The Origin and Evolution of Operons: The Piecewise Building of the Proteobacterial Histidine Operon (original) (raw)
Related papers
Journal of Molecular Evolution, 1994
The hisA and hisF genes belong to the histidine operon that has been extensively studied in the enterobacteria Escherichia coli and Salmonella typhimurium where the hisA gene codes for the phosphoribosyl-5-amino-1 -phosphoribosyl-4-imidazolecarboxamide isomerase (EC 5.3.1.16) catalyzing the fourth step of the histidine biosynthetic pathway, and the hisF gene codes for a cyclase catalyzing the sixth reaction.
Proteobacterial Histidine-Biosynthetic Pathways Are Paraphyletic
Journal of Molecular Evolution, 2000
In Lactococcus lactis there is a protein, HisZ, in the histidine-biosynthetic operon that exhibits significant sequence identity with histidyl-tRNA synthetase (HisRS) but does not aminoacylate tRNA. HisRS homologs that, like HisZ, cannot aminoacylate tRNA are represented in a highly divergent set of bacteria (including an aquificale, cyanobacteria, firmicutes, and proteobacteria), yet are missing from other bacteria, including mycrobacteria and certain proteobacteria. Phylogenetic analysis of the HisRS and HisRS-like family suggests that the HisZ proteins form a monophyletic group that attaches outside the predominant bacterial HisRS clade. These observations are consistent with a model in which the absences of HisZ from bacteria are due to its loss during evolution. It has recently been shown that HisZ from L. lactis binds to the ATP-PRPP transferase (HisG) and that both HisZ and HisG are required for catalyzing the first reaction in histidine biosynthesis. Phylogenetic analysis of HisG sequences shows conclusively that proteobacterial HisG and histidinol dehydrogenase (HisD) sequences are paraphyletic and that the partition of the Proteobacteria associated with the presence/absence of HisZ corresponds to that based on HisG and HisD paraphyly. Our results suggest that horizontal gene transfer played an important role in the evolution of the regulation of histidine biosynthesis.
A study in evolution: The histidine utilization genes of enteric bacteria
Journal of Molecular Biology, 1979
The histidine utilization (hut) system, MIGCPUH, comprises two operons, whose promoters are M and P. The DNA segments of phage h vectors coding for the hut genes of Salmonella typhimurium and Klebsiella aerogenes were compared by using electron microscopy to study the nature of the hut DNA homology. The hut S. typhimuriumlhut K. aerogenes DNA heteroduplexes were spread and mounted for electron microscopy under more and more denaturing conditions. The homology between hut S. typhimurium and hut K. aerogenes is extensive but, as denaturing conditions make base-pairing more difficult, the regions of lower homology are melt,ed, while the regions of higher homology remain base-paired. The denat,uration map could be correlated with the genetic map by the use of Ahut S. typhimurium phages carrying different portions of the hut genome. The sequences with the highest homology are in the structural genes for the four enzymes, while the regulatory regions, the promoters and t,lre hut repressor gene, are much less homologous.
Evolution of the structure and chromosomal distribution of histidine biosynthetic genes
1998
A database of more than 100 histidine biosynthetic genes from different organisms belonging to the three primary domains has been analyzed, including those found in the now completely sequenced genomes of Haemophilus influenzae, Mycoplasma genitalium, Synechocystis sp., Methanococcus jannaschii, and Saccharomyces cerevisiae. The ubiquity of his genes suggests that it is a highly conserved pathway that was probably already present in the last common ancestor of all extant life. The chromosomal distribution of the his genes shows that the enterobacterial histidine operon structure is not the only possible organization, and that there is a diversity of gene arrays for the his pathway. Analysis of the available sequences shows that gene fusions (like those involved in the origin of theEscherichia coli and Salmonella typhimurium hisIE and hisB gene structures) are not universal. In contrast, the elongation event that led to the extant hisA gene from two homologous ancestral modules, as well as the subsequent paralogous duplication that originated hisF, appear to be irreversible and are conserved in all known organisms. The available evidence supports the hypothesis that histidine biosynthesis was assembled by a gene recruitment process.
The role of gene fusions in the evolution of metabolic pathways: the histidine biosynthesis case
BMC Evolutionary Biology, 2007
Background Histidine biosynthesis is one of the best characterized anabolic pathways. There is a large body of genetic and biochemical information available, including operon structure, gene expression, and increasingly larger sequence databases. For over forty years this pathway has been the subject of extensive studies, mainly in Escherichia coli and Salmonella enterica, in both of which details of histidine biosynthesis appear to be identical. In these two enterobacteria the pathway is unbranched, includes a number of unusual reactions, and consists of nine intermediates; his genes are arranged in a compact operon (hisGDC [NB]HAF [IE]), with three of them (hisNB, hisD and hisIE) coding for bifunctional enzymes. We performed a detailed analysis of his gene fusions in available genomes to understand the role of gene fusions in shaping this pathway. Results The analysis of HisA structures revealed that several gene elongation events are at the root of this protein family: internal duplication have been identified by structural superposition of the modules composing the TIM-barrel protein. Several his gene fusions happened in distinct taxonomic lineages; hisNB originated within γ -proteobacteria and after its appearance it was transferred to Campylobacter species (ε -proteobacteria) and to some Bacteria belonging to the CFB group. The transfer involved the entire his operon. The hisIE gene fusion was found in several taxonomic lineages and our results suggest that it probably happened several times in distinct lineages. Gene fusions involving hisIE and hisD genes (HIS4) and hisH and hisF genes (HIS7) took place in the Eukarya domain; the latter has been transferred to some δ -proteobacteria. Conclusion Gene duplication is the most widely known mechanism responsible for the origin and evolution of metabolic pathways; however, several other mechanisms might concur in the process of pathway assembly and gene fusion appeared to be one of the most important and common.
Microorganisms
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 thro...
Molecular Biology and Evolution, 2006
The formation mechanism of operons remains unresolved: operons may form by rearrangements within a genome or by acquisition of genes from other species, that is, horizontal gene transfer (HGT). One hindrance to its elucidation is the unavailability of a method to accurately identify HGT, although it is generally considered to occur. It is critically important first to select horizontally transferred (HT) genes reliably and then to determine the extent to which HGT is involved in operon formation. For this purpose, we considered indels in terms of gene clusters instead of individual genes and chose candidates of HT genes in 8 species of Escherichia, Shigella, and Salmonella based on the minimization of indels. To select a benchmark set of positively HT genes against which we can evaluate the candidate set, we devised another procedure using intergenetic alignments. Comparison with the benchmark set demonstrated the absence of a significant number of false positives in the candidate set, showing the high reliability of the method. Analyses of Escherichia coli K-12 operons revealed that although approximately 20 operons were probably gained from the last common ancestor of the 8 gamma-proteobacteria, deletion of intervening genes accounts for the formation of no operons, whereas horizontal transfer expanded 2 operons and introduced 4 entire operons. Based on these observations and reasoning, we suggest that the main mechanism of operon gain is HGT rather than intragenomic rearrangements. We propose that genes with related essential functions tend to reside in conserved operons, whereas genes in nonconserved operons mostly confer slight advantage to the organisms and frequently undergo horizontal transfer and decay. HT genes constitute at least 5.5% of the genes in the 8 species and approximately 45% of which originate from other gamma-proteobacteria. Genes involved in viral functions and mobile and extrachromosomal element functions are HT more often than expected. This finding indicates frequent mediation of HGT by bacteriophages. On the other hand, not only informational genes (those involved in transcription, translation, and related processes) but also operational genes (those involved in housekeeping) are HT less frequently than expected.
Molecular Evolution of hisB Genes
Journal of Molecular Evolution, 2004
The sixth and eighth steps of histidine biosynthesis are catalyzed by an imidazole glycerol-phosphate (IGP) dehydratase (EC 4.2.1.19) and by a histidinol-phosphate (HOL-P) phosphatase (EC 3.1.3.15), respectively. In the enterobacteria, in Campylobacter jejuni and in Xylella/Xanthomonas the two activities are associated with a single bifunctional polypeptide encoded by hisB. On the other hand, in Archaea, Eucarya, and most Bacteria the two activities are encoded by two separate genes. In this work we report a comparative analysis of the amino acid sequence of all the available HisB proteins, which allowed us to depict a likely evolutionary pathway leading to the present-day bifunctional hisB gene. According to the model that we propose, the bifunctional hisB gene is the result of a fusion event between two independent cistrons joined by domain-shuffling. The fusion event occurred recently in evolution, very likely in the proteobacterial lineage after the separation of the γ- and the β-subdivisions. Data obtained in this work established that a paralogous duplication event of an ancestral DDDD phosphatase encoding gene originated both the HOL-P phosphatase moiety of the E. coli hisB gene and the gmhB gene coding for a DDDD phosphatase, which is involved in the biosynthesis of a precursor of the inner core of the outer membrane lipopolysaccharides (LPS).
Inference from Proteobacterial Operons Shows Piecewise Organization: A Reply to Price et al
Journal of Molecular Evolution, 2006
IntroductionPrice and collaborators (2006; preceding article ) have recently reported an interesting and exhaustive analysis of his gene orders in a large number of bacterial genomes deposited in the MicrobesOnline database ( http://www.microbesonline.org). This, coupled with a phylogenetic analysis using distance-based methods of the His concatamers, showed that a unified hisGDC(NB)BHAF(IE) operon is present in many lineages. This result has led the authors to hypothesize that this operon is ancient, an assumption that is in partial disagreement with our previous results (Fani et al. 2005). However, our work did not focus on the evolution of his operons in general (i.e., in all completed genomes) but on the construction of the proteobacterial operons. Our main conclusion was that the E. coli-type operon was constructed piecewise during proteobacterial evolution starting from a proteobacterial ancestor whose genome probably contained a set of scattered his genes (or only partially clus