Abstract
BackgroundInteractions between pathogenic oomycetes and microbiota residing on the surface of the host plant root are unknown, despite being critical to inoculum constitution. The nature of these interactions was explored for the polyphagous and telluric species Phytophthora parasitica.ResultsComposition of the rhizospheric microbiota of Solanum lycopersicum was characterized using deep re-sequencing of 16S rRNA gene to analyze tomato roots either free of or partly covered with P. parasitica biofilm. Colonization of the host root surface by the oomycete was associated with a shift in microbial community involving a Bacteroidetes/Proteobacteria transition and Flavobacteriaceae as the most abundant family. Identification of members of the P. parasitica-associated microbiota interfering with biology and oomycete infection was carried out by screening for bacteria able to (i) grow on a P. parasitica extract-based medium (ii), exhibit in vitro probiotic or antibiotic activity towards the oomycete (iii), have an impact on the oomycete infection cycle in a tripartite interaction S. lycopersicum-P. parasitica-bacteria. One Pseudomonas phylotype was found to exacerbate disease symptoms in tomato plants. The lack of significant gene expression response of P. parasitica effectors to Pseudomonas suggested that the increase in plant susceptibility was not associated with an increase in virulence. Our results reveal that Pseudomonas spp. establishes commensal interactions with the oomycete. Bacteria preferentially colonize the surface of the biofilm rather than the roots, so that they can infect plant cells without any apparent infection of P. parasitica.ConclusionsThe presence of the pathogenic oomycete P. parasitica in the tomato rhizosphere leads to a shift in the rhizospheric microbiota composition. It contributes to the habitat extension of Pseudomonas species mediated through a physical association between the oomycete and the bacteria.
Highlights
Interactions between pathogenic oomycetes and microbiota residing on the surface of the host plant root are unknown, despite being critical to inoculum constitution
Roots were inoculated for 3 h with 10 ml of P. parasitica zoospore suspension, were washed three times with sterile water, and were inoculated with bacterial isolates suspended in sterile water (OD = 0.2)
Our results suggest that the presence of oomycete on root surfaces led to an enrichment of sequences assigned belonging to Bacteroidetes (33% ± 10.8, 45% ± 5.2 for M1 and M2, respectively), and a reduction in the proportion of sequences assigned to the phylum Proteobacteria (63% ± 10.1, 52% ±3.9 for M1 and M2, respectively)
Summary
Interactions between pathogenic oomycetes and microbiota residing on the surface of the host plant root are unknown, despite being critical to inoculum constitution. Plant pathogens of the genera Phytophthora and Pythium, together with some obligate parasites (downy mildews and white rusts) cause highly destructive diseases on many dicots, thereby having major ecological and economic consequences worldwide [16]. They have evolved the ability to suppress PAMP-triggered immunity (PTI), a key aspect of plant innate immunity which contributes to microbial growth inhibition [17, 18]. Phytophthora parasitica has been shown to exploit intraspecific zoospore communication to improve adhesion to host cells and to express a set of effector and mucin-like genes by means of biofilm formation [28, 29]
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