Loki and its membrane potential

Nick Lane makes some interesting comments about Loki, currently accepted as being the closest living descendent of the archaeon which merged with an alpha proteobacterium to generate LECA, the Last Eukaryote Common Ancestor:

Lokiarchaeon is hydrogen dependent

Loki is fascinating. We don't quite have all of its genome, roughly 92% of it. There are bits missing for parts of ATP synthase and for the carbon monoxide dehydrogenase/acetyl-CoA synthase (CODH/ACS) complex but we can be pretty sure these are in that missing 8% of the genome which we have yet to find and sequence. After all, prokaryotes don't carry junk DNA. Having most of the genes for a functional complex suggests that the rest of those needed to make it work are present.

What is completely absent is anything suggesting any sort of respiratory chain. That's not so unusual, especially in anaerobes.

Or any sort of membrane pump.

No membrane pump? I suspect that there must be small ion pump of some sort either tucked away in the missing 8% of the genome or within some of the currently uninterpretable DNA. Certainly none of the large modern complex pumps are present in any part, so Ech, Rnf and MtrA-H are all out, although the MtrH gene alone is present. I'd assume MtrH is transferring methyl groups to somewhere other than to the absent MtrA-G Na+ pump, over to CODH/ACS seems most likely.

The core energy process appears to be based on using electron bifurcating hydrogenases to generate very low potential ferredoxins. This allows the CODH/ACS complex to generate acetyl phosphate or acetyl-CoA. Substrate level phosphorylation can then give ATP and it's all down hill, energetically speaking, from there onwards. This gives a strict anaerobic metabolism based on an external source of hydrogen.

Obviously a membrane gradient has many uses in addition to ATP synthesis so I wouldn't doubt for a moment that one is present. Keeping it energised is the trick.

It left me thinking about how you might generate a membrane potential in the absence of any obvious relative to modern day ion pumps. I recalled that Koonin had mentioned some very ancient sodium pumps based around either decarboxylation reactions or around pyrophosphate cleavage.

In Evolutionary primacy of sodium bioenergetics he comments:

"These ancestral ATPases [ATP synthase in reverse] would pump Na+ along with the Na+-transporting pyrophosphatase [62] and chemically-driven Na+-pumps, such as Na+-transporting decarboxylase [29,63], which, being found in both bacteria and archaea, appear to antedate the divergence of the three domains of life".

From which ref 62 is a good read

Na+-Pyrophosphatase: A Novel Primary Sodium Pump

"The role of Na+-PPase can be most easily conjectured in the thermophilic marine bacterium, T. maritima, which utilizes Na+ as the primary bioenergetic coupling ion and employs a Na+-ATP-synthase (35, 36). In this organism, Na+-PPase may work in concert with Na+-ATP-synthase to scavenge energy from biosynthetic waste (PPi) in order to maintain the Na+ gradient, especially under energy-limiting conditions".

And for Na+ pumping via conversion of succinate to proprionate:

Bacterial Na+- or H+-coupled ATP Synthases Operating at Low Electrochemical Potential

"A prominent example is Propionigenium modestum, which grows from the fermentation of succinate to propionate and CO2 (Schink and Pfennig, 1982; Dimroth and Schink, 1998). The free energy of this reaction is about -20 kJ/mol whereas approximately -70 kJ/mol is required to support ATP synthesis in growing bacteria (Thauer et al., 1977). To solve this apparent paradox, 3–4 succinate molecules must be converted into propionate before one ATP molecule can be synthesized".


This last process is somewhat more complex than pyrophosphate hydrolysis and looks less of a candidate for "hidden" membrane potential generation than the Na+PPase. After all, CODH/ACS is providing ATP and many reactions which need to be "one-way" cleave ATP to AMP and PPi. The PPi "waste" would then be available to pump Na+.

My guess would be that Loki will turn out to use Na+ membrane energetics...

Time will tell.

Peter