Friday, January 11, 2019

How primordial is oxidative phosphorylation?

It is perfectly possible to run a sophisticated metabolism using the energy available from an hydrogen rich geochemical proton gradient of the type still found in locations such as Lost City in the Atlantic. This provides an (almost) endless supply of electrons via FeS catalysts of sufficiently negative potential to reduce carbon dioxide to carbon monoxide. From here it is all down hill, energetically speaking, to acetate and metabolism. The process is completely dependent on geochemical conditions for the free-ride. These basic steps are still embedded in the carbon monoxide dehydrogenase/acetyl-CoA synthase complex discussed rather nicely in this 2018 paper (how did I miss it?):

Evolutionary history of carbon monoxide dehydrogenase/acetyl-CoA synthase, one of the oldest enzymatic complexes

Back in the Life series of posts I argued in favour of Koonin's concept that Na+ provided the primary electrochemical gradient which was used to drive a Na+ transporting rotary ATP synthase. It's all in here:

Evolutionary primacy of sodium bioenergetics

My own idea is that primordial Na+ energetics derived from a geochemical proton gradient which was converted to a Na+ gradient by a H+/Na+ antiporter. In order to detach from the geochemical proton gradient what is needed is a Na+ pump to replace this geochemically driven antiporter. Acetobacterium woodii has the most highly conserved version of such a Na+ coupled system and back in 2009 the Rnf complex was the primary suspect for being the site of Na+ pumping.

The ins and outs of Na+ bioenergetics in Acetobacterium woodii

By 2010 this was pretty well confirmed:

Bacterial Na+-translocating ferredoxin:NAD+ oxidoreductase

In its most autotrophic guise A woodii can still run its metabolism on molecular hydrogen. The process of electron bifurcation allows the generation of reduced ferredoxin from H2 and so can provide electrons of a potential to use NAD+ as their electron acceptor, with sufficient energy left over to pump a single Na+ ion, in imitation of the H+/Na+ geochemical driven antiporter used soon after the origin of life. This Na+ pumping allowed prokaryotes to leave hydrothermal vents, provided there was access to molecular hydrogen as food.

This core process which freed early life from the ties to geochemical alkaline hydrothermal vents is clearly the oxidation of reduced-ferredoxin, ie this is an oxidative reaction driving an electrochemical Na+ gradient to phosphorylate ADP to ATP using a Na+ driven rotary ATP synthase.

It is oxidative phosphorylation.

Oxidative-phosphorylation is as primordial as the exodus of prokaryotes from hydrothermal vents.

Peter

7 comments:

Unknown said...

Fascinating, Peter. Four more nails in the " Glucose metabolism is primitive" coffin. Who else will notice?

Peter said...

Thank you Unknown. I can see that some form of glucose synthesis was probably present in LUCA but it's synthesis would have been metabolically costly. Anoxygenic photosynthesis would have provided more and oxygenic photosynthesis lots. But the sort of conditions that a yeast might find to tempt it to abandon its mitochondria and produce a pint of cider of requires a little longer than all of those....

Peter

altavista said...

If oxphos is more efficient and had 1bn years headstart to refine itself, switching to glycolysis for energy is like water flowing uphill just for kicks.

Peter said...

Altavista, A woodii has persevered with hydrogen based ox-phos because it has benefited from exploiting anoxic environments. Not much use in a ton of cytochromes if there is no O2 to be the terminal acceptor... Of course if normally O2 based ox phos is caput for whatever reason then the presence of O2 is not really much use. Glycolysis might help here. I think we have interesting possibilities depending on the degree of ox-phos disruption, assuming it is present. I'm still struggling with trying to determine how much absolute respiration Chandel's HCT mitochondria are actually doing. Metformin reduces the amount of O2 consumption, but how does this compare to non neoplastic cells in terms of total O2 consumption? I'm thinking that comparisons would be very, very difficult. Hence use of relative respiration cf same cell type control, ie relative change. But relative change is how statins can be shown to reduce all cause mortality by 17% in FH people, which still means nothing.

But I also think I'm drowning in bias because I don't like much of the metformin research, especially nowadays.

Peter

Peter said...

Thank you Unknown. I can see that some form of glucose synthesis was probably present in LUCA but its synthesis would have been metabolically costly. Anoxygenic photosynthesis would have provided more and oxygenic photosynthesis lots. But the sort of conditions that a yeast might find to tempt it to abandon its mitochondria and produce a pint of cider of requires a little longer than all of those....

Peter

Another edited comment for another bl**dy apostrophe. Really must stop this.

Bob said...

Actually, the part I wish you had edited was "...produce a pint of cider of..." The last "of" makes no sense before "requires a little longer," although I think I know what you meant.

As for "its" vs "it's": I read somewhere that probably a future change to "official" English will be to drop the apostrophe from the "it is" version. Then no one will need worry about it again.

Peter said...

Thank you Unknown. I can see that some form of glucose synthesis was probably present in LUCA but its synthesis would have been metabolically costly. Anoxygenic photosynthesis would have provided more and oxygenic photosynthesis lots. But the sort of conditions that a yeast might find to tempt it to abandon its mitochondria and produce a pint of cider requires a little longer than all of those....

Peter

Another edited comment for another bl**dy apostrophe. Really must stop this. And the "of"!