Modeling and mutagenesis of amino acid residues critical for CO2 hydration by specialized NDH-1 complexes in cyanobacteria

Artier, Juliana; Walker, Ross; Miller, Neil T.; Zhang, Minquan; Price, G. Dean; Burnap, Robert L.

doi:10.1016/j.bbabio.2021.148503

Cited by 9 publications

(23 citation statements)

References 47 publications

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“…In contrast, the H89A substitution greatly restored the affinity for CO2 (K0.5 ~175 μM). Similarly, the Gln substitution only modestly affected CO2 uptake affinity in agreement with previous results [29].…”

Section: Cupb-h89 Plays a Catalytic Role In Co2-uptakesupporting

confidence: 92%

“…Thus, it seems likely that some or all of these facets of chemical versatility cannot be fulfilled by the Lys side chain. In this regard, it is important to note that mutation of the second amino acid Zn 2+ ligand, CupB-H86, also prevents accumulation of the CupB protein, pointing to the criticality of Zn 2+ ion binding for the stabilization of the CupB structure and its interaction with the membrane portion of the complex [29]. Thus, it can be concluded that both the disruption of the Zn 2+ ligation and the interaction of CupB-E95 and R91 contribute to the accumulation of the CupB protein.…”

Section: The Arg-glu Dyad Critical For Cupb Stabilitymentioning

confidence: 99%

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Elucidating the Role of Primary and Secondary Sphere Zn²⁺Ligands in the Cyanobacterial CO₂Uptake Complex NDH-1₄: The Essentiality of Arginine in Zinc Coordination and Catalysis

Walker,

Zhang,

Burnap

2024

Preprint

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The uptake of inorganic carbon in cyanobacteria is facilitated by an energetically intensive CO2-concentrating mechanism (CCM). Specialized Type-1 NDH complexes function as a part of this mechanism to couple photosynthetic energy generated by redox reactions of the electron transport chain (ETC) to CO2hydration. This active site of CO2hydration incorporates an arginine side chain as a Zn ligand, diverging from the typical histidine and/or cysteine residues found in standard CAs. In this study, we focused on mutating three amino acids in the active site of the constitutively expressed NDH-14 CO2 hydration complex inSynechococcussp. PCC7942: CupB-R91, which acts as a zinc ligand, and CupB-E95 and CupB-H89, both of which are in close interaction with the arginine ligand. These mutations aimed to explore how they affect the unusual metal ligation by CupB-R91 and potentially influence the unusual catalytic process. The most severe defects in activity among the targeted residues are due to a substitution of CupB-R91 and the ionically interacting E95 since both proved essential for the structural stability of the CupB protein. On the other hand, CupB-H89 mutations show a range of catalytic phenotypes indicating a role of this residue in the catalytic mechanism of CO2-hydration, but no evidence was obtained for aberrant carbonic anhydrase activity that would have indicated uncoupling of the CO2-hydration activity from proton pumping. The results are discussed in terms of possible alternative CO2hydration mechanisms.

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Section: Cupb-h89 Plays a Catalytic Role In Co2-uptakesupporting

confidence: 92%

Section: The Arg-glu Dyad Critical For Cupb Stabilitymentioning

confidence: 99%

Elucidating the Role of Primary and Secondary Sphere Zn²⁺Ligands in the Cyanobacterial CO₂Uptake Complex NDH-1₄: The Essentiality of Arginine in Zinc Coordination and Catalysis

Walker,

Zhang,

Burnap

2024

Preprint

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“…It is thought that NDH-1 3/4 converts CO 2 entering the cells into HCO 3 − due to the CA activity of their unique (in comparison with other NDH-1 complexes in cyanobacteria) constituent proteins, CupA/B, which are also known as ChpY/X [ 149 , 150 , 154 ]. Although the CA specific activity of CupA/B has not been confirmed experimentally, this hypothesis was well supported by the computer simulations as well as by a number of indirect data [ 154 , 155 , 156 , 157 ]. Two alternative hypotheses have been proposed regarding the functioning of NDH-1 3/4 complexes.…”

Section: Ccm Of Cyanobacteriamentioning

confidence: 98%

Adapting from Low to High: An Update to CO2-Concentrating Mechanisms of Cyanobacteria and Microalgae

Kupriyanova

Пронина

Los

2023

Plants

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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.

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“…to convert CO 2 to HCO 3 À in the cytoplasm, thus increasing the net influx of CO 2 and minimizing the efflux of CO 2 (Price et al 2002;Han et al 2017;Schuller et al 2020;Artier et al 2022). Both specialized NDH complexes contain a carbonic anhydrase-like protein (Shibata et al 2001): CupA is associated with the NDH-1 3 complex and CupB with the NDH-1 4 complex (Zhang et al 2004;Xu et al 2008b;Han et al 2017).…”

Section: Carbon Concentrating Mechanismsmentioning

confidence: 99%

“…No carbonic anhydrase has been detected in the cytoplasm of cyanobacteria, and contrary to the original expectations, expressing carbonic anhydrase in the cytoplasm leads to a high CO 2 requiring phenotype, further indicating that in the cytoplasm, bicarbonate concentration is high (Price and Badger 1989). Instead of carbonic anhydrase, two specialized NDH complexes, an inducible NDH‐1 3 (NDH‐1MS) and a constitutively expressed NDH‐1 4 (NDH‐1MS’) complex have been suggested to convert CO 2 to HCO 3 − in the cytoplasm, thus increasing the net influx of CO 2 and minimizing the efflux of CO 2 (Price et al 2002; Han et al 2017; Schuller et al 2020; Artier et al 2022). Both specialized NDH complexes contain a carbonic anhydrase‐like protein (Shibata et al 2001): CupA is associated with the NDH‐1 3 complex and CupB with the NDH‐1 4 complex (Zhang et al 2004; Xu et al 2008b; Han et al 2017).…”

Section: Carbon Concentrating Mechanismsmentioning

confidence: 99%

Inorganic carbon sensing and signalling in cyanobacteria

Kurkela,

Tyystjärvi

2024

Physiologia Plantarum

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Cyanobacteria utilize CO2 and HCO3− 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‐13 and NDH‐14, which convert CO2 to HCO3− 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 CO2 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.

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Modeling and mutagenesis of amino acid residues critical for CO2 hydration by specialized NDH-1 complexes in cyanobacteria

Cited by 9 publications

References 47 publications

Elucidating the Role of Primary and Secondary Sphere Zn²⁺Ligands in the Cyanobacterial CO₂Uptake Complex NDH-1₄: The Essentiality of Arginine in Zinc Coordination and Catalysis

Elucidating the Role of Primary and Secondary Sphere Zn²⁺Ligands in the Cyanobacterial CO₂Uptake Complex NDH-1₄: The Essentiality of Arginine in Zinc Coordination and Catalysis

Adapting from Low to High: An Update to CO2-Concentrating Mechanisms of Cyanobacteria and Microalgae

Inorganic carbon sensing and signalling in cyanobacteria

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Modeling and mutagenesis of amino acid residues critical for CO2 hydration by specialized NDH-1 complexes in cyanobacteria

Cited by 9 publications

References 47 publications

Elucidating the Role of Primary and Secondary Sphere Zn2+Ligands in the Cyanobacterial CO2Uptake Complex NDH-14: The Essentiality of Arginine in Zinc Coordination and Catalysis

Elucidating the Role of Primary and Secondary Sphere Zn2+Ligands in the Cyanobacterial CO2Uptake Complex NDH-14: The Essentiality of Arginine in Zinc Coordination and Catalysis

Adapting from Low to High: An Update to CO2-Concentrating Mechanisms of Cyanobacteria and Microalgae

Inorganic carbon sensing and signalling in cyanobacteria

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Product

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Elucidating the Role of Primary and Secondary Sphere Zn²⁺Ligands in the Cyanobacterial CO₂Uptake Complex NDH-1₄: The Essentiality of Arginine in Zinc Coordination and Catalysis

Elucidating the Role of Primary and Secondary Sphere Zn²⁺Ligands in the Cyanobacterial CO₂Uptake Complex NDH-1₄: The Essentiality of Arginine in Zinc Coordination and Catalysis