Ancient Origin of the Tryptophan Operon and the Dynamics of Evolutionary Change

Abstract

SUMMARY The seven conserved enzymatic domains required for tryptophan (Trp) biosynthesis are encoded in seven genetic regions that are organized differently (whole-pathway operons, multiple partial-pathway operons, and dispersed genes) in prokaryotes. A comparative bioinformatics evaluation of the conservation and organization of the genes of Trp biosynthesis in prokaryotic operons should serve as an excellent model for assessing the feasibility of predicting the evolutionary histories of genes and operons associated with other biochemical pathways. These comparisons should provide a better understanding of possible explanations for differences in operon organization in different organisms at a genomics level. These analyses may also permit identification of some of the prevailing forces that dictated specific gene rearrangements during the course of evolution. Operons concerned with Trp biosynthesis in prokaryotes have been in a dynamic state of flux. Analysis of closely related organisms among the Bacteria at various phylogenetic nodes reveals many examples of operon scission, gene dispersal, gene fusion, gene scrambling, and gene loss from which the direction of evolutionary events can be deduced. Two milestone evolutionary events have been mapped to the 16S rRNA tree of Bacteria, one splitting the operon in two, and the other rejoining it by gene fusion. The Archaea, though less resolved due to a lesser genome representation, appear to exhibit more gene scrambling than the Bacteria. The trp operon appears to have been an ancient innovation; it was already present in the common ancestor of Bacteria and Archaea. Although the operon has been subjected, even in recent times, to dynamic changes in gene rearrangement, the ancestral gene order can be deduced with confidence. The evolutionary history of the genes of the pathway is discernible in rough outline as a vertical line of descent, with events of lateral gene transfer or paralogy enriching the analysis as interesting features that can be distinguished. As additional genomes are thoroughly analyzed, an increasingly refined resolution of the sequential evolutionary steps is clearly possible. These comparisons suggest that present-day trp operons that possess finely tuned regulatory features are under strong positive selection and are able to resist the disruptive evolutionary events that may be experienced by simpler, poorly regulated operons.

Cohesion Group Approach for Evolutionary Analysis of Aspartokinase, an Enzyme That Feeds a Branched Network of Many Biochemical Pathways

“…In addition, the true Alteromonadales in the lower Gammaproteobacteria (but not Marinobacter and Saccharophagus) all possess the three character states depicted, which are present throughout all of the lower Gammaproteobacteria (except for some cases of recent wholesale reductive evolution in pathogens and endosymbionts). These character states are two fusions (aroH I -tyrA [6] and trpD-trpC [90]), as well as a fully merged trp operon from former split-operon components (90). It is noteworthy that our assertion that the taxonomic placement of Marinobacter and Saccharophagus is erroneous received strong confirmation from the results of Wu and Eison (88), in whose genome tree the orders Alteromonadales, Oceanospiralles, and Pseudomonadales were interspersed and paraphyletic.…”

“…The cohesion group approach for evolutionary analysis of biochemical pathways is illustrated by very detailed work done with the tryptophan (89,90) and the tyrosine (6) branches of aromatic amino acid biosynthesis. Individual cohesion groups provide a manageable assemblage of subsets of a given protein (or protein concatenates) that have evolutionary continuity.…”

“…The evolutionary times for acquisition of four character states (circled letters A, B, C, and D) are shown at appropriate positions on the tree. Fusion A is for genes encoding cyclohexadienyl dehydrogenase (tyrA) and enolpyruvyl-shikimate-3-phosphate synthase (aroF), fusion B is for genes encoding indoleglycerol phosphate synthase (trpD) and phosphoribosyl-anthranilate isomerase (trpC), fusion D is for genes encoding chorismate mutase (aroH) and cyclohexadienyl dehydrogenase (tyrA), and evolutionary event C is the merging of the split-operon components of the trp operon (90). The current designations of two organisms at the upper right as Alteromonadales is considered highly doubtful, as indicated by question marks, because unlike the five Alteromonadales organisms shown in yellow, they possess character state A and they lack character states B, C, and D. …”

Transcriptional Bursting in the Tryptophan Operon of E. coli and Its Effect on the System Stochastic Dynamics

“…The trp operon is regulated by three different negative-feedback mechanisms: repression, transcription attenuation, and enzyme inhibition. Below these regulatory mechanisms are briefly reviewed based on Grillo et al, 1999;Jeeves et al, 1999;Xie et al, 2003;Yanofsky, 2000;Yanofsky & Crawford, 1987). The reader should consult Figure 1 for a better understanding.…”

Az anyagcsere szerkezetének hatása a genetikai interakciókra és a genomszerveződésre

“…Omelchenko, 2003) fajban mindkét operonra érvényes hasonlóságokat találtak (például ismeretlen funkciójú gének inzerciója az operonokba). Ez a fajok között eltérő, míg fajon belül a különböző operonokra egyformán érvényes szelekciós hatásokra utalhat (Xie et al, 2003). Az egyes baktériumcsoportok alakja (például coccus, bacillus) és a sejtfal felépítésében közreműködő géncsoport génsorrendje közötti kapcsolat is szelekciós hatás jelenlétét sugallhatja (Tamames et al, 2001).…”