Massive Gene Flux Drives Genome Diversity between Sympatric Streptomyces Conspecifics

Abstract

In this work, by comparing genomes of closely related individuals of Streptomyces isolated at a spatial microscale (millimeters or centimeters), we investigated the extent and impact of horizontal gene transfer in the diversification of a natural Streptomyces population. We show that despite these conspecific strains sharing a recent common ancestor, all harbored significantly different gene contents, implying massive and rapid gene flux. The accessory genome of the strains was distributed across insertion/deletion events (indels) ranging from one to several hundreds of genes. Indels were preferentially located in the arms of the linear chromosomes (ca. 12 Mb) and appeared to form recombination hot spots. Some of them harbored biosynthetic gene clusters (BGCs) whose products confer an inhibitory capacity and may constitute public goods that can favor the cohesiveness of the bacterial population. Moreover, a significant proportion of these variable genes were either plasmid borne or harbored signatures of actinomycete integrative and conjugative elements (AICEs). We propose that conjugation is the main driver for the indel flux and diversity in Streptomyces populations. IMPORTANCE Horizontal gene transfer is a rapid and efficient way to diversify bacterial gene pools. Currently, little is known about this gene flux within natural soil populations. Using comparative genomics of Streptomyces strains belonging to the same species and isolated at microscale, we reveal frequent transfer of a significant fraction of the pangenome. We show that it occurs at a time scale enabling the population to diversify and to cope with its changing environment, notably, through the production of public goods.

On the Risks of Phylogeny-Based Strain Prioritization for Drug Discovery: Streptomyces lunaelactis as a Case Study

“…Previous 16S rRNA-based phylogeny analyses suggested that 18 strains collected during our various campaigns aimed at isolating actinomycetes from karstic environments belong to the species Streptomyces lunaelactis [ 13 , 14 , 15 ]. However, 16S rRNA is a weak marker for species determination in streptomycetes and we therefore performed MLSA using concatenated full-length sequences of housekeeping genes atpD , gyrB , recA , rpoB , and trpB .…”

“…However, genome assemblies of some S. albus strains contain many contigs on which some biosynthetic gene clusters (BGCs) might be scattered, thereby resulting in an overestimation of the total number of BGCs [ 9 ]. In a more recent study, Tidjani AR and colleagues showed, by comparative genomics of Streptomyces strains belonging to the same species and isolated at the microscale, that almost-clonal strains can present important genetic content diversity providing them with unique metabolite production capabilities [ 13 ].…”

Genome Sequences of Five Streptomyces Strains Isolated at Microscale

“…to a previously isolated cluster of strains (identical 16S rRNA gene sequences) (8,14) that was closely related to Streptomyces olivochromogenes DSM 40451 (99.9% identity in 16S rRNA gene sequences) (15). The strains RLB1-33, RPA4-2, and S1D4-11 and Streptomyces mirabilis CSSP107 exhibited identities of 99.9% to 99.2% in their 16S rRNA genes, indicating that they might belong to the same species or constitute sister species.…”

Genome Sequences of 11 Conspecific Streptomyces sp. Strains

“…The 11 strains selected showed identical 16S rRNA gene sequences and minimal MLSA divergence. These strains are related to Streptomyces olivochromogenes (strain DSM40451), with an average identity of 99.93% for the 16S rRNA gene sequences (8). A hybrid assembly using Oxford Nanopore technology for scaffolding and Illumina technology for sequence improvement was performed (Table 1).…”