It is well known that Darwin speculated on what might happen in "some warm little pond" (previously discussed here). But it was not until 1929 that J.B.S. Haldane developed a testable hypothesis involving a "prebiotic broth, or primordial soup". He proposed that organic compounds were made when methane, ammonia and water reacted as a result of energy supplied by ultraviolet radiation. The reaction products were suggested to have accumulated in a "hot dilute soup" in the primeval earth. In this scenario, further reactions led to macromolecules, protocells and then life.
"Backed up by Stanley Miller's (1953) inorganic synthesis of organic molecules in the laboratory, it seemed to generations of scientists that Haldane's narrative was basically right, and all that was left was to sort out the details."
It is time to move on from this unproductive research (source here)
Miller's experiments became an icon of naturalistic evolution and entered the textbooks with very little critical analysis of the findings. Even recently, Miller's work was acclaimed in the journal Science. Happily, there are opportunities to get beyond the hype but, as Jonathan Wells showed in his Icons of Evolution, these contributions rarely get beyond the technical literature. William Martin and colleagues have presented a strong case for retiring the primordial soup concept from active service. It has reached the grand old age of 81 and, as a hypothesis, it has not been confirmed. Normally, when hypotheses are tested and found wanting, they are discarded - but we are now overdue for this to happen with the primordial soup. It is "well past its sell-by date".
Two reasons are provided in the paper. The first is that a soup of organic chemicals will be in thermodynamic equilibrium. The reaction products are already present and there is no obvious source of energy to drive polymerisation or any other significant change. "Ionizing UV radiation inherently destroys as much as it creates."
"[T]he homogeneous soup has no internal free energy that would allow them to react further. Life is not just about replication; it is also a coupling of chemical reactions - exergonic ones that release energy and endergonic ones that utilise it, preventing the dissipation of energy as heat. It is commonplace to say that life requires energy, but the conception of a primordial soup fails to recognise or incorporate the importance of energy flux. On the congruence principle, what life needed was not some harsh and problematic source of energy like UV radiation (or lightning), but a continuous and replenishing source of chemical energy."
The second reason concerns fermentation as the primordial mechanism of energy generation in a world without oxygen. Haldane promoted this idea, and De Duve supported it as the mechanism for sustaining anaerobic life. "If there can be said to be a textbook view, this is it."
"But there are profound difficulties - both chemical and biological - in viewing fermentation as primitive rather than derived. Fermentation is chemically a disproportionation - not a simple redox reaction, in which electrons are stripped from a donor and passed onto an acceptor, driven by strong thermodynamics. In contrast with respiration, the amount of energy released by fermentation is tiny, reflecting its lack of thermodynamic driving force. To tap such an insignificant source of energy requires more rather than less sophistication, and indeed about 12 enzymes are needed to catalyse a complex succession of steps in glycolytic-type fermentations based around the Embden-Meyerhoff pathway. These enzymes are proteins encoded by genes, which would have had to evolve as a functional unit without any other source of energy in the primordial oceans - close to an impossibility in an RNA world, let alone the only way to evolve one."
The authors go on to defend their view that fermentation is a sophisticated, rather than a primordial, derivation. This brings them to the crunch question:
"But if there was no soup, and no energy from UV radiation or fermentation, then where was the energy that powered the emergence of life?"
They go on to propose alkaline hydrothermal vents as the primordial source of energy for life. They develop their idea that the origin of life can be considered distintly from the origin of replication. They support Russell et al's (1993) proposal that chemiosmosis is "an inherent property of life, one inherited from the very place and space where it arose". Their paper is exploratory, not plotting out any details of what the Last Universal Common Ancestor (LUCA) looked like, but considering how chemiosmosis might have worked in the setting of alkaline hydrothermal vents. Further discussion of this is needed, of course, but this blog is to draw attention to the challenge these authors present to OOL researchers generally and to textbook authors/educators.
"It is time to cast off the shackles of fermentation in some primordial soup as 'life without oxygen' - an idea that dates back to a time before anybody had any understanding of how ATP is made - and to embrace the most revolutionary idea in biology since Darwin as the key not only to the bioenergetics of all life on Earth today, but to its very origin.(80) Thus it seems to us likely that LUCA grew on the H2/CO2 couple, and that she was naturally chemiosmotic."
How did LUCA make a living? Chemiosmosis in the origin of life
Nick Lane, John F. Allen, William Martin
Bioessays, 32(4), 271-280, April 2010 | DOI: 10.1002/bies.200900131
Despite thermodynamic, bioenergetic and phylogenetic failings, the 81-year-old concept of primordial soup remains central to mainstream thinking on the origin of life. But soup is homogeneous in pH and redox potential, and so has no capacity for energy coupling by chemiosmosis. Thermodynamic constraints make chemiosmosis strictly necessary for carbon and energy metabolism in all free-living chemotrophs, and presumably the first free-living cells too. Proton gradients form naturally at alkaline hydrothermal vents and are viewed as central to the origin of life. Here we consider how the earliest cells might have harnessed a geochemically created proton-motive force and then learned to make their own, a transition that was necessary for their escape from the vents. Synthesis of ATP by chemiosmosis today involves generation of an ion gradient by means of vectorial electron transfer from a donor to an acceptor. We argue that the first donor was hydrogen and the first acceptor CO2.
New Research Rejects 80-Year Theory of 'Primordial Soup' as the Origin of Life, ScienceDaily (3 February 2010)
Warren, D. Back to the beginning, The Ottawa Citizen (6 February 2010)
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