We provide here a comparative genome analysis of ten strains within the Pseudomonas fluorescens group including seven new genomic sequences. These strains exhibit a diverse spectrum of traits involved in biological control and other multitrophic interactions with plants, microbes, and insects. Multilocus sequence analysis placed the strains in three sub-clades, which was reinforced by high levels of synteny, size of core genomes, and relatedness of orthologous genes between strains within a sub-clade. The heterogeneity of the P. fluorescens group was reflected in the large size of its pan-genome, which makes up approximately 54% of the pan-genome of the genus as a whole, and a core genome representing only 45–52% of the genome of any individual strain. We discovered genes for traits that were not known previously in the strains, including genes for the biosynthesis of the siderophores achromobactin and pseudomonine and the antibiotic 2-hexyl-5-propyl-alkylresorcinol; novel bacteriocins; type II, III, and VI secretion systems; and insect toxins. Certain gene clusters, such as those for two type III secretion systems, are present only in specific sub-clades, suggesting vertical inheritance. Almost all of the genes associated with multitrophic interactions map to genomic regions present in only a subset of the strains or unique to a specific strain. To explore the evolutionary origin of these genes, we mapped their distributions relative to the locations of mobile genetic elements and repetitive extragenic palindromic (REP) elements in each genome. The mobile genetic elements and many strain-specific genes fall into regions devoid of REP elements (i.e., REP deserts) and regions displaying atypical tri-nucleotide composition, possibly indicating relatively recent acquisition of these loci. Collectively, the results of this study highlight the enormous heterogeneity of the P. fluorescens group and the importance of the variable genome in tailoring individual strains to their specific lifestyles and functional repertoire.
The GacS/GacA signal transduction system is a central regulator in Pseudomonas spp., including the biological control strain P. fluorescens Pf-5, in which GacS/GacA controls the production of secondary metabolites and exoenzymes that suppress plant pathogens. A whole genome oligonucleotide microarray was developed for Pf-5 and used to assess the global transcriptomic consequences of a gacA mutation in P. fluorescens Pf-5. In cultures at the transition from exponential to stationary growth phase, GacA significantly influenced transcript levels of 635 genes, representing more than 10% of the 6147 annotated genes in the Pf-5 genome. Transcripts of genes involved in the production of hydrogen cyanide, the antibiotic pyoluteorin and the extracellular protease AprA were at a low level in the gacA mutant, whereas those functioning in siderophore production and other aspects of iron homeostasis were significantly higher in the gacA mutant than in wild-type Pf-5. Notable effects of gacA inactivation were also observed in the transcription of genes encoding components of a type VI secretion system and cytochrome c oxidase subunits. Two novel gene clusters expressed under the control of gacA were identified from transcriptome analysis, and we propose global-regulator-based genome mining as an approach to decipher the secondary metabolome of Pseudomonas spp.
Typically pathogens deploy virulence effectors to disable defense. Plants defeat effectors with resistance proteins that guard effector targets. Here we show that a pathogen exploits a resistance protein by activating it to confer susceptibility. Interactions of victorin, an effector produced by the necrotrophic fungus Cochliobolus victoriae, TRX-h5, a defense-associated thioredoxin, and LOV1, an Arabidopsis susceptibility protein, recapitulate the guard mechanism of plant defense. In LOV1’s absence, victorin inhibits TRX-h5 resulting in compromised defense but not disease by C. victoriae. In LOV1’s presence, victorin binding to TRX-h5 activates LOV1 and elicits a resistance-like response that confers disease susceptibility. We propose victorin is or mimics a conventional pathogen virulence effector that was defeated by LOV1 and confers virulence to C. victoriae solely because it incites defense.
The antibiotics pyoluteorin and 2,4-diacetylphloroglucinol (DAPG) contribute to the biological control of soilborne plant diseases by some strains of Pseudomonas fluorescens, including Pf-5. These secondary metabolites also have signalling functions with each compound reported to induce its own production and repress the other's production. The first step in DAPG biosynthesis is production of phloroglucinol (PG) by PhlD. In this study, we show that PG is required at nanomolar concentrations for pyoluteorin production in Pf-5. At higher concentrations, PG is responsible for the inhibition of pyoluteorin production previously attributed to DAPG. DAPG had no effect on pyoluteorin production, and monoacetylphloroglucinol showed both stimulatory and inhibitory activities but at concentrations 100-fold greater than the levels of PG required for similar effects. We also demonstrate that PG regulates pyoluteorin production in P. aeruginosa and that a phlD gene adjacent to the pyoluteorin biosynthetic gene cluster in P. aeruginosa strain LESB58 can restore pyoluteorin biosynthesis to a ΔphlD mutant of Pf-5. Bioinformatic analyses show that the dual role of PhlD in the biosynthesis of DAPG and the regulation of pyoluteorin production could have arisen within the pseudomonads during the assembly of these biosynthetic gene clusters from genes and gene subclusters of diverse origins.
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