Autocatalytic chemical networks at the origin of metabolism.

Joana C Xavier,William F Martin,Stuart Kauffman,Mike Steel,Wim Hordijk

doi:10.1098/rspb.2019.2377

Abstract

Modern cells embody metabolic networks containing thousands of elements and form autocatalytic sets of molecules that produce copies of themselves. How the first self-sustaining metabolic networks arose at life's origin is a major open question. Autocatalytic sets smaller than metabolic networks were proposed as transitory intermediates at the origin of life, but evidence for their role in prebiotic evolution is lacking. Here, we identify reflexively autocatalytic food-generated networks (RAFs)—self-sustaining networks that collectively catalyse all their reactions—embedded within microbial metabolism. RAFs in the metabolism of ancient anaerobic autotrophs that live from H2 and CO2 provided with small-molecule catalysts generate acetyl-CoA as well as amino acids and bases, the monomeric components of protein and RNA, but amino acids and bases without organic catalysts do not generate metabolic RAFs. This suggests that RAFs identify attributes of biochemical origins conserved in metabolic networks. RAFs are consistent with an autotrophic origin of metabolism and furthermore indicate that autocatalytic chemical networks preceded proteins and RNA in evolution. RAFs uncover intermediate stages in the emergence of metabolic networks, narrowing the gaps between early Earth chemistry and life.

Highlights

Cells are autocatalytic in that they require themselves for reproduction
The reflexively autocatalytic food-generated networks (RAFs) of the methanogen and the acetogen intersect in a primordial network that generates amino acids, nucleosides, and acetyl-CoA from a starting set of simple food molecules, shedding light on the nature of autocatalytic networks that existed before the first cells arose from the elements on the early Earth
Compounds generated from the food set become part of the network, autocatalytic networks can start small and grow, in principle to a size approaching the complexity of metabolic networks of modern cells [15], and very little catalysis by individual elements is required for autocatalytic networks to emerge [19,20]

Summary

Introduction

Cells are autocatalytic in that they require themselves for reproduction. The origin of the first cells from the elements on the early Earth roughly 4 billion years ago [1,2,3,4] must have been stepwise. RAFs impose that all necessary catalysts need to be produced by the network at some point, but not necessarily at the first time they are required This feature models the emergence of specificity, speed, and efficiency in autocatalysis. If autocatalytic chemical networks antedate genetically encoded proteins, cofactor-dependent RAFs might have been involved and, if so, should have left evidence for their existence in modern metabolic networks. The RAFs of the methanogen and the acetogen intersect in a primordial network that generates amino acids, nucleosides, and acetyl-CoA from a starting set of simple food molecules, shedding light on the nature of autocatalytic networks that existed before the first cells arose from the elements on the early Earth

Results

Discussion

Material and methods

Findings

54. Ijiri A et al 2018 Deep-biosphere methane