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(a, b) Effect of light intensity on the quantum yield of photosystem II (yield(II)) (a) and the redox state of primary plastoquinone, QA (b), in the Synechocystis wild‐type (WT) and ::ecaB. The actinic light intensity was 100 μmol photons m⁻² s⁻¹. The culture containing 0.2 mM inorganic carbon (Ci) was directly used for the measurement. GL, cultured at growth light (40 μmol photons m⁻² s⁻¹); HL, cultured at high light (200 μmol photons m⁻² s⁻¹). The parameters were calculated from the fluorescence parameters of WT and ::ecaB grown at various pH values. Asterisks indicate significant differences in (b) (t‐test; **, P < 0.01). PAR, photosynthetically active radiation.
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Carbonic anhydrases (CAs) are involved in CO2 uptake and conversion, a fundamental process in photosynthetic organisms. Nevertheless, the mechanism underlying the regulation of CO2 uptake and intracellular conversion in cyanobacteria is largely unknown.
We report the characterization of a previously unrecognized thylakoid‐located CA Slr0051 (EcaB)...
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Citations
... The CCM provides algae with an additional ecological advantage as it allows both CO 2 and HCO 3 − to be efficiently exploited by carbonic anhydrases (CAs), which significantly contribute to the transformation of CO 2 [57]. CAs are found in the archaea Methanosarcina [58,59], yeasts [60], microalgae and Cyanobacteria [61][62][63][64][65][66][67], diatom algae [68], and fungi [69][70][71]. Chloroplast stroma, mitochondria, periplasmic space, and chloroplast thylakoid lumens of eukaryotic algae have all been found to contain CAs [55]. ...
Recent studies actively debate oxic methane (CH4) production processes in water and terrestrial ecosystems. This previously unknown source of CH4 on a regional and global scale has the potential to alter our understanding of climate-driving processes in vulnerable ecosystems, particularly high-latitude ecosystems. Thus, the main objective of this study is to use the incubation approach to explore possible greenhouse gas (GHG) fluxes by the most widely distributed species of epiphytic lichens (ELs; Evernia mesomorpha Nyl. and Bryoria simplicior (Vain.) Brodo et D. Hawksw.) in the permafrost zone of Central Siberia. We observed CH4 production by hydrated (50%–400% of thallus water content) ELs during 2 h incubation under illumination. Moreover, in agreement with other studies, we found evidence that oxic CH4 production by Els is linked to the CO2 photoassimilation process, and the EL thallus water content regulates that relationship. Although the GHG fluxes presented here were obtained under a controlled environment and are probably not representative of actual emissions in the field, more research is needed to fully comprehend ELs’ function in the C cycle. This particular research provides a solid foundation for future studies into the role of ELs in the C cycle of permafrost forest ecosystems under ongoing climate change (as non-methanogenesis processes in oxic environments).
... Cyanobacteria possesses three types of CAs: α, β, and γ. In model freshwater and marine species, these enzymes are found in carboxysomes, associated with thylakoid membranes, or in the cell's outer layers external to the cytoplasmic membrane (CM) [2][3][4][5][6]. ...
... The physiological significance of cyanobacterial intracellular (carboxysomal and thylakoid) CAs is determined by their involvement in the operation of the CO 2 -concentrating mechanism (CCM), which enhances photosynthetic carbon fixation efficiency in the Calvin cycle [5,7,8]. The intracellular pool of HCO 3 − in CCM is formed with the participation of (1) three bicarbonate transporters-BCT1 (bicarbonate transporter 1), SbtA (sodiumbicarbonate transporter A), and BicA (bicarbonate transporter A), and (2) two CO 2 uptake systems (NDH-1 3/4 ) that represent special modification of NADPH dehydrogenase (NDH-1) complexes [9]. ...
... The intracellular pool of HCO 3 − in CCM is formed with the participation of (1) three bicarbonate transporters-BCT1 (bicarbonate transporter 1), SbtA (sodiumbicarbonate transporter A), and BicA (bicarbonate transporter A), and (2) two CO 2 uptake systems (NDH-1 3/4 ) that represent special modification of NADPH dehydrogenase (NDH-1) complexes [9]. Sun et al. [5] suggested that the thylakoid form of β-CA EcaB has a role in NDH-1 3/4 function. HCO 3 − , which accumulates in the cytoplasm, is transformed Table 1. ...
Under standard laboratory conditions, Synechococcus elongatus PCC 7942 lacks EcaASyn, a periplasmic carbonic anhydrase (CA). In this study, a S. elongatus transformant was created that expressed the homologous EcaACya from Cyanothece sp. ATCC 51142. This additional external CA had no discernible effect on the adaptive responses and physiology of cells exposed to changes similar to those found in S. elongatus natural habitats, such as fluctuating CO2 and HCO3− concentrations and ratios, oxidative or light stress, and high CO2. The transformant had a disadvantage over wild-type cells under certain conditions (Na+ depletion, a reduction in CO2). S. elongatus cells lacked their own EcaASyn in all experimental conditions. The results suggest the presence in S. elongatus of mechanisms that limit the appearance of EcaASyn in the periplasm. For the first time, we offer data on the expression pattern of CCM-associated genes during S. elongatus adaptation to CO2 replacement with HCO3−, as well as cell transfer to high CO2 levels (up to 100%). An increase in CO2 concentration coincides with the suppression of the NDH-14 system, which was previously thought to function constitutively.
... Recently, the NDH-1 3 complex was shown to utilize a redox-driven proton-pumping system and a CO 2 channel to convert CO 2 to HCO 3 À (Schuller et al. 2020). A carbonic anhydrase-like protein, EcaB, has been shown to interact with CupA and CupB subunits and was suggested to regulate the conversion of CO 2 to HCO 3 À by the NDH-1 3 and NDH-1 4 complexes (Sun et al. 2019a). ...
Cyanobacteria utilize CO 2 and HCO 3 ⁻ as inorganic carbon (Ci) sources. In low Ci, like in ambient air, cyanobacteria efficiently collect Ci using a carbon concentrating mechanism (CCM). The CCM includes bicarbonate transporters SbtA, BicA and BCT1; the specialized NDH complexes NDH‐1 3 and NDH‐1 4 , which convert CO 2 to HCO 3 ⁻ in the cytoplasm; and carboxysomes that are protein shell encapsulated ribulose‐1,5‐bisphosphate carboxylase/oxygenase (RuBisCo) and carbonic anhydrase containing bodies in which the first reaction of carbon fixation occurs. Ci‐dependent regulation of bicarbonate transporters and specialized NDH complexes, especially the regulation of the SbtA transporter, are well understood. CcmR (also called NdhR), CyAbrB2, CmpR and RbcR act as transcription factors regulating CCM genes. Ci signalling molecules detecting the metabolic status of the cells include 2‐oxoglutarate, which accumulates when the Ci/nitrogen ratio of the cell is high, and 2‐phosphoglycolate, the first intermediate of the photorespiration pathway, whose accumulation indicates low Ci. These signalling molecules act as corepressors and coactivators of the CcmR repressor protein, whereas 2‐phosphoglycolate and ribulose‐1,5‐bisphosphate activate transcription activator CmpR. In addition, bicarbonate or CO 2 activates the adenylyl cyclase that produces cAMP, and ATP/ADP/AMP provide information about the energy status of the cell. Less is known about the molecular mechanisms regulating carboxysome dynamics or how production, activity and degradation of photosynthetic complexes are regulated by prevailing Ci conditions or which mechanisms adjust cell division according to Ci. This minireview summarizes the present knowledge about molecular mechanisms regulating cyanobacterial acclimation to prevailing Ci.
... The carbonic anhydrases in the periplasm (external CA, eCA) and the chloroplast (internal CA, iCA) are both responsible for the regulation of the balance between CO 2 and HCO 3 − in total DIC [32][33][34] . It is known that the membrane-impermeable AZA inhibitor targets on the inhibition of periplasmic eCA 35 . While the membranepermeable EZA inhibitor targets on both eCA and iCA as it is a kind of comprehensive inhibitor to CCM 36 . ...
The CO2 concentration at ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) is crucial to improve photosynthetic efficiency for biomass yield. However, how to concentrate and transport atmospheric CO2 towards the Rubisco carboxylation is a big challenge. Herein, we report the self-assembly of metal-organic frameworks (MOFs) on the surface of the green alga Chlorella pyrenoidosa that can greatly enhance the photosynthetic carbon fixation. The chemical CO2 concentrating approach improves the apparent photo conversion efficiency to about 1.9 folds, which is up to 9.8% in ambient air from an intrinsic 5.1%. We find that the efficient carbon fixation lies in the conversion of the captured CO2 to the transportable HCO3⁻ species at bio-organic interface. This work demonstrates a chemical approach of concentrating atmospheric CO2 for enhancing biomass yield of photosynthesis.
... Highaffinity C i uptake systems (NDH-1 3 , SbtA and BCT1) are primarily responsible for the operation of the induced CCM [5], ensuring the accumulation of the intracellular HCO 3 − pool. In addition, the increased level of the thylakoid β-CA, EcaB, is recorded under these conditions [115]. This occurrence is explained by the involvement of EcaB in the operation of the NDH-1 3 complex. ...
... Two alternative hypotheses have been proposed regarding the functioning of NDH-1 3/4 complexes. Their fundamental difference lies in the assumption of whether the CO 2 substrate is supplied to the CupA/B active centers: (a) from the cytoplasm [115] or (b) from the thylakoid lumen [158]. It has also been suggested that the CA activity of NDH-1 3/4 may be maintained or regulated by β-CA and EcaB, whose specific activity and interaction with CupA/B proteins have been demonstrated [115]. ...
... Their fundamental difference lies in the assumption of whether the CO 2 substrate is supplied to the CupA/B active centers: (a) from the cytoplasm [115] or (b) from the thylakoid lumen [158]. It has also been suggested that the CA activity of NDH-1 3/4 may be maintained or regulated by β-CA and EcaB, whose specific activity and interaction with CupA/B proteins have been demonstrated [115]. ...
The intracellular accumulation of inorganic carbon (Ci) by microalgae and cyanobacteria under ambient atmospheric CO2 levels was first documented in the 80s of the 20th Century. Hence, a third variety of the CO2-concentrating mechanism (CCM), acting in aquatic photoautotrophs with the C3 photosynthetic pathway, was revealed in addition to the then-known schemes of CCM, functioning in CAM and C4 higher plants. Despite the low affinity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) of microalgae and cyanobacteria for the CO2 substrate and low CO2/O2 specificity, CCM allows them to perform efficient CO2 fixation in the reductive pentose phosphate (RPP) cycle. CCM is based on the coordinated operation of strategically located carbonic anhydrases and CO2/HCO3− uptake systems. This cooperation enables the intracellular accumulation of HCO3−, which is then employed to generate a high concentration of CO2 molecules in the vicinity of Rubisco’s active centers compensating up for the shortcomings of enzyme features. CCM functions as an add-on to the RPP cycle while also acting as an important regulatory link in the interaction of dark and light reactions of photosynthesis. This review summarizes recent advances in the study of CCM molecular and cellular organization in microalgae and cyanobacteria, as well as the fundamental principles of its functioning and regulation.
... To our knowledge, susceptibility of Synechocystis CcaA to inhibitors has not been investigated in detail so far but recombinant CcaA is enzymatically active [7,11], and AZA-tolerant Synechocystis mutants have been described and hypothesized to harbour mutations in CA [45], even prior to the initial cloning of the ccaA gene [10]. Moreover, the high level of homology between CcaA and CahB1 (Figure 1; [26]), and the fact that CcaA is the only essential CA identified in Synechocystis so far [16,23], strongly suggest that CcaA would also be susceptible to AZA inhibition. Thus, the P I fraction is considered to likely contain enriched and intact carboxysomes with whom active CahB1 enzyme co-precipitates in both WT + cahB1 and ∆ccaA + cahB1 (Figure 3c). ...
Cyanobacteria mostly rely on the active uptake of hydrated CO2 (i.e., bicarbonate ions) from the surrounding media to fuel their inorganic carbon assimilation. The dehydration of bicarbonate in close vicinity of RuBisCO is achieved through the activity of carboxysomal carbonic anhydrase (CA) enzymes. Simultaneously, many cyanobacterial genomes encode extracellular α- and β-class CAs (EcaA, EcaB) whose exact physiological role remains largely unknown. To date, the CahB1 enzyme of Sodalinema gerasimenkoae (formerly Microcoleus/Coleofasciculus chthonoplastes) remains the sole described active extracellular β-CA in cyanobacteria, but its molecular features strongly suggest it to be a carboxysomal rather than a secreted protein. Upon expression of CahB1 in Synechocystis sp.
PCC6803, we found that its expression complemented the loss of endogenous CcaA. Moreover, CahB1 was found to localize to a carboxysome-harboring and CA-active cell fraction. Our data suggest that CahB1 retains all crucial properties of a cellular carboxysomal CA and that the secretion mechanism and/or the machinations of the Sodalinema gerasimenkoae carboxysome are different from
those of Synechocystis.
... It is known that the membrane-impermeable AZ inhibitor targets on the inhibition of periplasmic eCA [33] . While the membrane-permeable EZ inhibitor targets on both eCA and iCA as it is a kind of comprehensive inhibitor to CCM [34] . Figure 4a exhibits the biomass growth curves of C. pyrenoidosa when MOF or CA inhibitors were added. ...
The CO 2 concentration at ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) is crucial to improve photosynthetic efficiency for biomass yield. However, how to concentrate and transport atmospheric CO 2 towards to the Rubisco carboxylation is a big challenge. Here in, we report the self-assembly of metal-organic frameworks (MOFs) on the surface of a microalgae that can greatly enhance the photosynthetic efficiency. The non-genetic concentrating CO 2 approach improved photosynthetic efficiency by about 2 folds, which is up to 7.5% in ambient air from an intrinsic 3.6%. We find that the efficient carbon fixation lies in the conversion of the captured CO 2 to the transportable HCO 3 ⁻ species at bio-organic interface. This work demonstrated a non-genetic approach of concentrating atmospheric CO 2 for enhancing biomass yield of photosynthesis.
... The intracellular carbon types in cytosol can be both CO 2 and HCO − 3 for most chlorophyte microalgae and eukaryotic microalgae, but carbon exists only with HCO − 3 type for cyanobacteria [75]. Such a difference is because there is no cytosolic CA in cyanobacteria, resulting in a slow conversion rate of HCO − 3 to CO 2 [76]. The cytosolic carbon is then transferred into the carboxysome, in which all carbons including CO 2 and HCO − 3 are converted into CO 2 form by the related CA [76]. ...
... Such a difference is because there is no cytosolic CA in cyanobacteria, resulting in a slow conversion rate of HCO − 3 to CO 2 [76]. The cytosolic carbon is then transferred into the carboxysome, in which all carbons including CO 2 and HCO − 3 are converted into CO 2 form by the related CA [76]. The elevated CO 2 concentration in carboxysomes caused by CCM strongly favors the carboxylase over oxygenase activity at RUBISCO active sites. ...
Microalgae biotechnology is a promising pathway to cope with CO2 emission and energy crisis due to high CO2 fixation rate and lipids productivity. However, bottlenecks of high energy cost, low photosynthetic efficiency and poor economic feasibility severely hinder its commercialization. Understanding process mechanisms of microalgae photosynthetic CO2 fixation and lipids production, and thus seeking possible regulations to enhance weak links are potential process regulation strategy for augmented competitiveness. Firstly, mass transfer and conversion processes of microalgae photosynthesis involving CO2 and light were comprehensively illuminated in this review. In detail, mechanisms of CO2 and light transfer in microalgae suspension, bioavailable carbon and photon assimilation by microalgae cells, as well as intracellular mass conversion were illustrated. Besides, synergistic effects of light and CO2 on microalgae photosynthesis were depicted from perspective of electrons and protons supply-demand relationships between photosynthetic photo-reaction and dark-reaction steps in chlorophyll. Possible weak links in these processes were emphasized to provide guideline for regulation. Secondly, available regulation strategies for CO2 and light mass transfer, cellular assimilation and intracellular conversion were summarized. Subsequently, economic and environmental impacts of process regulation on microalgae CO2 fixation and biodiesel output were evaluated to lit up large-scale applicability. Finally, challenges and future directions of microalgae biotechnology were described to inspire in-depth research and engineering practice. This review may provide a novel process regulation standpoint for operating microalgae-based CO2 fixation and biodiesel production in the most efficient manner, further facilitating the applicability of microalgae biotechnology towards carbon neutrality and biodiesel production.
... Our group found that the CO 2 uptake systems NDH-1MS and NDH-1MS' are associated with a carbonic anhydrase EcaB, which catalyzes the conversion of CO 2 into HCO − 3 in response to high pH values, high light, or low CO 2 concentrations, thereby helping to balance the redox state of inter photosystem electron carriers and maintain efficient photosynthesis (Sun et al., 2019). ...
Light reaction of photosynthesis is efficiently driven by protein complexes arranged in an orderly in the thylakoid membrane. As the 5th complex, NAD(P)H dehydrogenase complex (NDH-1) is involved in cyclic electron flow around photosystem I to protect plants against environmental stresses for efficient photosynthesis. In addition, two kinds of NDH-1 complexes participate in CO2 uptake for CO2 concentration in cyanobacteria. In recent years, great progress has been made in the understanding of the assembly and the structure of NDH-1. However, the regulatory mechanism of NDH-1 in photosynthesis remains largely unknown. Therefore, understanding the regulatory mechanism of NDH-1 is of great significance to reveal the mechanism of efficient photosynthesis. In this mini-review, the author introduces current progress in the research of cyanobacterial NDH-1. Finally, the author summarizes the possible regulatory mechanism of cyanobacterial NDH-1 in photosynthesis and discusses the research prospect.
... Ribulose bisphosphate carboxylase (RuBisCO) subunits, RbcS and RbcL, and structural proteins of carboxysome CcmK-N were less abundant under ATHC than under the ATLC conditions and clearly the least abundant under the LAH and MT trophic modes. Similarly, both carbonic anhydrases, the thylakoid-located EcaB (Sun et al., 2019) and CcaA, showed lower abundance under ATHC and even more so under MT and LAH. Importantly, enzymes of glycolate metabolism involved in photorespiration, particularly glyoxylate aminotransferase (Slr0006) (Eisenhut et al., 2008), showed downregulation under all the carbon-rich conditions compared to control ATLC. ...
Proteomes of an oxygenic photosynthetic cyanobacterium, Synechocystis sp. PCC 6803, were analyzed under photoautotrophic (low and high CO2, assigned as ATLC and ATHC), photomixotrophic (MT), and light-activated heterotrophic (LAH) conditions. Allocation of proteome mass fraction to seven sub-proteomes and differential expression of individual proteins were analyzed, paying particular attention to photosynthesis and carbon metabolism–centered sub-proteomes affected by the quality and quantity of the carbon source and light regime upon growth. A distinct common feature of the ATHC, MT, and LAH cultures was low abundance of inducible carbon-concentrating mechanisms and photorespiration-related enzymes, independent of the inorganic or organic carbon source. On the other hand, these cells accumulated a respiratory NAD(P)H dehydrogenase I (NDH-11) complex in the thylakoid membrane (TM). Additionally, in glucose-supplemented cultures, a distinct NDH-2 protein, NdbA, accumulated in the TM, while the plasma membrane-localized NdbC and terminal oxidase decreased in abundance in comparison to both AT conditions. Photosynthetic complexes were uniquely depleted under the LAH condition but accumulated under the ATHC condition. The MT proteome displayed several heterotrophic features typical of the LAH proteome, particularly including the high abundance of ribosome as well as amino acid and protein biosynthesis machinery-related components. It is also noteworthy that the two equally light-exposed ATHC and MT cultures allocated similar mass fractions of the total proteome to the seven distinct sub-proteomes. Unique trophic condition-specific expression patterns were likewise observed among individual proteins, including the accumulation of phosphate transporters and polyphosphate polymers storing energy surplus in highly energetic bonds under the MT condition and accumulation under the LAH condition of an enzyme catalyzing cyanophycin biosynthesis. It is concluded that the rigor of cell growth in the MT condition results, to a great extent, by combining photosynthetic activity with high intracellular inorganic carbon conditions created upon glucose breakdown and release of CO2, besides the direct utilization of glucose-derived carbon skeletons for growth. This combination provides the MT cultures with excellent conditions for growth that often exceeds that of mere ATHC.
