Subtelomeres are fast-evolving regions of the Streptomyces linear chromosome

Abstract

Streptomyces possess a large linear chromosome (6–12 Mb) consisting of a conserved central region flanked by variable arms covering several megabases. In order to study the evolution of the chromosome across evolutionary times, a representative panel of Streptomyces strains and species (125) whose chromosomes are completely sequenced and assembled was selected. The pan-genome of the genus was modelled and shown to be open with a core-genome reaching 1018 genes. The evolution of Streptomyces chromosome was analysed by carrying out pairwise comparisons, and by monitoring indexes measuring the conservation of genes (presence/absence) and their synteny along the chromosome. Using the phylogenetic depth offered by the chosen panel, it was possible to infer that within the central region of the chromosome, the core-genes form a highly conserved organization, which can reveal the existence of an ancestral chromosomal skeleton. Conversely, the chromosomal arms, enriched in variable genes evolved faster than the central region under the combined effect of rearrangements and addition of new information from horizontal gene transfer. The genes hosted in these regions may be localized there because of the adaptive advantage that their rapid evolution may confer. We speculate that (i) within a bacterial population, the variability of these genes may contribute to the establishment of social characters by the production of ‘public goods’ (ii) at the evolutionary scale, this variability contributes to the diversification of the genetic pool of the bacteria.

Pan-Genome of the Genus Streptomyces and Prioritization of Biosynthetic Gene Clusters With Potential to Produce Antibiotic Compounds

“…Besides, many of the genomes the authors used are fragmented, which can introduce errors in pan-genome calculations ( Tonkin-Hill et al, 2020 ). A recent paper reported a pan-genome size of 106,000 genes and 1,018 core genes by using 125 complete Streptomyces genomes and a percent similarity threshold of 40% in BLASTp ( Lorenzi et al, 2021 ); this might explain the differences with the present study, although, the core genes number is quite similar to the soft-core genes that we calculated. What is remarkable in these two approaches is the similar value of gamma (γ) in the mathematical fit of the genome size (0.62 compared to the 0.6 obtained in this work).…”

Evolution of genome fragility enables microbial division of labor

“…core region located at their centromere, and a telomeric region which is prone to various forms of recombination and instability and contains much of the accessory genes [40,41]. This leads to high within-and between-species variability at the chromosome ends [42]. Both fragile sites (including genomic inverted repeats and other recombination hotspots, associated to intrachromosomal recombination and to mobile genetic elements)…”

“…It is well known that Streptomyces genomes contain a conserved (mutationally quiet) core region located at their centromere, and a telomeric region which is prone to various forms of recombination and instability and contains much of the accessory genes [40, 41]. This leads to high within- and between-species variability at the chromosome ends [42]. Both fragile sites (including genomic inverted repeats and other recombination hotspots, associated to intrachromosomal recombination and to mobile genetic elements) and biosynthetic clusters are unevenly distributed in Streptomyces genomes [19, 41, 43], suggesting that their position is highly non random.…”

Ribosomal RNA operons define a central functional compartment in the Streptomyces chromosome

“…ambofaciens, Streptomyces venezuelae) to access intra-species evolution and include strains for which -omics data were available for further analyses. We re-annotated all genomes and detected orthologous genes, as previously described (Lorenzi et al 2021).…”

“…previously described(McDonald et Currie 2017;Lorenzi et al 2021;Caicedo-Montoya, Manzo-Ruiz, et Ríos-Estepa 2021) division of the Streptomyces genus into two main monophyletic clades (clades '1' and '2') and other lineages further referred to as group 'O' (for 'others') (Figure2). By crossing this tree with genome nomenclature based on rrn categories and dnaA orientation, we propose a parsimonious scenario explaining the diversity observed in the panel of 127 analyzed genomes.…”