Oxidation potentials and electron donation to photosystem II of manganese complexes containing bicarbonate and carboxylate ligands

Kozlov, Yuri N.; Zharmukhamedov, Sergey K.; Tikhonov, K. G.; Dasgupta, Jyotishman; Kazakova, A.A.; Dismukes, G. Charles; Klimov, Vyacheslav V.

doi:10.1039/b406569g

Cited by 53 publications

(34 citation statements)

References 33 publications

(63 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Interestingly, O 2 evolution measurements indicate that the presence of bicarbonate anion enhances the rate of photoassembly [80]. This effect can be rationalized as carboxylate coordination of the Mn(H) ion is known to stabilize the corresponding Mn(II) → Mn(III) oxidation potential from 1.5 to 0.5 V when bound to PSII [81]. Conveniently, this new potential is well within the range of 1.1 V accessible by the photooxidized active-site tyrosyl radical ( ).…”

Section: Past Studiesmentioning

confidence: 99%

Multifrequency pulsed EPR studies of biologically relevant manganese(II) complexes

et al. 2007

View full text Add to dashboard Cite

Electron paramagnetic resonance studies at multiple frequencies (MF EPR) can provide detailed electronic structure descriptions of unpaired electrons in organic radicals, inorganic complexes, and metalloenzymes. Analysis of these properties aids in the assignment of the chemical environment surrounding the paramagnet and provides mechanistic insight into the chemical reactions in which these systems take part. Herein, we present results from pulsed EPR studies performed at three different frequencies (9, 31, and 130 GHz) on [Mn(II)(H 2 O) 6 ] 2+ , Mn(II) adducts with the nucleotides ATP and GMP, and the Mn(II)-bound form of the hammerhead ribozyme (MnHH). Through line shape analysis and interpretation of the zero-field splitting values derived from successful simulations of the corresponding continuous-wave and field-swept echodetected spectra, these data are used to exemplify the ability of the MF EPR approach in distinguishing the nature of the first ligand sphere. A survey of recent results from pulsed EPR, as well as pulsed electron-nuclear double resonance and electron spin echo envelope modulation spectroscopic studies applied to Mn(II)-dependent systems, is also presented. Mn-Containing Biological SystemsManganese operates as a cofactor in numerous proteins, serving both catalytic and structural roles [1][2][3][4]. Many Mn-dependent enzymes take advantage o f the rich redox chemistry available to the metal, accessing the +2, +3, +4, and perhaps even the +5 oxidation states during their turnover. For example, Mn-superoxide dismutase (MnSOD), which detoxifies the cell of the superoxide radical , cycles between the Mn(II) and Mn(III) oxidation states via the ping-pong type mechanism shown below [5][6][7][8][9].(1a) (1b) Other examples of such mononuclear redox-active enzymes include the manganese peroxidase responsible for lignin degradation by white-rot fungus [10][11][12]; a unique Mndependent form of lipoxygenase [13][14][15][16]; oxalate decarboxylase [17,18]; as well as an extradiol catechol dioxygenase [19][20][21]. NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptIn order to help minimize kinetic and thermodynamic penalties associated with electron transfer events and the execution of chemical reactions, two or more metal centers can be coupled together to provide active sites capable of conducting multiple electrons while still operating within a physiologically accessible range of reduction potentials [22]. Only three such examples of redox-active polynuclear Mn enzymes are known: Mn-catalase that disproportionates hydrogen peroxide [23][24][25][26]; a Mn form of ribonucleotide reductase (Mn-RNR) [27,28]; and, arguably the most recognized Mn-dependent enzyme, the photosynthetic core of green plants, algae, and certain cyanobacteria termed photosystem II (PSII) [29,30]. Through a series of photoinitiated electron transfer events, oxidizing equivalents are stored on the tetranuclear Mn core of PSII -the oxygen-evolving complex (OEC) -which then extracts four electr...

show abstract

Section: Past Studiesmentioning

confidence: 99%

Multifrequency pulsed EPR studies of biologically relevant manganese(II) complexes

et al. 2007

View full text Add to dashboard Cite

show abstract

“…However, no experimental evidence characterizing these subsequent intermediates is yet available. 1 and IM 1 *-Bicarbonate coordination of free Mn 2+ in water lowers the oxidation potential for photoconversion to Mn 3+ by a large amount (0.5-0.6 V vs. NHE) [91]. This thermodynamic stabilization is thought to be responsible for the increased stability of the Mn 3+ photoactivation intermediate that forms in the presence of bicarbonate, as seen by slowing of the recombination reaction that causes its decay [49].…”

Section: Trapping Assembly Intermediatesmentioning

confidence: 99%

Photoassembly of the water-oxidizing complex in photosystem II

Dasgupta

Ananyev

Dismukes

2008

Coordination Chemistry Reviews

166

121

View full text Add to dashboard Cite

The light-driven steps in the biogenesis and repair of the inorganic core comprising the O 2 -evolving center of oxygenic photosynthesis (photosystem II water-oxidation complex, PSII-WOC) are reviewed. These steps, known collectively as photoactivation, involve the photoassembly of the free inorganic cofactors to the cofactor-depleted PSII-(apo-WOC) driven by light and produce the active O 2 -evolving core comprised of Mn 4 CaO x Cl y . We focus on the functional role of the inorganic components as seen through the competition with non-native cofactors ("inorganic mutants") on water oxidation activity, the rate of the photoassembly reaction, and on structural insights gained from EPR spectroscopy of trapped intermediates formed in the initial steps of the assembly reaction. A chemical mechanism for the initial steps in photoactivation is given that is based on these data. Photoactivation experiments offer the powerful insights gained from replacement of the native cofactors, which together with the recent X-ray structural data for the resting holoenzyme provide a deeper understanding of the chemistry of water oxidation. We also review some new directions in research that photoactivation studies have inspired that look at the evolutionary history of this remarkable catalyst.

show abstract

“…The oxidation potential of Mn-bicarbonate complex (0.52-0.67 V ) is close to the midpoint redox potential of the primary electron donor in the RCs of anoxygenic bacteria (Kozlov et al 2004) and therefore it has been suggested (Dismukes et al 2001) that the capability of bicarbonate to form easily oxidizable complexes with manganese ions might be critical to the evolutional origin of the first O 2 -evolving cyanobacteria from a non-oxygenic bacterial precursor in the Archean period (O2.2 Gyr ago) when the concentration of bicarbonate dissolved in water was 30-30 000 times greater than today.…”

Section: Introductionmentioning

confidence: 99%

“…Changes in redox properties of manganese ions upon formation of complexes with bicarbonate evidently play a key role in the effect described above. In fact, upon the addition of NaHCO 3 to an aqueous solution of Mn 2C , the potential for oxidation of Mn 2C to Mn 3C was shifted from 1.18 to 0.52-0.68 V at pH 8.3 as a result of formation of bi(carbonate) complexes (Kozlov et al 1997(Kozlov et al , 2004Dasgupta et al 2006). Formation of Mn complex with carboxylates (formate, acetate) induced similar lowering of the oxidation potential; however, only bicarbonate stimulated the electron transfer from Mn 2C to PSII reaction centres (RCs; Kozlov et al 2004).…”

Section: Introductionmentioning

confidence: 99%

“…In fact, upon the addition of NaHCO 3 to an aqueous solution of Mn 2C , the potential for oxidation of Mn 2C to Mn 3C was shifted from 1.18 to 0.52-0.68 V at pH 8.3 as a result of formation of bi(carbonate) complexes (Kozlov et al 1997(Kozlov et al , 2004Dasgupta et al 2006). Formation of Mn complex with carboxylates (formate, acetate) induced similar lowering of the oxidation potential; however, only bicarbonate stimulated the electron transfer from Mn 2C to PSII reaction centres (RCs; Kozlov et al 2004). On the basis of the electrochemical and electron paramagnetic resonance (EPR) data, it was proposed that the unique capability of Mn 2C -bicarbonate complexes to be photooxidized by PSII could be due to four possible reasons: (i) significantly larger decrease in the oxidation potential of Mn 2C (down to 0.52 V ), (ii) electroneutrality of the functional electron transfer complex, (iii) the more favourable energetics reflected in the two pK a values for H 2 CO 3 /HCO 3 K and HCO 3 K / CO 3 2K and greater number of proton transfer sites, and (iv) multiple composition possibilities for the Mn 3C photoproduct such as Mn 3C (HCO 3 K ) 3 , Mn 3C (HCO 3 K )(CO 3 2K ) and Mn 3C (HCO 3 K ) 2 (OH K ) (due to the high Lewis acidity of Mn 3C ; pK a !1; Kozlov et al 2004;Dasgupta et al 2006).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Redox interaction of Mn–bicarbonate complexes with reaction centres of purple bacteria

Khorobrykh

Terentyev

Zharmukhamedov

et al. 2007

Phil. Trans. R. Soc. B

View full text Add to dashboard Cite

It is found that dark reduction of photooxidized primary electron donor P 870 C in reaction centres from purple anoxygenic bacteria (two non-sulphur Fe-oxidizing Rhodovulum iodosum and Rhodovulum robiginosum, Rhodobacter sphaeroides R-26 and sulphur alkaliphilic Thiorhodospira sibirica) is accelerated upon the addition of Mn 2C jointly with bicarbonate (30-75 mM). The effect is not observed if Mn 2C and HCO 3 K have been replaced by Mg 2C and HCO 2 K , respectively. The dependence of the effect on bicarbonate concentration suggests that formation of Mn 2C -bicarbonate complexes, Mn(HCO 3 ) C and/or Mn(HCO 3 ) 2 , is required for re-reduction of P 870 C with Mn 2C . The results are considered as experimental evidence for a hypothesis on possible participation of Mnbicarbonate complexes in the evolutionary origin of oxygenic photosynthesis in the Archean era.

show abstract

Oxidation potentials and electron donation to photosystem II of manganese complexes containing bicarbonate and carboxylate ligands

Cited by 53 publications

References 33 publications

Multifrequency pulsed EPR studies of biologically relevant manganese(II) complexes

Multifrequency pulsed EPR studies of biologically relevant manganese(II) complexes

Photoassembly of the water-oxidizing complex in photosystem II

Redox interaction of Mn–bicarbonate complexes with reaction centres of purple bacteria

Contact Info

Product

Resources

About