The virulome ofStreptomyces scabieiin response to cello-oligosaccharides elicitors
Authors: Deflandre Benoit , Stulanovic Nudzejma , Planckaert Sören , Anderssen Sinaeda , Bonometti Beatrice , Karim Latifa , Coppieters Wouter , Devreese Bart , Rigali Sébastien 
Published: August 2021

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The development of spots or lesions symptomatic of the common scab disease on root and tuber crops is caused by few pathogenicStreptomyceswithStreptomyces scabiei87-22 as the model species. Thaxtomin phytotoxins are the primary virulence determinants, mainly acting by impairing cellulose synthesis, and their production inS.scabieiis in turn boosted by the cello-oligosaccharides released from host plants. In this work we aimed to determine which molecules and which biosynthetic gene clusters (BGCs) of the specialized metabolism ofS. scabiei87-22 show a production and/or transcriptional response to cello-oligosaccharides. Comparative metabolomic and transcriptomic analyses revealed that molecules of the virulome ofS. scabieiinduced by cellobiose and cellotriose include i) thaxtomins and concanamycins phytotoxins (and to a lesser extent N-coronafacoyl-L-isoleucine), ii) desferrioxamines, scabichelin and turgichelin siderophores in order to acquire iron essential for housekeeping functions, iii) ectoine for protection against osmotic shock once inside the host, and iv) bottromycins and concanamycins antimicrobials possibly to prevent other microorganisms from colonizing the same niche. Importantly, both cell-oligosaccharides reduced the production of the spore germination inhibitors germicidins and the plant growth regulators rotihibins. The metabolomic study also revealed that cellotriose is in general a more potent elicitor of the virulome compared to cellobiose. This result supports an earlier hypothesis that suggested that the trisaccharide would be the real virulence-triggering factor released from the plant cell wall through the action of thaxtomins. Interestingly, except for thaxtomins, none of these BGCs’ expression seems to be under direct control of the cellulose utilization repressor CebR suggesting the existence of another master regulator sensing the internalization of cello-oligosaccharides. Finally, we found nine additional cryptic and orphan BGCs that have their expression awakened by cello-oligosaccharides, demonstrating that other and yet to be discovered metabolites are part of the virulome ofS.scabiei.

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Impact statement

Unveiling the environmental triggers that signal proper conditions for host colonization and what is the composition of the arsenal of metabolites specialized for this task (the virulome) is key to understand host-pathogen interactions. In this work, focused on the induction of the common scab disease caused byStreptomycesspecies, we provided further knowledge to both aspects i.e., i) highlighting the capability of cellotriose to trigger the entire virulome and not only the production of thaxtomin phytotoxins, and ii) identifying the set of metabolites that specifically respond to cello-oligosaccharides emanating from the plant under attack. Importantly, we also revealed that the expression of nine cryptic/orphan biosynthetic gene clusters (BGCs) involved in the production of unknown compounds was drastically activated upon cello-oligosaccharides import suggesting that a significant part of the virulome ofS.scabieiremains to be discovered. Finally, we unexpectedly found that the expression control of most of the known and cryptic BGCs does not depend on the cello-oligosaccharide utilization repressor CebR which suggests the existence of another and yet unknown master regulator of the virulence inS.scabiei.

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Significance as a BioResource to the community

Not Applicable

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Outcome

Not Applicable

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Data summary

[A section describing all supporting external data including the DOI(s) and/or accession numbers(s), and the associated URL.]

The authors confirm all supporting data, code and protocols have been provided within the article or through supplementary data files. RNAseq data were publicly deposited, and our experimental and analytical pipeline were described on the GEO database repository (Accession number: GSE181490)