The Histidine Biosynthetic Genes in the Superphylum Bacteroidota-Rhodothermota-Balneolota-Chlorobiota: Insights into the Evolution of Gene Structure and Organization

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.

Synergistic Effects and Toxic Mechanism of Phosphine with Ethyl Formate against Citrus Mealybug (Planococcus citri)

“…Another down-regulated protein is phosphoribosyl formimino-5-aminoimidazole carboxamideribotide isomerase which is involved in histidine biosynthesis. The decreased expression of this enzyme may reduce histidine production during the fumigation and inhibit the regulation and metabolism of trace elements, and the repair and growth of tissue [38,39]. Therefore, individual fumigation of EF and PH 3 can inhibit similar biochemical processes in P. citri adults and they are considered to be their presumable target sites.…”

Proposal to include the categories kingdom and domain in the International Code of Nomenclature of Prokaryotes

“…Under the ICNP, this approach would contravene Principle 4 [1,2]. For instance, the PVC superphylum was alternatively called Bacteroidetes-Chlorobi superphylum [46][47][48] or Bacteroidota-Rhodothermota-Balneolota-Chlorobiota superphylum [49,50] but one also finds Bacteroidetes-Ignavibacterium-Chlorobi superphylum [51] and Bacteroidetes-Chlorobi-Ignavibacteriae superphylum [52]. It may be identical to the Chlorobium-Cytophaga kingdom mentioned by Woese [53].…”

The Operon as a Conundrum of Gene Dynamics and Biochemical Constraints: What We Have Learned from Histidine Biosynthesis

“…The necessity to produce histidine suggests that this biosynthetic pathway is ancient and that it was already part of the metabolic abilities of the LCA [ 44 , 61 , 62 ]. However, the results of the evolutionary comparison of the his genes in the three cellular domains clearly indicate that, after the divergence from the LCA, his gene organization, structure, and order have faced extensive reorganizations in the three cell lineages [ 60 , 63 , 64 ].…”

“…Since the first studies performed on histidine biosynthetic genes, results showed that his genes may also be organized in sub-operons (e.g., in Streptomyces coelicolor [ 79 ], B. subtilis and Azospirillum brasilense [ 80 , 81 ] or scattered along the chromosomal DNA [ 82 , 83 ]. Comparative analyses of the structure and organization of his biosynthetic genes performed on proteobacteria [ 13 ], archaea [ 84 ], and the Bacteroidota-Rhodothermota-Balneolota-Chlorobiota (BRBC) superphylum [ 64 ], highlighted a heterogeneous disposition and organization of his genes, i.e., genes assembled in more or less compact operons, sub-operons, or regulons (defined as sets of functionally related genes scattered throughout the genome that can be efficiently co-regulated).…”