How incomplete was LUCA?

LUCA is the Last Universal Common Ancestor and she had a number of quite odd characteristics which provide some insight in to what conditions might have been like at the dawn of life on Earth.

I hope we have all watched Lex Fridman chatting with Nick Lane:

Somewhere around 8m 50s they tackle the subject of why the existence of both bacteria and archaea imply life only originated once on earth. Towards 15m they discuss the differences between the two life forms and the very high probability that they both arose within the same localised vent system.

What I felt was missing from the discussion was the incomplete nature of LUCA. It's implied but not explicit. Maybe that's just me and my own biases but the fact that LUCA was incomplete and differentiated in to bacteria and archaea as alternative routes to completion is very central to how life evolved and has something to say about the conditions at the time.

The core reaction at the origin of life is

CO₂ + 2H+ + 2e-   ->   CO + H₂O

The electrons come from reduced ferredoxin, which is a fossilised remnant of the FeS structure of the hydrothermal vent system, where the pH differential across FeS minerals, between vent and oceanic fluids, provides electrons (and hydrogen) with the power to reduce CO₂. I went over it in horrible detail back here.

This next image is cropped from the excellent paper

Biochemical fossils of the ancient transition from geoenergetics to bioenergetics in prokaryotic one carbon compound metabolism

and shows exactly the core reaction at the origin of life, it runs from bottom to top.

We also know from Huber and Wächtershäuser's work

Activated acetic acid by carbon fixation on (Fe,Ni)S under primordial conditions

that supplying a methyl source (they used CH3-SH) and an iron/nickel/sulphur catalyst, that activated acetate was easily formed from exogenous CO (but not from CO₂, you need the reduced ferredoxin for that step, as above). Thus:

CO + CH3-SH + H₂O -> CH3.COO-SH   (activated acetate is energetically approximately equivalent to ATP)

In origin of life scenarios the initial supply of methyl groups is assumed to be of geochemical origin in the vents. To leave the vents you need a) a source of reduced ferredoxin to generate the CO from CO₂ and b) a source of methyl groups to replace the geochemical CH3-SH. Oh, and some hydrogen but thats another story.

Archaea and bacteria have solved the problems of ferredoxin supply and methyl supply in completely different ways. Neither could have left the vents without solving these problems. Which means that LUCA was dependent on geochemical CH3-SH and the two derivatives of LUCA escaped the vents by different techniques for its replacement. But ribosome function, RNA replication, DNA synthesis (but not duplication) are so similar that it is almost certain that both escapes occurred from the same overall vent population. These then spread out to other vents and took over all of the early Earth. If other vent systems were in the process of developing "life" then that life lost out to archaea and bacteria and their shared early features. LUCA is thought to have had somewhere around 30 core enzymes.

When you pick up papers on the phylogenetics of various proteins which can be traced back to LUCA by non-Lane-ophiles you have to mentally appreciate quite how limited LUCA was and how early in evolution LUCA differentiated in to archaea and bacteria. This happened while still trapped an oceanic alkaline hydrothermal vent. That's how far back LUCA lived, fixed in one location.

So it's sort of odd that oxygen centred enzymes such as catalase, superoxide dismutase (iron based, FeSOD) and the globin oxygen binding protein ancestor (precursor of haemoglobin et al) were all present in LUCA. In an anoxic ocean.

So when I look at ROS signalling I'm thinking of the nature of LUCA, ie a very, very early, pre free living organism.

Peter

Aside: why two escapes? Crude fatty acid membranes and early isoprenoid membranes were both fairly permeable to both protons (from the oceanic side) and OH- ions (from the vent fluid side). This was essential to allow continuous ingress of protons to drive a H+/Na+ antiporter. Fully impermeable membranes would not allow neutralisation of those protons by OH- ions and metabolism would collapse.

Somewhere (I cannot recall where) I read that mixing fatty acid membranes with isoprenoid membranes produces a membrane which is fully impermeable to both protons and OH- ions, shutting down the ability to neutralise those ingressing protons on which LUCA based her metabolism. If one LUCA population invented fatty acid membranes in one geographical area of a vent and another LUCA population, geographically distant but still within the same vent, chose isoprenpoids then the area of mixing of the populations would become an impossible situation for a metabolism based on the necessity of proton and OH- permeability. Which would keep the populations separate, within the same vent, to evolve differing tools to allow escape. End aside.