On the origin of biochemistry at an alkaline hydrothermal vent

Abstract

A model for the origin of biochemistry at an alkaline hydrothermal vent has been developed that focuses on the acetyl-CoA (Wood-Ljungdahl) pathway of CO2 fixation and central intermediary metabolism leading to the synthesis of the constituents of purines and pyrimidines. The idea that acetogenesis and methanogenesis were the ancestral forms of energy metabolism among the first free-living eubacteria and archaebacteria, respectively, stands in the foreground. The synthesis of formyl pterins, which are essential intermediates of the Wood-Ljungdahl pathway and purine biosynthesis, is found to confront early metabolic systems with steep bioenergetic demands that would appear to link some, but not all, steps of CO2 reduction to geochemical processes in or on the Earth's crust. Inorganically catalysed prebiotic analogues of the core biochemical reactions involved in pterin-dependent methyl synthesis of the modern acetyl-CoA pathway are considered. The following compounds appear as probable candidates for central involvement in prebiotic chemistry: metal sulphides, formate, carbon monoxide, methyl sulphide, acetate, formyl phosphate, carboxy phosphate, carbamate, carbamoyl phosphate, acetyl thioesters, acetyl phosphate, possibly carbonyl sulphide and eventually pterins. Carbon might have entered early metabolism via reactions hardly different from those in the modern Wood-Ljungdahl pathway, the pyruvate synthase reaction and the incomplete reverse citric acid cycle. The key energy-rich intermediates were perhaps acetyl thioesters, with acetyl phosphate possibly serving as the universal metabolic energy currency prior to the origin of genes. Nitrogen might have entered metabolism as geochemical NH3 via two routes: the synthesis of carbamoyl phosphate and reductive transaminations of alpha-keto acids. Together with intermediates of methyl synthesis, these two routes of nitrogen assimilation would directly supply all intermediates of modern purine and pyrimidine biosynthesis. Thermodynamic considerations related to formyl pterin synthesis suggest that the ability to harness a naturally pre-existing proton gradient at the vent-ocean interface via an ATPase is older than the ability to generate a proton gradient with chemistry that is specified by genes.

Early Microbial Evolution: The Age of Anaerobes

“…The acetyl-CoA pathway is regarded as the most ancient of the six pathways of CO 2 fixation known (Fuchs 2011) and in contrast to earlier views; it is the only one that occurs in both archaea and bacteria (Berg et al 2010). The source of electrons for CO 2 fixation is geological H 2 (Martin and Russell 2007), the same electron donor that modern microbes using the acetyl-CoA harness, and the source of energy is the exergonic reduction of CO 2 to acetate in the case of acetogens or methane in the case of methanogens (Sousa et al 2013b). The H 2 required to push the equilibrium toward the accumulation of reduced organic compounds comes from a geochemical process called serpentinization (Martin and Russell 2007;Russell et al 2010), which has been going on as long as there has been water on Earth (Sleep et al 2004).…”

The Origin of Life: Chemical Evolution of a Metabolic System in a Mineral Honeycomb?

“…Similarly, other authors ascribe a critical role to the 3D porous structure of iron monosulphide precipitates or aragonite (CaCO 3 ) in hydrothermal vent systems (Koonin and Martin 2005;Martin and Russell 2003;Martin and Russell 2007). Recently, the extreme accumulation of nucleotides in simulated hydrothermal pore systems driven by thermodiffusion has been shown.…”

“…Raw materials (''resources'') flow into each pore at a constant rate from an external source like in a ''black smoker'' (Martin and Russell 2003;Martin and Russell 2007;Parsons et al 1998).…”

Peptide and RNA contributions to iron–sulphur chemical gardens as life's first inorganic compartments, catalysts, capacitors and condensers

“…The ultimate reduction or waste product was probably initially acetate [12][13][14][15], and the womb or omphalos of life a chemical garden-like precipitate over a submarine alkaline spring, especially where it vented into the acidulous, iron-bearing Hadean Ocean [16][17][18]. Much as predicted, a comparable spring-the so-called Lost City-was discovered in the North Atlantic in 1999 [16,19,20].…”