Physiological and Molecular Aspects of the Inorganic Carbon-Concentrating Mechanism in Cyanobacteria

Abstract

This paper reviews progress made in elucidating the inorganic carbon concentrating mechanism in cyanobacteria at the physiological and molecular levels. Emphasis is placed on the mechanism of inorganic carbon transport, physiological and genetical analysis of high-CO2-requiring mutants, the polypeptides induced during adaptation to low C02, the functional significance of carboxysomes, and the role of carbonic anhydrase. We also make occasional reference to the green algal inorganic carbon-concentrating mechanism.Many photosynthetic microorganisms possess a mechanism for active intracellular accumulation of CQ2 that enables them to compensate for the 5-to 20-fold difference (in green algae and cyanobacteria, respectively) between the CO2 concentration in their environment and the Km(CO2) of their Rubisco. The activity of the Q-concentrating mechanism increases during adaptation from high to low external CO2 concentrations, one of a syndrome of changes that lead to an elevated apparent photosynthetic affinity for extracellular Ci. This review focuses on certain aspects of the Ci-concentrating system currently under active investigation. Although rigid limitation of space obliges us to confine ourselves largely to cyanobacteria, we also occasionally refer to green algae in cases in which progress has recently been made relevant to the topic discussed (for earlier reviews, see refs. 1,2,7,[13][14][15]20). MECHANISM OF C, UPTAKEThe intracellular level of CQ, at the steady-state of photosynthesis, is considerably higher than could be accounted for by the passive equilibration of CO2 and HCO3-across the cell membrane, indicating active transport (2,13,15 Nae requirement for HC03-uptake (see below) suggests that uptake might be a secondary active Na+ symport, driven by a transmembrane Na+ gradient established by a Nae extrusion pump. Alternatively, particularly at pH values below 7.0, proton symport driven by the protonmotive force generated by the HI pump could be envisaged, although this would demand a stoichiometry greater than 1:1 (12, 13).A role for Na+ in the Ci uptake mechanism was suggested by its highly specific effect on apparent photosynthetic affinity for external CQ and on the Km(HCO3-) of the Ci transport system (12, 13, 15). The effect of Na+ is far larger in the case of HCO3-than is CO2 uptake, but only micromolar Na+ concentrations are required to achieve the maximal effect on CO2 uptake; millimolar Na+ concentrations are required in the case of HCO3- (12,15). For some as yet unknown reason, HCO3 uptake in nonaerated cultures ofSynechococcus is not Nae dependent (15). Three alternative models to account for the Nae effect on HC03-uptake have been considered, but ithas not yet proved possible to distinguish among them experimentally (12

Tetraphenylphosphonium cation (TPP+) is not a reliable membrane potential probe in the cyanobacterium Synechococcus R‐2 PCC 7942

“…This result is consistent with similar findings using the )'Rb+\valinomycin method (Ritchie et al, 1996). Transient hyperpolarization, based upon the use of lipophilic cation probes, has also been reported after inorganic carbon has been added to blue-green algal cells (Kaplan et al, 1982 ;Miller et al, 1984 ;Zenvirth et al, 1984 ;Kaplan et al, 1989 ;Miller et al, 1990 ;Kaplan et al, 1991). Chlorophyll fluorescence changes in response to added HCO $ − have also been interpreted as reflecting hyperpolarization of the membrane (Miller & Canvin, 1987 ;Miller et al, 1988).…”

“…Many of the reported membrane potential determinations for blue-green algae are based solely on the use of lipophilic cation probes (Kaplan et al, 1980 ;Reed et al, 1980 ;Zdrou & Tromballa, 1981 ;Kaplan et al, 1982 ;Miller et al, 1984 ;Reinhold et al, 1984 ;Zenvirth et al, 1984 ;Kaplan, 1985 ;Peschek et al, 1985 ;Budd & Kerson, 1987 ;Kaplan et al, 1989Kaplan et al, , 1991. Some of the above studies did not take proper account of the extensive binding of lipophilic cations to the surfaces of cells and so their estimates of the membrane potential are inaccurate.…”

A periplasmic, α-type carbonic anhydrase from Rhodopseudomonas palustris is essential for bicarbonate uptake

“…In plants, intracellular CA enhances the rate of CO # to HCO − $ conversion, for fixation by phosphoenolpyruvate carboxylase . CA has been proposed to be involved in C i utilization in most anaerobic bacteria and archaea (Alber & Ferry, 1994 ;Kaplan et al, 1991). CA function in processes other than C i utilization has also been verified in several bacteria.…”

Phenotypic Complementation of High CO2-Requiring Mutants of the Cyanobacterium Synechococcus sp. Strain PCC 7942 by Inosine 5′-Monophosphate

“…Modification of several sites within the genomic region of rbc in Synechococcus PCC 7942, including rbcS, resulted in high C02-requiring mutants (9,13,20). It was, therefore, suggested that this region contains a cluster of genes, the products of which are involved in various functions of the Ci-concentrating mechanism and, hence, in the ability of cyanobacteria to grow in the presence of low CO2.…”

“…When transferred from high-to low-CO2 conditions, the cells undergo an adaptation process that includes the induction of a Ci-concentrating mechanism. As a consequence of this increase in the ability to accumulate Ci internally, the apparent photosynthetic affinity for extemal Ci is 10-to 20-fold higher in low than in high C02-grown cells (1,3,8,9,14,18 Cultures of Synechococcus sp. strain PCC 7942 and the mutants obtained following modifications of this strain were grown in the presence of high (5% C02 in air) or low (air) levels of C02 as previously described (12).…”