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MBE Advance Access published online on September 8, 2004
Molecular Biology and Evolution, doi:10.1093/molbev/msh253
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved
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Accepted August 12, 2004

Research Article

Integrating the Universal Metabolism into a Phylogenetic Analysis

Chomin Cunchillos 1 and Guillaume Lecointre 2*

1 Institut Charles Darwin International, BP 70, 93230 Romainville, FRANCE
2 UMR 7138 "Systématique, Adaptation, Evolution", Département "Systématique et Evolution", Muséum National d'Histoire Naturelle, 43 rue Cuvier, 75231 PARIS cedex 05 FRANCE.

* To whom correspondence should be addressed. E-mail: lecointr{at}mnhn.fr.


  Abstract

The darwinian concept of "descent with modification" applies to metabolic pathways: pathways sharing similarities must have inherited them from an exclusive, hypothetical ancestral pathway. Comparative anatomy of biochemical pathways is performed using five criteria of homology. Primary homologies of "type I" were defined as several pathways sharing the same enzyme with high specificity for its substrate. Primary homologies of "type II" were defined as the sharing of similar enzymatic functions, or cofactors, or functional family, or recurrence of a set of reactions. Standard cladistic analysis is used to infer the evolutionary history of metabolic development and the relative ordering of biochemical reactions through time, from a single matrix integrating the whole basic universal metabolism. The cladogram shows that the earliest pathways to emerge are metabolism of amino acids of groups I and II (Asp, Asn, Glu, Gln). The earliest enzymatic functions are mostly linked to amino acid catabolism: deamination, transamination, and decarboxylation. For some amino acids, catabolism and biosynthesis occur at the same time (Asp, Glu, Lys, Met). Catabolism precedes anabolism for Asn, Gln, Arg, Trp, His, Tyr, Phe; and anabolism precedes catabolism for Pro, Ala, Leu, Val, Ile, Cys, Gly, Ser, Thr. The urea cycle evolves from arginine synthesis. Metabolism of fatty acids and sugars develops after the full development of metabolism of amino acids of groups I and II, and they are associated with the anabolism of amino acids of groups III and IV. Syntheses of aromatic amino acids are branched within sugar metabolism. The Krebs cycle occurs relatively late after the setting of metabolism of amino acids of groups I and II. One portion of the Krebs cycle has a catabolic origin, while the other portion has an anabolic origin in pathways of amino acids of groups III and IV. It is not possible to order glycolysis and gluconeogenesis with regard to the Krebs cycle, as they all belong to "period 6". Pentose-Phosphate and Calvin cycles are later (periods 7 and 8 respectively). Cladistic analysis of the structure of biochemical pathways makes hypotheses in biochemical evolution explicit and parsimonious.

Keywords: metabolism; metabolic pathways; biochemical evolution.
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