Abstract
BackgroundIt is generally assumed that primordial cells had small genomes with simple genes coding for enzymes able to react with a wide range of chemically related substrates, interconnecting different metabolic routes. New genes coding for enzymes with a narrowed substrate specificity arose by paralogous duplication(s) of ancestral ones and evolutionary divergence. In this way new metabolic pathways were built up by primordial cells. Useful hints to disclose the origin and evolution of ancestral metabolic routes and their interconnections can be obtained by comparing sequences of enzymes involved in the same or different metabolic routes. From this viewpoint, the lysine, arginine, and leucine biosynthetic routes represent very interesting study-models. Some of the lys, arg and leu genes are paralogs; this led to the suggestion that their ancestor genes might interconnect the three pathways. The aim of this work was to trace the evolutionary pathway leading to the appearance of the extant biosynthetic routes and to try to disclose the interrelationships existing between them and other pathways in the early stages of cellular evolution.ResultsThe comparative analysis of the genes involved in the biosynthesis of lysine, leucine, and arginine, their phylogenetic distribution and analysis revealed that the extant metabolic "grids" and their interrelationships might be the outcome of a cascade of duplication of ancestral genes that, according to the patchwork hypothesis, coded for unspecific enzymes able to react with a wide range of substrates. These genes belonged to a single common pathway in which the three biosynthetic routes were highly interconnected between them and also to methionine, threonine, and cell wall biosynthesis. A possible evolutionary model leading to the extant metabolic scenarios was also depicted.ConclusionThe whole body of data obtained in this work suggests that primordial cells synthesized leucine, lysine, and arginine through a single common metabolic pathway, whose genes underwent a set of duplication events, most of which can have predated the appearance of the last common universal ancestor of the three cell domains (Archaea, Bacteria, and Eucaryotes). The model proposes a relative timing for the appearance of the three routes and also suggests a possible evolutionary pathway for the assembly of bacterial cell-wall.
Highlights
It is generally assumed that primordial cells had small genomes with simple genes coding for enzymes able to react with a wide range of chemically related substrates, interconnecting different metabolic routes
The duplication event(s) followed by evolutionary divergence, allowing gaining of novel metabolic capabilities, permitted the new metabolic pathways to be less branched and interconnected to each other. How can this issue be studied? Useful hints to disclose the origin and evolution of metabolic pathways and the possible ancestral interrelationships between different routes may be obtained by comparing the sequence and the structure of genes of the same and different routes fromorganisms belonging to the three cells domains (Archaea, Bacteria and Eucarya)
The phylogenetic analysis performed allowed us to determine a possible relative timing of the appearance of genes that are involved in the extant lysine (DAP) and arginine biosynthetic routes
Summary
It is generally assumed that primordial cells had small genomes with simple genes coding for enzymes able to react with a wide range of chemically related substrates, interconnecting different metabolic routes. Useful hints to disclose the origin and evolution of metabolic pathways and the possible ancestral interrelationships between different routes may be obtained by comparing the sequence and the structure of genes (and/or the products they code for) of the same and different routes from (micro)organisms belonging to the three cells domains (Archaea, Bacteria and Eucarya). In this context the lysine, arginine, and leucine biosynthetic pathways represent interesting study-models. The high degree of sequence similarity shared by these enzymes led to the suggestion that: i) the assembly of both the DAP and AAA routes might be explained as the outcome of a series of gene duplication events followed by specialization [19], ii) the DAP route should represent the ancestral pathway leading to lysine and, iii) the AAA pathway should be a more recent invention of evolution[19]
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