Pan-genome analysis identifies intersecting roles for Pseudomonas specialized metabolites in potato pathogen inhibition
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Curated by eLife
Evaluation Summary:
This work uses large-scale genome sequencing and analysis, mass spectrometry and bioassays to investigate the genomic diversity of Pseudomonas strains and their potential role in plant protection. The authors identified a novel group of cyclic lipopeptides that could inhibit Streptomyces scabies, the causal agent of potato scab, and showed how genomic diversity in closely related bacterial strains can contribute to plant pathogen suppression in the field.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Abstract
Agricultural soil harbors a diverse microbiome that can form beneficial relationships with plants, including the inhibition of plant pathogens. Pseudomonas spp. are one of the most abundant bacterial genera in the soil and rhizosphere and play important roles in promoting plant health. However, the genetic determinants of this beneficial activity are only partially understood. Here, we genetically and phenotypically characterize the Pseudomonas fluorescens population in a commercial potato field, where we identify strong correlations between specialized metabolite biosynthesis and antagonism of the potato pathogens Streptomyces scabies and Phytophthora infestans . Genetic and chemical analyses identified hydrogen cyanide and cyclic lipopeptides as key specialized metabolites associated with S. scabies inhibition, which was supported by in planta biocontrol experiments. We show that a single potato field contains a hugely diverse and dynamic population of Pseudomonas bacteria, whose capacity to produce specialized metabolites is shaped both by plant colonization and defined environmental inputs.
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Author Response:
Public Review:
This manuscript from Pacheco-Moreno et al. compares the microbiome of potato fields with and without irrigation. Irrigation is known to control potato scab caused by Streptomyces scabies and the authors hypothesized that changes in the microbiome may contribute to disease suppression after irrigation. Using 16S rRNA sequencing, they identified a number of taxa, including Pseudomonas that are enriched after irrigation. They went on to isolate and sequence the genomes of many Pseudomonas strains. By correlating the ability of Pseudomonas to suppress Streptomyces growth in vitro with genomic data, the authors identified a novel group of cyclic lipopeptides (CLPs) that can inhibit Streptomyces in vitro and in planta.
This work provides a substantial contribution that advances our understanding of disease …
Author Response:
Public Review:
This manuscript from Pacheco-Moreno et al. compares the microbiome of potato fields with and without irrigation. Irrigation is known to control potato scab caused by Streptomyces scabies and the authors hypothesized that changes in the microbiome may contribute to disease suppression after irrigation. Using 16S rRNA sequencing, they identified a number of taxa, including Pseudomonas that are enriched after irrigation. They went on to isolate and sequence the genomes of many Pseudomonas strains. By correlating the ability of Pseudomonas to suppress Streptomyces growth in vitro with genomic data, the authors identified a novel group of cyclic lipopeptides (CLPs) that can inhibit Streptomyces in vitro and in planta.
This work provides a substantial contribution that advances our understanding of disease suppressive soil mechanisms. It is novel in scope in that it focuses on suppression of a bacterial pathogen, while many prior studies focus on suppression of fungal pathogens. Additionally, the large-scaled comparative genomics is a useful resource, and the identification of CLPs that inhibit Streptomyces is novel. Importantly, the authors provide in planta data to show role a for CLPs in disease suppression in vivo. The manuscript is well written and the data are well presented. The analyses are quite thorough and I appreciate the extensive use of genetics and metabolomics to support the genomic predictions. The main weakness is a lack of data the conclusively links the change in microbiome function to disease suppression after irrigation in the field. However, I think the data they've presented, combined with those in the drought literature, might suggest that an increase in total Pseudomonas (and the corresponding disease-suppressive genes) in well-watered soil might contribute to suppression, rather than a change in function of Pseudomonas.
While the reviewer is correct that we cannot conclusively link disease suppression to a change in microbiome function after irrigation, we are confident that our results demonstrate a real and repeatable phenomenon that must be considered in future studies of soil scab suppression. Independent field experiments conducted two years apart both show a decrease in the proportion of suppressive pseudomonads associated with potato roots. The first experiment (Figures 1 & 2) contained too few sequenced isolates to draw statistically robust conclusions, therefore we designed the second experiment (Figure 8) to investigate this phenomenon further. This experiment showed highly significant differences in the proportion of suppressive isolates on irrigated and non-irrigated roots. The alternative hypothesis presented by the reviewer; that relative Pseudomonas and Streptomyces abundance are affected by irrigation and this may be a factor in scab suppression, is also a valid possibility, although relatively small abundance changes were observed in the data reported in Figure 1. We have amended the discussion to include this as an alternative explanation for our results.
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Evaluation Summary:
This work uses large-scale genome sequencing and analysis, mass spectrometry and bioassays to investigate the genomic diversity of Pseudomonas strains and their potential role in plant protection. The authors identified a novel group of cyclic lipopeptides that could inhibit Streptomyces scabies, the causal agent of potato scab, and showed how genomic diversity in closely related bacterial strains can contribute to plant pathogen suppression in the field.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Public Review:
This manuscript from Pacheco-Moreno et al. compares the microbiome of potato fields with and without irrigation. Irrigation is known to control potato scab caused by Streptomyces scabies and the authors hypothesized that changes in the microbiome may contribute to disease suppression after irrigation. Using 16S rRNA sequencing, they identified a number of taxa, including Pseudomonas that are enriched after irrigation. They went on to isolate and sequence the genomes of many Pseudomonas strains. By correlating the ability of Pseudomonas to suppress Streptomyces growth in vitro with genomic data, the authors identified a novel group of cyclic lipopeptides (CLPs) that can inhibit Streptomyces in vitro and in planta.
This work provides a substantial contribution that advances our understanding of disease suppressive soil …
Public Review:
This manuscript from Pacheco-Moreno et al. compares the microbiome of potato fields with and without irrigation. Irrigation is known to control potato scab caused by Streptomyces scabies and the authors hypothesized that changes in the microbiome may contribute to disease suppression after irrigation. Using 16S rRNA sequencing, they identified a number of taxa, including Pseudomonas that are enriched after irrigation. They went on to isolate and sequence the genomes of many Pseudomonas strains. By correlating the ability of Pseudomonas to suppress Streptomyces growth in vitro with genomic data, the authors identified a novel group of cyclic lipopeptides (CLPs) that can inhibit Streptomyces in vitro and in planta.
This work provides a substantial contribution that advances our understanding of disease suppressive soil mechanisms. It is novel in scope in that it focuses on suppression of a bacterial pathogen, while many prior studies focus on suppression of fungal pathogens. Additionally, the large-scaled comparative genomics is a useful resource, and the identification of CLPs that inhibit Streptomyces is novel. Importantly, the authors provide in planta data to show role a for CLPs in disease suppression in vivo. The manuscript is well written and the data are well presented. The analyses are quite thorough and I appreciate the extensive use of genetics and metabolomics to support the genomic predictions. The main weakness is a lack of data the conclusively links the change in microbiome function to disease suppression after irrigation in the field. However, I think the data they've presented, combined with those in the drought literature, might suggest that an increase in total Pseudomonas (and the corresponding disease-suppressive genes) in well-watered soil might contribute to suppression, rather than a change in function of Pseudomonas.
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