Provisioning the origin and early evolution of life

Abstract

There is a lot of controversy in the origin and early evolution of life field, but most people agree that at the advent of genetically coded protein synthesis, cells must have had access to ribonucleotides, amino acids, lipids and some sort of energy source. However, the provenance of these materials is a contentious issue - did early life obtain its building blocks prefabricated from the environment, or did it synthesise them from feedstocks such as CO₂ and N₂? In the first case, synthesis conditions need not have been compatible with life and any kind of reaction network that furnished the building blocks - and not much else - could have provisioned the subsequent origin and early evolution of life. In the second case, synthesis must have been under life-compatible conditions, with the reaction network either along the same lines as extant biology or along different ones. On the basis of experimental evidence, we will argue in favour of prefabrication and against synthesis by life in its nascent state, especially synthesis that resembles extant biosynthesis, which we suggest would have been well-nigh impossible without biological catalysts.

Figure 1.. To what extent do life-compatible conditions overlap conditions for the synthesis of (proto)biological building blocks?

Four representative possibilities are shown: (a) no overlap, (b) limited overlap, (c) complete overlap, and (d) two different sets of conditions are needed for building block synthesis, one set partly overlaps life-compatible conditions and the other not at all.

Figure 2.. Cyanosulfidic protometabolic reaction network leading from HCN and derivatives thereof to pyrimidine ribonucleotides, and amino acid and lipid precursors.

Pathways, intermediates and products specific to a particular product class are shown in colour (pyrimidine ribonucleotides, purple; amino acids, green; lipids, orange) with products boxed, shared starting materials, pathways and intermediates are shown in black.

Figure 3.. Minimal biosynthetic reaction network leading from CO₂ and N₂ (or ) to ribonucleotides, amino acids and lipid precursors.

Hub compounds are indicated by large disks and other compounds are indicated by smaller disks coloured according to biosynthetic route/product class (partial gluconeogenesis, pink; purine ribonucleotides, light blue; pyrimidine ribonucleotides, purple; amino acids, green; lipids, orange). Feedstocks are indicated by black squares and the immediate metabolites thereof as small black disks. ATP(/GTP)-consuming reactions are shown as red arrows, the number of which matches the number of high-energy phosphate bonds consumed per reaction. Oxidation reactions are shown by blue arrows. A more complete description of each reaction is provided in the Supplementary Material, as is a list of abbreviations.