Abstract
Streptomyces scabies is an economically important plant pathogen well-known for damaging root and tuber crops by causing scab lesions. Thaxtomin A is the main causative agent responsible for the pathogenicity of S. scabies and cello-oligosaccharides are environmental triggers that induce the production of this phytotoxin. How cello-oligosaccharides are sensed or transported in order to induce the virulent behavior of S. scabies? Here we report that the cellobiose and cellotriose binding protein CebE, and MsiK, the ATPase providing energy for carbohydrates transport, are the protagonists of the cello-oligosaccharide mediated induction of thaxtomin production in S. scabies. Our work provides the first example where the transport and not the sensing of major constituents of the plant host is the central mechanism associated with virulence of the pathogen. Our results allow to draw a complete pathway from signal transport to phytotoxin production where each step of the cascade is controlled by CebR, the cellulose utilization regulator. We propose the high affinity of CebE to cellotriose as possible adaptation of S. scabies to colonize expanding plant tissue. Our work further highlights how genes associated with primary metabolism in nonpathogenic Streptomyces species have been recruited as basic elements of virulence in plant pathogenic species.
Highlights
The bacterial genus Streptomyces mostly consists of soil saprophytes able to produce a large arsenal of biologically active metabolites[1] and catabolic enzymes making them well adapted to life in challenging soil environments[2,3]
At least five global regulators belonging to the bld gene family directing secondary metabolism and/or morphological differentiation of Streptomyces are involved in the regulation of toxin production[10] in addition to the pathway-specific transcriptional activator, 1Centre for Protein Engineering, Integrative Biological Sciences (InBioS) Research Unit, University of Liège, Institut de Chimie B6a, B-4000, Liège, Belgium. 2Department of Biology, California State University Bakersfield, Bakersfield, CA 93311-1022, USA. 3Department of Plant Pathology, University of Florida, Gainesville, FL 32611-0180, USA. 4Laboratory for Protein Biochemistry and Biomolecular Engineering, Department of Biochemistry and Microbiology, Ghent University, B-9000, Ghent, Belgium. *These authors contributed to this work. †These authors jointly supervised this work
After having described how cellobiose and cellotriose unlock production of thaxtomin A12, we investigated and describe in this study how S. scabies links extracellular plant material sensing to the onset of its virulent behavior
Summary
The bacterial genus Streptomyces mostly consists of soil saprophytes able to produce a large arsenal of biologically active metabolites[1] and catabolic enzymes making them well adapted to life in challenging soil environments[2,3]. A selected group of Streptomyces species including Streptomyces scabies, Streptomyces acidiscabies, Streptomyces turgidiscabies and Streptomyces ipomoeae causes raised or pitted scab lesions on economically-important root and tuber crops like potato, radish, beet, peanut, and sweet potato[7] These pathogenic species produce a family of non-ribosomally produced cyclic 2,5-diketopiperazines called thaxtomins. CebR has been shown to bind upstream as well as within the thaxtomin biosynthetic cluster, and specific interaction between CebR and cellobiose or cellotriose was shown to trigger the release of the repressor from its binding sites hereby allowing transcription of the thaxtomin biosynthetic (txtA and txtB) and regulatory (txtR) genes[12]. After having described how cellobiose and cellotriose unlock production of thaxtomin A12, we investigated and describe in this study how S. scabies links extracellular plant material sensing to the onset of its virulent behavior
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