Promiscuous Pathogenicity Islands and Phylogeny of Pathogenic Streptomyces spp.

Abstract

Approximately 10 Streptomyces species cause disease on underground plant structures. The most economically important of these is potato scab, and the most studied of these pathogens is Streptomyces scabiei (syn. S. scabies). The main pathogenicity determinant of scab-causing Streptomyces species is a nitrated diketopiperazine, known as thaxtomin A (ThxA). In the pathogenic species Streptomyces turgidiscabies, ThxA biosynthetic genes reside on a mobile pathogenicity island (PAI). However, the mobilization of PAIs in other Streptomyces species remains uncharacterized. Here, we investigated the mobilization of the PAI of S. scabiei 87-22. Based on whole genome sequences, we inferred the evolutionary relationships of pathogenic Streptomyces species and discovered that Streptomyces sp. strain 96-12, a novel pathogenic species isolated from potatoes in Egypt, was phylogenetically grouped with nonpathogenic species rather than with known pathogenic species. We also found that Streptomyces sp. strain 96-12 contains a PAI that is almost identical to the PAI in S. scabiei 87-22, despite significant differences in their genome sequences. This suggested direct or indirect in vivo mobilization of the PAI between S. scabiei and nonpathogenic Streptomyces species. To test whether the S. scabiei 87-22 PAI could, indeed, be mobilized, S. scabiei 87-22 deletion mutants containing antibiotic resistance markers in the PAI were mated with Streptomyces diastatochromogenes, a nonpathogenic species. The PAI of S. scabiei was site-specifically inserted into the aviX1 gene of S. diastatochromogenes and conferred pathogenicity in radish seedling assays. Our results demonstrated that S. scabiei, the earliest described Streptomyces pathogen, could be the source of a PAI responsible for the emergence of novel pathogenic species.

Genetic background affects pathogenicity island function and pathogen emergence in Streptomyces

“…A soft nutrient agar overlay containing antibiotics was used to select for transconjugants. In our previous study, we demonstrated the mobilization of the complete TR element or TR2 alone between S. scabiei and S. diastatochromogenes (Zhang et al ., ). PAIst was also found to excise from the chromosome in three distinct forms: as the 105‐kb region, the 569‐kb region or the entire 674‐kb PAIst (Huguet‐Tapia et al ., ).…”

“…To explore the mobilization of regions containing the ThxA biosynthetic genes, we used S. turgidiscabies Car811 with a thiostrepton resistance (thio R ) marker inserted in its PAIst (Kers et al, 2005) and a mutant strain of S. scabiei 87-22 created by replacing its lantibiotic biosynthetic genes lanA (SCAB_32021) and lanB (SCAB_32031) located in TR with the hygromycin B resistance (hyg R ) marker (hereafter referred to as S. scabiei DlanAB) (Zhang et al, 2016). A schematic genetic organization of the S. scabiei TR with the hyg R marker and the S. turgidiscabies PAIst with the thio R marker is shown in Fig.…”

“…PAIst also encodes another two secreted proteins implicated in virulence, namely tomatinase (TomA) ) and a necrogenic protein (Nec1) (Bukhalid et al, 1998). Recently, we have demonstrated that, in S. scabiei, the ThxA biosynthetic cluster is also mobilizable (Zhang and Loria, 2017;Zhang et al, 2016). The cluster is located on a 177-kb PAI, called the toxicogenic region (TR), which can be separated into two subregions (TR1 and TR2) by three attachment (att) sites (Chapleau et al, 2016).…”

“…The cluster is located on a 177-kb PAI, called the toxicogenic region (TR), which can be separated into two subregions (TR1 and TR2) by three attachment (att) sites (Chapleau et al, 2016). TR1 contains the ThxA biosynthetic cluster and TR2 contains the integrative and conjugative element (Chapleau et al, 2016;Zhang et al, 2016). We have shown previously that mobilization of the 674-kb PAIst from S. turgidiscabies into S. coelicolor does not confer a pathogenicity phenotype or Thx production (Kers et al, 2005).…”

Effects of AttM lactonase on the pathogenicity ofStreptomyces scabies

“…is regarded as an acquired trait since the pathogenicity island (PAI) harbouring the main virulence determinants is found to be mobilized from pathogenic to nonpathogenic species among streptomycetes, thereby giving rise to the newly emerged pathogenic strains (Wanner and Kirk ; Zhang et al . ). Given that S. scabies is the most ancient phytopathogenic Streptomyces sp.…”