The article specifies a number of stages from abiotic chemicals via protocells to free-living cells. Together they form a theory for the origin of life (OOL). The model is an 'energy-first information-later' model. In the first phase there are no proteins and dna. In the last stage proteins and dna are present (dna-protein world). It means that the base sequence of dna specifies the amino acid sequence of proteins. This is also known as the genetic code. The dna-protein world implies dna replication, transcription, translation, ribosomes. In other words, it requires a great number of highly complex proteins.
The authors know that complex enzymes and proteins can not be present in the first stages of the origin of life because life cannot start with the dna-protein world. They claim that in an early stage amino acids, bases, sugars, and lipids can be produced. Although this suggests more, they do not claim that proteins or dna are present in this early stage.
However, a crucial aspect of their model is the presence, at an early stage, of special proteins in membranes ('sodium-proton antiporter'). Without the presence of such a protein the model simply does not work. Now my criticism is:
At any stage before the dna-protein world, the presence of a non-random protein, no matter how simple, is forbidden.
Lane and Martin seem to violate this rule most clearly in this statement:
"Finally, the origins of Na+ pumping required no mechanistically groundbreaking genetic innovations, just a protein, an antiporter that transduced a geochemical gradient (H+) into a biochemical one (Na+)."If that antiporter protein consists of a few hundred amino acids than its presence before the dna-protein world is forbidden. At other places in their article they suggest that this protein is simple:
"Thus, a simple Na+/H+ antiporter in protocells within vent pores would produce Na+ gradients."However, even a simple protein is forbidden because it assumes the dna-protein world. There is no small dna-protein world producing small proteins. It's all or nothing. If there exists a dna-protein world, it can produce proteins of any length.
I think they could make the error because they focus on energy problems:
"But if energy conserved by proteins is needed to make proteins, where did the energy come from that gave rise to the first proteins?"Analogously, I would ask: "if information is needed to make proteins, where did the information come from that gave rise to the first proteins?". It is true that energy is required to produce proteins, but information is also required. From a chemical point of view, proteins with random amino acids could be produced . If so, of what use are those proteins? Useful proteins have a specific sequence of amino acids. As far as I know, the specification can only come from DNA or RNA . Furthermore, a large number of identical copies of a specified protein can only be produced in the dna-protein world.
The authors state "At a later protocellular stage, membrane lipids and proteins became genetically encoded". But this implies that a specific functional protein that is not encoded by DNA or RNA exists and later 'became genetically encoded'. Encoding a protein that already exists is impossible because the central dogma of molecular genetics forbids the flow of information from proteins to DNA or RNA . So, if the model depends on the existence of specific non-random proteins before the emergence of the dna-protein world, the model fails.
Similarily Ed Young  makes the same error in his Nature news article with the revealing subtitle 'The origin of ion-pumping proteins could explain how life began in, and escaped from, undersea thermal vents.'. Indeed he writes:
"Lane and Martin think that proto-cells escaped this dilemma because they evolved a sodium-proton antiporter — a simple protein that uses the influx of protons to pump sodium ions out of the cell"The presence of proteins is forbidden in the early stages of every origin of life scenario. Furthermore, Young writes: 'evolved'. Evolving is not possible in a pre-RNA-world or pre-DNA-protein world.
The error is hidden because the article does not strictly separate the different stages and the possibilities and limitations of each stage separately. I am not saying that the ideas in the article are of no value. The publication is important in other respects. But the OOL scenario present in Cell seems fatally flawed by the premature presence of proteins.
- Nick Lane and William Martin (2012) The Origin of Membrane Bioenergetics, Cell 151, December 21, 2012 (free access)
- Ed Yong (2012) How life emerged from deep-sea rocks, Nature, 20 December 2012 (free access)
- According to Pier Luigi Luisi (2006) The emergence of Life: "In fact, we simply do not know how to make long polypeptides by prebiotic means." (p. 64) [added: 28 Dec 2012]
- There are no exceptions or violations of the central dogma of molecular genetics known today: information never flows back from proteins to RNA or DNA. Furthermore, proteins do not self-replicate. (added: 28 Dec 2012). The only alternative would be the evolution of the protein from scratch in the DNA-protein world [added 2-1-13]
- Recently, a sequence-specific nonribosomal peptide synthesis by an artificial molecular machine is reported in Science 11 Jan 2013: "we report on the design, synthesis, and operation of a rotaxane-based small-molecule machine in which a functionalized macrocycle operates on a thread containing building blocks in a predetermined order to achieve sequence-specific peptide synthesis". So, this is peptide synthesis not based on DNA, nor RNA, nor a ribosome. (Rotaxane is a (very) primitive analog of the ribosome.) This is an interesting mechanism, despite the loss of the sequence information on the strand as it is translated into the product. This system is not heritable information because the information is destructed in the process. Another disadvantage is that peptides are too small to function as an antiporter. [added: 12 Jan 2013]
Acknowledgments: I thank Marleen Roelofs for pointing me to both articles.
Update 25 Dec 2012
I rewrote the following section and included it in the text:
The authors state "At a later protocellular stage, membrane lipids and proteins became genetically encoded". But this implies there is a specific functional protein that is not encoded by DNA or RNA and 'later became genetically encoded'. Encoding a protein that already exists is impossible because the central dogma of molecular genetics forbids the flow of information from proteins to DNA or RNA.
Update 27 Dec 2012
This blog does not attack the natural Origin Of Life! I am merely trying to help the natural selection of fitter Origin-Of-Life theories by elimination of less fitter theories.
31 dec: minor editorial improvement of the intro.
Update 12 Jan 2013
Note 5 added.