The bicarbonate effect, oxygen evolution, and the shadow of Otto Warburg

Stemler, Alan

doi:10.1007/1-4020-3324-9_37

Cited by 24 publications

(21 citation statements)

References 19 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Several research groups followed up on these initial results and identified two possible sites of C i interaction within PSII (reviewed in refs. [9][10][11][12]. Functional and spectroscopic studies showed that HCO − 3 facilitates the reduction of the secondary plastoquinone electron acceptor (Q B ) of PSII by participating in the protonation of Q 2− B .…”

mentioning

confidence: 99%

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Koroidov

Shevela

Shutova

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

Cyanobacteria, algae, and plants oxidize water to the O 2 we breathe, and consume CO 2 during the synthesis of biomass. Although these vital processes are functionally and structurally well separated in photosynthetic organisms, there is a long-debated role for CO 2 /HCO − 3 in water oxidation. Using membrane-inlet mass spectrometry we demonstrate that HCO − 3 acts as a mobile proton acceptor that helps to transport the protons produced inside of photosystem II by water oxidation out into the chloroplast's lumen, resulting in a light-driven production of O 2 and CO 2 . Depletion of HCO − 3 from the media leads, in the absence of added buffers, to a reversible down-regulation of O 2 production by about 20%. These findings add a previously unidentified component to the regulatory network of oxygenic photosynthesis and conclude the more than 50-y-long quest for the function of CO 2 / HCO − 3 in photosynthetic water oxidation.O xygenic photosynthesis in cyanobacteria, algae, and higher plants leads to the reduction of atmospheric CO 2 to energy-rich carbohydrates. The electrons needed for this process are extracted in a cyclic, light-driven process from water that is split into dioxygen (O 2 ) and protons. This reaction is catalyzed by a penta-μ-oxo bridged tetra-manganese calcium cluster (Mn 4 CaO 5 ) within the oxygen-evolving complex (OEC) of photosystem II (PSII) (1-4). The possible roles of inorganic carbon, C i ðC i = CO 2 ; H 2 CO 3 ; HCO − 3 ; CO 2− 3 Þ, in this process have been a controversial issue ever since Otto Warburg and Günter Krippahl (5) reported in 1958 that oxygen evolution by PSII strictly depends on CO 2 and therefore has to be based on the photolysis of H 2 CO 3 ("Kohlensäure") and not of water. These first experiments were indirect and, as became apparent later, were wrongly interpreted (6-8). Several research groups followed up on these initial results and identified two possible sites of C i interaction within PSII (reviewed in refs. 9-12). Functional and spectroscopic studies showed that HCO − 3 facilitates the reduction of the secondary plastoquinone electron acceptor (Q B ) of PSII by participating in the protonation of Q 2− B . Binding of HCO − 3 (or CO 2− 3 ) to the nonheme Fe between the quinones Q A and Q B was recently confirmed by X-ray crystallography (3,13,14). Despite this functional role at the acceptor side, the very tight binding of HCO − 3 to this site makes it impossible for the activity of PSII to be affected by changing the C i level of the medium; instead inhibitors such as formate need to be added to induce the acceptor-side effect (15). Consequently, the watersplitting electron-donor side of PSII has also been studied intensively (for recent reviews, see refs. 11 and 12). Although a tight binding of C i near the Mn 4 CaO 5 cluster is excluded on the basis of X-ray crystallography (3, 14), FTIR spectroscopy (16), and mass spectrometry (17, 18), the possibility that a weakly bound HCO − 3 affects the activity of PSII at the donor side remains a viable option (reviewed i...

show abstract

mentioning

confidence: 99%

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Koroidov

Shevela

Shutova

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

show abstract

“…Alternative concepts like Otto Warburg's (Warburg and Krippahl, 1958;Warburg et al, 1965), who proposed that ''activated CO 2 '' is converted to an aldehyde during oxygen evolution (for a historical survey, see Stemler, 2002), have been discarded mainly because of mass-spectrometric results that show that in PSII preparations the isotopic composition of liberated dioxygen agrees well with the one of the surrounding water even after relatively short mixing times with H 2…”

mentioning

confidence: 99%

“…Strictly speaking, however, these data are still compatible with a catalytic role of bicarbonate if the equilibrium between water, CO 2 , and bicarbonate is rapidly installed, as mediated, for example, by a carbonic anhydrase (CA; Silverman and Tu, 1975;Tu and Silverman, 1975). An intrinsic CA activity is indeed linked to the core and/or extrinsic proteins of PSII (Dai et al, 2001;Stemler, 2002;Villarejo et al, 2002;Khristin et al, 2004). The above-cited mass-spectrometric experiments were not designed to specifically address the bicarbonate question, and therefore the CA activity was not assessed in detail.…”

mentioning

confidence: 99%

“…The function of the observed CA activity of PSII and of thylakoid membranes as a whole remains to be elucidated (see Table I and Fig. 2B; for review, see Stemler, 1998Stemler, , 2002. It has been suggested that the lumenal CA of thylakoids may play a role in the formation of a proton gradient across the thylakoid membrane in the dark in order to support ATP synthesis (van Hunnik and Sultemeyer, 2002).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Evidence That Bicarbonate Is Not the Substrate in Photosynthetic Oxygen Evolution

et al. 2005

View full text Add to dashboard Cite

(J.C., W.J.); and Max-PlanckInstitut fü r Bioanorganische Chemie, 45470 Muelheim an der Ruhr, Germany (K.B., J.M.)It is widely accepted that the oxygen produced by photosystem II of cyanobacteria, algae, and plants is derived from water. Earlier proposals that bicarbonate may serve as substrate or catalytic intermediate are almost forgotten, though not rigorously disproved. These latter proposals imply that CO 2 is an intermediate product of oxygen production in addition to O 2 . In this work, we investigated this possible role of exchangeable HCO 3 2 in oxygen evolution in two independent ways. (1) We studied a possible product inhibition of the electron transfer into the catalytic Mn 4 Ca complex during the oxygen-evolving reaction by greatly increasing the pressure of CO 2 . This was monitored by absorption transients in the near UV. We found that a 3,000-fold increase of the CO 2 pressure over ambient conditions did not affect the UV transient, whereas the S 3 / S 4 / S 0 transition was half-inhibited by raising the O 2 pressure only 10-fold over ambient, as previously established. (2) The flash-induced O 2 and CO 2 production by photosystem II was followed simultaneously with membrane inlet mass spectrometry under approximately 15% H 2 18 O enrichment. Light flashes that revealed the known oscillatory O 2 release failed to produce any oscillatory CO 2 signal. Both types of results exclude that exchangeable bicarbonate is the substrate for (and CO 2 an intermediate product of) oxygen evolution by photosynthesis. The possibility that a tightly bound carbonate or bicarbonate is a cofactor of photosynthetic water oxidation has remained.

show abstract

“…For references, seeGovindjee and van Rensen (1978, 1993),Stemler (1982Stemler ( , 2005,Vermaas and Govindjee (1982),van Rensen et al (1999), andEaton-Rye (2007).…”

mentioning

confidence: 98%

Recollections of Thomas John Wydrzynski

Govindjee

2008

Photosynth Res

View full text Add to dashboard Cite

In appreciation of his contribution to the Photosystsem II research and commemoration of the book Photosystem II: The Light-Driven Water-Plastoquinone Oxido-Reductase, co-edited with Kimiyuki Satoh, I present here some of my recollections of Thomas John Wydrzynski and by several others with whom he has associated over the years at Urbana (Illinois), Berkeley (California), Standard Oil Company-Indiana (Illinois), Berlin (Germany), Gothenburg (Sweden), and Canberra (Australia). We not only recognize him for his unique career path in Photosystem II research, but also for his qualities as a collaborative scientist working on the only system on Earth that has the ability to oxidize water to molecular oxygen using the energy of sunlight.

show abstract

The bicarbonate effect, oxygen evolution, and the shadow of Otto Warburg

Cited by 24 publications

References 19 publications

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation

Evidence That Bicarbonate Is Not the Substrate in Photosynthetic Oxygen Evolution

Recollections of Thomas John Wydrzynski

Contact Info

Product

Resources

About