Abstract
Streptomyces species are saprophytic soil bacteria that produce a diverse array of specialized metabolites, including half of all known antibiotics. They are also rhizobacteria and plant endophytes that can promote plant growth and protect against disease. Several studies have shown that streptomycetes are enriched in the rhizosphere and endosphere of the model plant Arabidopsis thaliana. Here, we set out to test the hypothesis that they are attracted to plant roots by root exudates, and specifically by the plant phytohormone salicylate, which they might use as a nutrient source. We confirmed a previously published report that salicylate over-producing cpr5 plants are colonized more readily by streptomycetes but found that salicylate-deficient sid2-2 and pad4 plants had the same levels of root colonization by Streptomyces bacteria as the wild-type plants. We then tested eight genome sequenced Streptomyces endophyte strains in vitro and found that none were attracted to or could grow on salicylate as a sole carbon source. We next used 13CO2 DNA stable isotope probing to test whether Streptomyces species can feed off a wider range of plant metabolites but found that Streptomyces bacteria were outcompeted by faster growing proteobacteria and did not incorporate photosynthetically fixed carbon into their DNA. We conclude that, given their saprotrophic nature and under conditions of high competition, streptomycetes most likely feed on more complex organic material shed by growing plant roots. Understanding the factors that impact the competitiveness of strains in the plant root microbiome could have consequences for the effective application of biocontrol strains.
Highlights
Streptomyces species are saprophytic soil bacteria that play an important ecological role as composters in soil and are prolific producers of antimicrobial compounds (van der Meij et al, 2017; Hutchings et al, 2019)
A previous study reported that A. thaliana cpr5 plants that constitutively produce salicylate have an altered root microbiota compared to wild-type plants, and that certain streptomycetes were better able to colonize these plants in vitro, due to their ability to metabolize salicylate (Lebeis et al, 2015)
This method has been used previously to assess colonization efficiency by other streptomycete strains in the plant root microbiome (Bonaldi et al, 2015; Chen et al, 2016). The results of these assays show that root colonization was significantly affected by plant genotype (Figure 1), irrespective of the Streptomyces strain used as an inoculum; plant genotype had a significant effect on the log-transformed cfu g−1 (F(3,39) 6.17, p < 0.01), whereas the strain-genotype interaction term was insignificant (F(3,39) 0.51, p 0.68) in an ANOVA test
Summary
Streptomyces species are saprophytic soil bacteria that play an important ecological role as composters in soil and are prolific producers of antimicrobial compounds (van der Meij et al, 2017; Hutchings et al, 2019). It is thought that the plant host might establish a beneficial root microbiome by producing particular types of root exudates that attract microbial species with desirable metabolic traits (Bais et al, 2006; Badri and Vivanco, 2009). The abundance of bacteria in the A. thaliana rhizosphere and roots has been shown to correlate with concentrations of the defence phytohormone salicylic acid (Lebeis et al, 2015) Plant growth hormones such as indole-3-acetic acid have been shown to modulate the production of Streptomyces specialized metabolites which may aid their competitive establishment in the root microbiome (Worsley et al, 2020)
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