Diverse mobile genetic elements shaped the evolution of streptomyces virulence

Authors: WEISBERG, ALEXANDRA - Oregon State University; PEARCE, EMMA - Oregon State University; Kramer, Charles; CHANG, JEFF - Oregon State University; Clarke, Christopher

Submitted to: Microbial Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/22/2023
Publication Date: 11/6/2023
Citation: Weisberg, A., Pearce, E., Kramer, C.G., Chang, J., Clarke, C.R. 2023. Diverse mobile genetic elements shaped the evolution of streptomyces virulence. Microbial Genomics. https://doi.org/10.1099/mgen.0.001127.
DOI: https://doi.org/10.1099/mgen.0.001127

Interpretive Summary: Streptomyces is a diverse genus of bacteria that includes several species that can cause common scab disease on potato and other tuber and root crops. The primary means by which Streptomyces causes plant disease is the toxin Thaxtomin A. We performed whole genome sequencing on 174 strains of Streptomyces to characterize the diversity of disease-causing members and identify the diversity of mobile genetic elements in the bacterial genome that contain disease related genes and can be transferred between Streptomyces species. Surprisingly, our analyses suggests that natural transfer of the disease-related genes leading to novel pathogenic species emergence is exceedingly rare. Moreover, the analyses suggest that recent spread of the pathogen between grower field sites is also rare. However, spread of the pathogen appeared to be common up until approximately the last one-hundred years. These results suggests that the implementation of certified disease-free seed potato production systems significantly reduced spread of the pathogen. The disease severity or virulence of 60 of the strains was also measured, but surprisingly neither species nor repertoire of virulence genes was predictive of disease severity suggesting that unknown factors contribute to strain virulence. These results will guide further research to develop control measures for common scab disease.

Technical Abstract: Mobile genetic elements can innovate bacteria with new traits. In plant pathogenic Streptomyces, frequent and recent acquisition of integrative and conjugative or mobilizable genetic elements is predicted to lead to the emergence of new lineages that gained the capacity to synthesize Thaxtomin A and cause common scab disease on tuber and root crops. Here, we identified components of the Streptomyces-potato pathosystem implicated in virulence and investigated them as a nested and interacting system to reevaluate evolutionary models. We sequenced and analyzed genomes of 174 strains isolated from over six decades of sampling primarily from field-grown potatoes. Virulence genes were associated to multiple subtypes of genetic elements differing in mechanisms of transmission and evolutionary histories. Evidence is consistent with few ancient acquisition events followed by recurrent loss or swaps of elements carrying Thaxtomin A-associated genes. Subtypes of another genetic element implicated in virulence are more distributed across Streptomyces. However, neither the subtype classification of genetic elements containing virulence genes nor taxonomic identity was predictive of pathogenicity on potato. Last, findings suggested that phytopathogenic strains are generally endemic to potato fields and some lineages were established by historical spread and further dispersed by few recent transmission events. Results from a system-wide characterization refine our understanding by revealing multiple mechanisms that gene and bacterial dispersion have had on shaping the evolution of a Gram-positive pathogen in agricultural settings.