Pseudomonas syringae naturally lacking the canonical type III secretion system are ubiquitous in nonagricultural habitats, are phylogenetically diverse and can be pathogenic - PubMed
Pseudomonas syringae naturally lacking the canonical type III secretion system are ubiquitous in nonagricultural habitats, are phylogenetically diverse and can be pathogenic
Moudjahidou Demba Diallo et al. ISME J. 2012 Jul.
Abstract
The type III secretion system (T3SS) is an important virulence factor of pathogenic bacteria, but the natural occurrence of variants of bacterial plant pathogens with deficiencies in their T3SS raises questions about the significance of the T3SS for fitness. Previous work on T3SS-deficient plant pathogenic bacteria has focused on strains from plants or plant debris. Here we have characterized T3SS-deficient strains of Pseudomonas syringae from plant and nonplant substrates in pristine nonagricultural contexts, many of which represent recently described clades not yet found associated with crop plants. Strains incapable of inducing a hypersensitive reaction (HR(-)) in tobacco were detected in 65% of 126 samples from headwaters of rivers (mountain creeks and lakes), snowpack, epilithic biofilms, wild plants and leaf litter and constituted 2 to 100% of the P. syringae population associated with each sample. All HR(-) strains lacked at least one gene in the canonical hrp/hrc locus or the associated conserved effector locus, but most lacked all six of the genes tested (hrcC, hrpL, hrpK1, avrE1 and hrpW1) and represented several disparate phylogenetic clades. Although most HR(-) strains were incapable of causing symptoms on cantaloupe seedlings as expected, strains in the recently described TA-002 clade caused severe symptoms in spite of the absence of any of the six conserved genes of the canonical T3SS according to PCR and Southern blot assays. The phylogenetic context of the T3SS variants we observed provides insight into the evolutionary history of P. syringae as a pathogen and as an environmental saprophyte.
Figures

Fraction of HR− strains in the total P. syringae populations in environmental samples in terms of the density of the P. syringae population in the sample. Population densities are expressed as log c.f.u. g−1 for biofilms, plant and leaf litter or log c.f.u. l−1 for water, rain and snow (as snowmelt). The data constitute values from 100 of the 126 samples described in Table 1. For these 100 samples, they were processed to permit quantification of the density of the HR− component population as well as that of the total P. syringae population.

Population dynamics of P. syringae (a) and disease (b) in cantaloupe seedlings after inoculation with either HR+ or HR− strains. HR+ strains are represented by solid lines and symbols (♦ CC0654; ▴ DC3000; ▪ USA-032) and HR− strains by dashed lines and open symbols (⋄ TA-043; ▵ SZ-030; □ CC1504). At each sampling time, 3–6 seedlings were cut off at the soil level and individually macerated to determine population densities. Disease was rated on each of the 3–6 plants sampled. Plants inoculated with strains SZ-030 and CC1504 did not show any disease symptoms. Only one plant inoculated with strain DC3000 showed disease symptoms at 2 days after inoculation. For strain TA-043, half of the inoculated plants showed symptoms at 7 days after inoculation. Error bars indicate the s.e.m.

Reaction of cantaloupe plants at the cotyledon stage to inoculation with HR+ and HR− strains of P. syringae after 7 days of incubation: plants were inoculated with (a) sterile distilled water, (b) HR− strain CC1524 in the clade of the same name (c) HR+ strain CC0094 in the Group 2b clade, or (d) HR− strain TA043 in the TA002 clade. Plants shown here were chosen at random among the 12 plants inoculated for each strain.
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References
-
- Clarke CR, Cai R, Studholme DJ, Guttman DS, Vinatzer BA. Pseudomonas syringae strains naturally lacking the classical P. syringae hrp/hrc locus are common leaf colonizers equipped with an atypical type III secretion system. Mol Plant Microb Interact. 2010;23:198–210. - PubMed
-
- Cornelis GR, Van Gijsegem F. Assembly and function of type III secretory systems. Annu Rev Microbiol. 2000;54:735–774. - PubMed
-
- Downie JA. The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev. 2010;34:150–170. - PubMed