Abstract
Pectobacterium versatile (formerly P. carotovorum) is a recently defined species of soft rot enterobacteria capable of infecting many plant hosts and damaging different tissues. Complex transcriptional regulation of virulence properties can be expected for such a versatile pathogen. However, the relevant information is available only for related species and is rather limited. The PhoPQ two-component system, originally described in pectobacteria as PehRS, was previously shown to regulate a single gene, pehA. Using an insertional phoP mutant of Pectobacterium versatile (earlier—P. carotovorum), we demonstrate that PhoP regulates at least 115 genes with a majority of them specific for pectobacteria. The functions performed by PhoP-controlled genes include degradation, transport and metabolism of plant-derived carbon sources (polygalacturonate, arabinose-containing polysaccharides and citrate), modification of bacterial cell envelope and stress resistance. We also demonstrated PhoP involvement in establishing the order of plant cell wall decomposition and utilisation of the corresponding breakdown products. Based on experimental data and in silico analysis, we defined a PhoP binding site motif and provided proof for its universality in enteric bacteria. Scanning P. versatile genome for the locations of this motif suggested a much larger PhoP regulon enriched with the genes important for a plant pathogen, which makes PhoP a global virulence regulator. Potential PhoP targets include many regulatory genes and PhoP control over one of them, expI, was confirmed experimentally, highlighting the link between the PhoPQ two-component and quorum sensing systems. High concentrations of calcium and magnesium ions were found to abolish the PhoPQ-dependent transcription activation but did not relieve repression. Reduced PhoP expression and minimisation of PhoP dependence of regulon members’ expression in P. versatile cells isolated from potato tuber tissues suggest that PhoPQ system is a key switch of expression levels of multiple virulence-related genes fine-tuned to control the development of P. versatile-host plant pathosystem.
Highlights
Pectobacterium spp. are pectinolytic bacteria that cause soft rot and other diseases in a variety of plants
Since phoP is the first gene of the phoPQ operon and a polar effect of phoP inactivation on the expression of phoQ was expected, complementation was achieved by a plasmid carrying the whole phoPQ operon together with the full regulatory region
In Chinese cabbage virulence tests carried out at low inoculum doses (103 cells), the mutant strain caused less damage than the wild type strain, and observed virulence defect was fully complemented by the plasmid expressing phoPQ (Figures 1A,B)
Summary
Pectobacterium spp. are pectinolytic bacteria that cause soft rot and other diseases in a variety of plants. Members of this genus were often considered to be broad host range pathogens. Genomic studies revealed significant diversity within this group, resulting in the ongoing subdivision of the previously described species and elevation of subspecies to species level. That resulted in better separation of the related strains according to their environmental preferences. Candidatus Pectobacterium maceratum was suggested as a new name for a group of strains isolated from potato and cabbage (Shirshikov et al, 2018). More isolates from various sources, including Chrysanthemum, Iris and water, were united with Ca. P. maceratum strains and renamed as Pectobacterium versatile (Portier et al, 2019). The P. versatile taxon includes two strains that have been well characterised previously, Ecc and SCC1. The 3-2 strain used in this work belongs to this species
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