Genetic background affects pathogenicity island function and pathogen emergence in Streptomyces

Abstract

With few exceptions, thaxtomin A (ThxA), a nitrated diketopiperazine, is the pathogenicity determinant for plant-pathogenic Streptomyces species. In Streptomyces scabiei (syn. S. scabies), the ThxA biosynthetic cluster is located within a 177-kb mobile pathogenicity island (PAI), called the toxicogenic region (TR). In S. turgidiscabies, the ThxA biosynthetic cluster is located within a 674-kb pathogenicity island (PAIst). The emergence of new plant pathogens occurs in this genus, but not frequently. This raises the question of whether the mobilization of these pathogenicity regions, through mating, is widespread and whether TR and PAIst can confer plant pathogenicity. We showed that ThxA biosynthetic clusters on TR and PAIst were transferred into strains from five non-pathogenic Streptomyces species through mating with S. scabiei and S. turgidiscabies. However, not all of the transconjugants produced ThxA and exhibited the virulence phenotype, indicating that the genetic background of the recipient strains affects the functionality of the ThxA biosynthetic cluster and therefore would be expected to affect the emergence of novel pathogenic Streptomyces species. Thxs have been patented as natural herbicides, but have yet to be commercialized. Our results also demonstrated the potential of the heterologous production of ThxA as a natural and biodegradable herbicide in non-pathogenic Streptomyces species.

An Integrative Approach for the Characterization of Plant-Pathogenic Streptomyces spp. Strains Based on Metabolomic, Bioactivity, and Phylogenetic Analysis

“…Indeed, the txtA gene was absent in all tested S. niveiscabiei strains, whereas the presence of this gene is reported in the type strain of this species; NRRL B-24457 ( Park et al, 2003a ). We suggest that these strains might have lost this gene or BGC, as has been observed with some strains from different species ( S. scabies and S. acidiscabies) ( Zhang et al, 2016 , 2018 ).…”

“…Indeed, the txtA gene was absent in all tested S. niveiscabiei strains, whereas the presence of this gene is reported in the type strain of this species; NRRL B-24457 (Park et al, 2003a). We suggest that these strains might have lost this gene or BGC, as has been observed with some strains from different species (S. scabies and S. acidiscabies) (Zhang et al, 2016(Zhang et al, , 2018. Interestingly, apart from detecting the presence of DMSN in strain St1015, which was used as reference strain, it was detected in culture supernatants of other five S. niveiscabiei strains.…”

Secondary Metabolites Isolated From Streptomyces sp. MJM3055 and Their Cytotoxicity Against Jurkat Cells

“…1 The species are widely distributed in the most diverse habitats, like polar territories, deserts, highlands, insects, plant stems, and marine sediments. [2][3][4][5] Streptomyces species have shown an outstanding capacity for the production of secondary metabolites, many of which were broadly used for the treatment of human diseases. Secondary metabolites produced by Streptomyces species belong to different classes of compounds; polyketides, peptides, polyketide-peptide hybrids, aminoglycosides, and polyene macrolides have been characterized, with different biological activities, including antibacterial, antifungal, anticancer, and immune suppression.…”

High-Yield Production of Herbicidal Thaxtomins and Thaxtomin Analogs in a Nonpathogenic Streptomyces Strain

“…Indeed, S. albus J1074 has been used to produce a number of structurally diverse natural products of actinomycete and nonstreptomycete origins (31)(32)(33)(34)(35)(36)(37) and can demonstrate a higher productivity than other hosts (38)(39)(40)(41). Very recently, we expressed mobile pathogenicity islands (PAIs) (177 kb and 674 kb) from two pathogenic Streptomyces strains, which contain the thaxtomin gene cluster, mobile elements, and others, in five nonpathogenic Streptomyces hosts, including S. albus J1074, S. avermitilis NRRL8165, S. coelicolor M145, S. diastatochromogenes ATCC 12309, and S. lividans 1326 (42). Strikingly, S. albus J1074 expressing the 177-kb PAI from S. scabiei produced the highest level of thaxtomins among all 10 engineered strains and two native producers when cultured in Thx defined medium supplemented with 1% cellobiose (TDMc).…”

“…This result indicates the significant influences of the genetic backgrounds of expression hosts on gene cluster expression and clearly illustrates the attractive capability of S. albus J1074 in heterologous production of natural products. However, the PAI-based production of thaxtomins in S. albus J1074 has limitations to developing industrial processes, e.g., the mobility nature of PAI, potentially leading to the genetic instability of the production strain, technical difficulties in engineering the biosynthetic gene cluster for further improving the production yield, and cost and safety concerns regarding the use of two antibiotics in the fermentation media (42).…”