Abstract
Actinomycetes are generally recognized as a diverse group of gram-positive, mycelium-forming, soil bacteria that play an important role in mineralization processes and plant health, being Streptomyces the most well-known genus from this group. Although plant pathogenicity is a rare attribute in this genus, some species have significant impact worldwide due to their ability to cause important crop diseases such as potato common scab (CS). In this work, an integrative approach was applied to investigate the pathogenic potential of Streptomyces spp. isolates obtained from a local collection of actinomycetes isolated from potato fields. Secretion of phytotoxic compounds was verified in most pathogenic strains from our collection (27 out of 29), and we followed metabolomic analysis to investigate those phytotoxins. We first evaluated the production of the known phytotoxins thaxtomin A (TXT) and desmethylmensacarcin (DMSN) in phytotoxic Streptomyces spp. by HPLC analysis, resulting in 17 TXT and 6 DMSN producers. In addition, NMR-based metabolomic models were able to classify strains according to their phytotoxicity, and metabolomic data was also used to infer chemotaxonomy within pathogenic species. A correlation between phylogeny and the production of distinct phytotoxins was found, supporting the idea that there are “species specific” metabolites produced by this genus. The recently discovered polyketide DMSN was associated unequivocally with S. niveiscabiei strains and was not produced by other species in the growth conditions employed. Two S. niveiscabiei and two S. puniciscabiei phytotoxic strains that did not produce TXT nor DMSN suggest the production of other kind of metabolites involved in phytotoxicity, and allowed the prioritization of these strains for further chemical studies. Indeed, we found two S. niveiscabiei strains whose supernatants were not phytotoxic in the radish assay, suggesting other pathogenic mechanisms involved. We believe our work will be useful to help understand relations between metabolites and phylogenetic clades within actinomycetes.
Highlights
As producers of two-thirds of all known antibiotics and many other bioactive compounds, actinomycetes are a rich source of secondary metabolites
Thaxtomins have been identified as essential pathogenicity determinants within plant-pathogenic Streptomyces species
Recent studies have shown that other phytotoxic compounds contribute to the development of common scab (CS), like some specialized metabolites that were not previously known to exhibit phytotoxicity (Li et al, 2019)
Summary
As producers of two-thirds of all known antibiotics and many other bioactive compounds, actinomycetes are a rich source of secondary metabolites. The majority of these compounds are produced by members of the genus Streptomyces (Berdy, 2005), which comprises Gram-positive, filamentous, spore-forming actinobacteria that are naturally found in soil and aquatic sediments. A dozen or so out of the hundreds of species described up to date, are known to be pathogenic to plants (Loria et al, 2006). The first described and best characterized pathogen species is S. scabies, while more recently emerged or restricted pathogens include S. acidiscabies, S. turgidiscabies, S. europaeiscabiei, S. luridiscabiei, S. puniciscabiei, S. niveiscabiei, S. reticuliscabiei, and S. bottropensis (Lambert and Loria, 1989a,b; Miyajima et al, 1998; Bouchek-Mechiche et al, 2000; Park et al, 2003a; Madhaiyan et al, 2020)
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