatum grown in synchronous culture under ambient and elevated CO2

“…The α and F v /F m increased with increasing CO 2 , indicating that the efficiency of light-harvesting and energy conversion in photosynthesis were increased. Down-regulation of Rubisco and inorganic carbon concentrating mechanisms (CCM) activities has been reported in many species (Wong 1979;Vu et al 1983;Bowes 1993;Colman 2002;Matsuda et al 2002). The present study indicated that the apparent carboxylating efficiency and the photosynthetic affinity for CO 2 markedly decreased under elevated CO 2 in S. costatum, suggesting that the similar down-regulation of Rubisco and CCM activities may also exist in this alga.…”

“…The photosynthetic affinity for CO 2 and carbonic anhydrase activity in many microalgae declines with CO 2 enrichment (Bowes 1993;Matsuda et al . 2002;Colman et al . 2002).…”

Evidence for a plasmalemma-based CO2 concentrating mechanism in Laminaria saccharina

“…The subcellular location and function of these components have been extensively studied in cyanobacteria and microalgae (see Colman et al 2002 andBadger 2003, for recent reviews). In all cases, internal carbonic anhydrase (CA) seems to be an essential component of the CCMs.…”

The evolution of inorganic carbon concentrating mechanisms in photosynthesis

“…(c) Algae There is apparently greater diversity of CCMs in algae than in cyanobacteria (table 1c-g,i ) and less is known about the mechanisms and molecular genetics of the CCMs (Badger et al 1998;Colman et al 2002;Giordano et al 2005). Pyrenoids, which are within the chloroplast stroma and contain rubisco, occur in many algae expressing CCMs.…”

“…CCMs occur today in all the cyanobacteria examined, in all algae apart from a few members of the Chlorophyta and Rhodophyta as well as most or all members of the Chrysophyceae and Synurophyceae, as well as in some hornworts, lycopsids and ferns, and in a significant number of flowering plants ( Winter & Smith 1995;Badger et al 1998Badger et al , 2002Sage & Monson 1998;Colman et al 2002;Keeley & Rundel 2003;Price & Badger 2003;Edwards et al 2004;Giordano et al 2005;Raven et al 2005a-c;Price et al 2007;Roberts et al 2007a,b; (b) Cyanobacteria In cyanobacteria, the CCM is based on accumulation of HCO K 3 in the cytosol (table 1a,b), movement of this HCO K 3 through their proteinaceous shells into the carboxysomes containing rubisco, and conversion to CO 2 using one or more carbonic anhydrase (CA) enzymes (Badger et al 2002;Price et al 2007). The open ocean cyanobacteria with form IA rubiscos have a restricted suite of HCO K 3 accumulation processes and, probably, little capacity to acclimatize to decreased inorganic C availability (an unlikely event in the pelagic ocean).…”