Abstract
One of the most studied metabolic routes is the biosynthesis of histidine, especially in enterobacteria where a single compact operon composed of eight adjacent genes encodes the complete set of biosynthetic enzymes. It is still not clear how his genes were organized in the genome of the last universal common ancestor community. The aim of this work was to analyze the structure, organization, phylogenetic distribution, and degree of horizontal gene transfer (HGT) of his genes in the Bacteroidota-Rhodothermota-Balneolota-Chlorobiota superphylum, a group of phylogenetically close bacteria with different surviving strategies. The analysis of the large variety of his gene structures and organizations revealed different scenarios with genes organized in more or less compact—heterogeneous or homogeneous—operons, in suboperons, or in regulons. The organization of his genes in the extant members of the superphylum suggests that in the common ancestor of this group, genes were scattered throughout the chromosome and that different forces have driven the assembly of his genes in compact operons. Gene fusion events and/or paralog formation, HGT of single genes or entire operons between strains of the same or different taxonomic groups, and other molecular rearrangements shaped the his gene structure in this superphylum.
Highlights
The origin and evolution of metabolic pathways represent one of the most crucial events that occurred during molecular and cellular evolution [1], since they rendered the primordial cells less dependent on the exogenous supply of abiotically formed molecules.This issue is often linked to the origin and evolution of operons [2] and can be studied through either directed evolution experiments and/or the comparative analysis of genes involved in the same metabolic pathway
One of the most studied metabolic routes is the biosynthesis of histidine, which has been extensively studied in Salmonella enterica and Escherichia coli [3]
Histidine biosynthesis protein sequences were downloaded from UniProtKB
Summary
The origin and evolution of metabolic pathways represent one of the most crucial events that occurred during molecular and cellular evolution [1], since they rendered the primordial cells less dependent on the exogenous supply of abiotically formed molecules This issue is often linked to the origin and evolution of operons [2] and can be studied through either directed evolution experiments and/or the comparative analysis of genes involved in the same metabolic pathway. Three of the eight genes (hisD, hisNB, and hisIE) encode bifunctional enzymes, while two (hisH and hisF) encode a heterodimeric enzyme catalyzing a single biosynthetic step, for a total of 10 enzymatic reactions [4] This pathway represents an important metabolic crossroad since it is intimately connected to (at least) two important metabolic routes: nitrogen metabolism and de novo synthesis of purines. This interconnection is due to the activity of imidazole-glycerolphosphate synthase (IGPS), a heterodimeric enzyme composed of the glutaminase subunit
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