1
Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei.
FEBS J. 2010 Aug; 277(16):3396-403
All selected articles haveThis article has been added to your saved articles
You can follow/unfollow articles via MyF1000 or via the article or browse pages.
03 Sep 2010
Confirmation, Interesting Hypothesis, New Finding
DOI: 10.3410/f.4974956.4906054
This report demonstrates for the first time that the so-called energy conserving hydrogenase (Ech) from Methanosarcina mazei pumps protons and confirms the hypothesis that this membrane-bound enzyme complex is indeed involved in energy conservation.
Methanosarcina species, members of the methanogenic...Continue reading
Methanosarcina species, members of the methanogenic...Continue reading
This report demonstrates for the first time that the so-called energy conserving hydrogenase (Ech) from Methanosarcina mazei pumps protons and confirms the hypothesis that this membrane-bound enzyme complex is indeed involved in energy conservation.
Methanosarcina species, members of the methanogenic Archaea, thrive from the overall decarboxylation of acetate to methane and CO2. In the initial ATP-dependent step, acetate is converted to acetyl-CoA, which is cleaved to CO and a methyl group attached to a pterin cofactor. CO is oxidized to CO2 by ferredoxin and the methyl group is transferred to coenzyme M (CoM-SH), whereby an electrochemical Na+ gradient is formed. Methyl-S-CoM combines with coenzyme B (CoB-SH) to generate methane and the heterodisulfide, CoM-SS-CoB. Ferredoxin is re-oxidized by protons to yield H2 catalyzed by Ech, whereby a proton-motive force is formed as shown in this paper. It has been earlier established that H2 is funneled via a second hydrogenase and methanophenazine to the heterodisulfide reductase that recycles CoM-SH and CoB-SH by reduction. The latter membrane process provides the major part of the conserved energy equivalent to one ATP, again via a proton-motive force. Because one ATP is consumed in the first step, growth of M. mazei relies only on the Na+-pumping methyltransferase and Ech in equal parts. The discovery of Ech as a proton-pumping enzyme now completely explains the bioenergetics of these important greenhouse gas producing methanogens. In other organisms Ech operates in the reverse direction. It catalyzes the reduction of ferredoxin with H2 driven by a proton-motive force. Reduced ferredoxin is required e.g. for the synthesis of pyruvate from acetyl-CoA and CO2. Several subunits of the Ech complex are related to complex I of the mitochondrial respiratory chain, a proton-pumping NADH:quinone oxidoreductase. Many anaerobic bacteria contain Rnf, the genes of which were first discovered in Rhodobacter capsulatus, where they are involved in nitrogen fixation (Rnf = Rhodobacter nitrogen fixation). Rnf is a ferredoxin:NAD reductase functionally similar to Ech, but related in part to the Na+-pumping NADH:quinone oxidoreductase from the pathogenic bacterium Vibrio cholerae. It has been postulated that in clostridia Rnf is a Na+/H+-pump involved in energy conservation (see reference {1}, in which I am a coauthor). In R. capsulatus, Rnf most likely catalyzes the reverse electron flow from NADH to ferredoxin driven by an electrochemical Na+/H+ gradient. Reduced ferredoxin is the electron source for nitrogen fixation, the reduction of dinitrogen (N2) to ammonia. It remains to be established, however, whether Rnf pumps Na+ or H+.
Methanosarcina species, members of the methanogenic Archaea, thrive from the overall decarboxylation of acetate to methane and CO2. In the initial ATP-dependent step, acetate is converted to acetyl-CoA, which is cleaved to CO and a methyl group attached to a pterin cofactor. CO is oxidized to CO2 by ferredoxin and the methyl group is transferred to coenzyme M (CoM-SH), whereby an electrochemical Na+ gradient is formed. Methyl-S-CoM combines with coenzyme B (CoB-SH) to generate methane and the heterodisulfide, CoM-SS-CoB. Ferredoxin is re-oxidized by protons to yield H2 catalyzed by Ech, whereby a proton-motive force is formed as shown in this paper. It has been earlier established that H2 is funneled via a second hydrogenase and methanophenazine to the heterodisulfide reductase that recycles CoM-SH and CoB-SH by reduction. The latter membrane process provides the major part of the conserved energy equivalent to one ATP, again via a proton-motive force. Because one ATP is consumed in the first step, growth of M. mazei relies only on the Na+-pumping methyltransferase and Ech in equal parts. The discovery of Ech as a proton-pumping enzyme now completely explains the bioenergetics of these important greenhouse gas producing methanogens. In other organisms Ech operates in the reverse direction. It catalyzes the reduction of ferredoxin with H2 driven by a proton-motive force. Reduced ferredoxin is required e.g. for the synthesis of pyruvate from acetyl-CoA and CO2. Several subunits of the Ech complex are related to complex I of the mitochondrial respiratory chain, a proton-pumping NADH:quinone oxidoreductase. Many anaerobic bacteria contain Rnf, the genes of which were first discovered in Rhodobacter capsulatus, where they are involved in nitrogen fixation (Rnf = Rhodobacter nitrogen fixation). Rnf is a ferredoxin:NAD reductase functionally similar to Ech, but related in part to the Na+-pumping NADH:quinone oxidoreductase from the pathogenic bacterium Vibrio cholerae. It has been postulated that in clostridia Rnf is a Na+/H+-pump involved in energy conservation (see reference {1}, in which I am a coauthor). In R. capsulatus, Rnf most likely catalyzes the reverse electron flow from NADH to ferredoxin driven by an electrochemical Na+/H+ gradient. Reduced ferredoxin is the electron source for nitrogen fixation, the reduction of dinitrogen (N2) to ammonia. It remains to be established, however, whether Rnf pumps Na+ or H+.
References
1.
Energy conservation via electron-transferring flavoprotein in anaerobic bacteria.
J Bacteriol 2008 Feb; 3(190):784-91
PMID: 18039764
Disclosures
None declared
Add Comment
Buckel W: F1000Prime Recommendation of [Welte C et al., FEBS J 2010, 277(16):3396-403]. In F1000Prime, 03 Sep 2010; DOI: 10.3410/f.4974956.4906054. F1000Prime.com/4974956#eval4906054
F1000Prime Recommendations, Dissents and Comments for [Welte C et al., FEBS J 2010, 277(16):3396-403]. In F1000Prime, 19 May 2013; F1000Prime.com/4974956
Only registered/signed-in users can make comments.
Sign in or Subscribe to create your user account and join the discussion.
Sign in or Subscribe to create your user account and join the discussion.
No comments yet.
Methanosarcina mazei belongs to the group of aceticlastic methanogens and converts acetate into the potent greenhouse gases CO(2) and CH(4). The aceticlastic respiratory chain involved in methane formation comprises the three transmembrane proteins Ech hydrogenase, F(420) nonreducing hydrogenase and heterodisulfide reductase. It has been shown that the latter two contribute to the proton motive force. The data presented here clearly demonstrate that Ech hydrogenase is also involved in energy conservation. ATP synthesis was observed in a cytoplasm-free vesicular system of Ms. mazei that was dependent on the oxidation of reduced ferredoxin and the formation of molecular hydrogen (as catalysed by Ech hydrogenase). Such an ATP formation was not observed in a Deltaech mutant strain. The protonophore 3,5-di-tert-butyl-4-hydroxybenzylidene-malononitrile (SF6847) led to complete inhibition of ATP formation in the Ms. mazei wild-type without inhibiting hydrogen production by Ech hydrogenase, whereas the sodium ion ionophore ETH157 did not affect ATP formation in this system. Thus, we conclude that Ech hydrogenase acts as primary proton pump in a ferredoxin-dependent electron transport system.
DOI: 10.1111/j.1742-4658.2010.07744.x
PMID: 20629748
