A mutualistic interaction between Streptomyces bacteria, strawberry plants and pollinating bees

Kim, Da-Ran; Cho, Gyeongjun; Jeon, Chang-Wook; Weller, David M.; Thomashow, Linda S.; Paulitz, Timothy C.; Kwak, Youn‐Sig

doi:10.1038/s41467-019-12785-3

Cited by 115 publications

(98 citation statements)

References 42 publications

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“…Streptomyces species are effective at colonizing the rhizosphere and endosphere of plant roots where they can promote plant growth and provide protection against disease (11)(12)(13)34,35). It has even been suggested that their diverse specialized metabolism and filamentous growth may have evolved to give them a competitive advantage in this niche since it occurred ~50 million years after plants first colonized land (3).…”

Section: Discussion Although Typically Described As Free-living Soilmentioning

confidence: 99%

Investigating the role of root exudates in recruitingStreptomycesbacteria to theArabidopsis thalianaroot microbiome

Worsley¹,

Macey²,

Prudence³

et al. 2020

Preprint

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Streptomyces species are saprophytic soil bacteria that produce a diverse array of specialised 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 colonised more readily by streptomycetes but found that salicylate-deficient sid2-2 and pad4 plants had the same levels of root colonisation 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.ImportanceStreptomyces bacteria are ubiquitous in soil but their role as rhizobacteria is less well studied. Our recent work demonstrated that streptomycetes isolated from A. thaliana roots can promote growth and protect against disease across plant species and that plant growth hormones can modulate the production of bioactive specialised metabolites by these strains. Here we used 13CO2 DNA stable isotope probing to identify which bacteria feed on plant metabolites in the A. thaliana rhizosphere and, for the first time, in the endosphere. We found that Streptomyces species are outcompeted for these metabolites by faster growing proteobacteria and instead likely subsist on more complex organic material such as cellulose derived from plant cell material that is shed from the roots. This work thus reveals the “winners and losers” in the battle between soil bacteria for plant metabolites and could inform the development of methods to apply streptomycetes as plant growth-promoting agents.

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Section: Discussion Although Typically Described As Free-living Soilmentioning

confidence: 99%

Investigating the role of root exudates in recruitingStreptomycesbacteria to theArabidopsis thalianaroot microbiome

Worsley¹,

Macey²,

Prudence³

et al. 2020

Preprint

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“…In addition to Lactobacillus, the core bacterial community of Source K included Bifidobacterium, which is speculated to be involved with pollen digestion in honey bees [22]. One library within Source K included a high abundance of Streptomyces, which has been previously detected in pollen stores of honey bees [76] and stingless bees [96], and is known to defend against pathogens including Paenibacillus larvae and Melisococcus plutonius that cause American foulbrood and European foulbrood disease, respectively [97,98]. The bacterial community of Source B was significantly more diverse compared to Source K, and contained higher abundances of Betaproteobacteria, Gammaproteobacteria, and Bacteroides within the Flavobacteriaceae and Sphingobacteriaceae family, which have been previously detected in beebread [43,88].…”

Section: Bacterial Communitymentioning

confidence: 99%

Microbial Diversity Associated with the Pollen Stores of Captive-Bred Bumble Bee Colonies

Dharampal

Diaz‐Garcia

Haase

et al. 2020

Insects

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The pollen stores of bumble bees host diverse microbiota that influence overall colony fitness. Yet, the taxonomic identity of these symbiotic microbes is relatively unknown. In this descriptive study, we characterized the microbial community of pollen provisions within captive-bred bumble bee hives obtained from two commercial suppliers located in North America. Findings from 16S rRNA and ITS gene-based analyses revealed that pollen provisions from the captive-bred hives shared several microbial taxa that have been previously detected among wild populations. While diverse microbes across phyla Firmicutes, Proteobacteria, Bacteroidetes, Actinobacteria, and Ascomycota were detected in all commercial hives, significant differences were detected at finer-scale taxonomic resolution based on the supplier source. The causative agent of chalkbrood disease in honey bees, Ascosphaera apis, was detected in all hives obtained from one supplier source, although none of the hives showed symptoms of infection. The shared core microbiota across both commercial supplier sources consisted of two ubiquitous bee-associated groups, Lactobacillus and Wickerhamiella/Starmerella clade yeasts that potentially contribute to the beneficial function of the microbiome of bumble bee pollen provisions.

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“…The microbial community in strawberry owers shifts throughout the growing season from one of high diversity (weeks 0-12) to one of low diversity (weeks 14-24), a pattern coincident with the loss of S. globisporus SP6C4, which we consider to be a core member of the ower microbial community [6]. Here, we recalculated strawberry ower microbial population data to identify the top 10 OTUs and the diversity of the microbial community throughout the growing season ( Fig.…”

Section: Microbiome Collapse and Diseasementioning

confidence: 99%

“…We previously observed collapse of the anthosphere microbial community structure coincident with the aging of strawberry plants [6]. In particular, the loss of diversity and reduction in population density of Streptomyces globisporus SP6C4, a core microbe, was negatively correlated with onset of two major anthosphere diseases, gray mold (Botrytis cinerea) which includes brown spots on ower petals, and blossom blight (Cladosporioides sp.…”

Section: Introductionmentioning

confidence: 97%

“…The plant microbiome includes associated microorganisms residing above and below ground, and inside or outside of plant tissues [1]. Plants in nature interact endlessly with diverse microbial species including mutualists that in uence plant health and reproduction by providing phytohormones, xing nitrogen, solubilizing phosphorus, facilitating mineral uptake, and protecting against pathogen attack [2][3][4][5][6][7][8][9][10][11][12].…”

Section: Introductionmentioning

confidence: 99%

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Glutamic Acid Reshapes The Phytobiome To Protect Plants Against Pathogens

Kim¹,

Jeon²,

Cho³

et al. 2020

Preprint

Self Cite

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Background: The physiology and growth of plants are strongly influenced by their associated microbiomes. Conversely, the composition of the phytobiome is flexible, responding to the state of the host and raising the possibility that it can be engineered to benefit the plant. However, technology for engineering the structure of the microbiome is not yet available.Results: Here we show that glutamic acid reshapes the plant microbial community and enriches populations of Streptomyces, a functional core microbe, both above and below ground, in strawberry and tomato. Upon application of glutamic acid, the population size of Streptomyces increased dramatically in the anthosphere and the rhizosphere. At the same time, diseases caused by species of Fusarium were significantly reduced in both habitats. Plant resistance-related genes were not activated, suggesting that glutamic acid modulates the microbiome community directly, rather than activating the host’s own protective mechanisms.Conclusions: Much is known about the structure of plant-associated microbial communities, but little has been learned about how the community composition and complexity are controlled. Our results demonstrate that the microbiome community can be engineered and unlock the mode of action of glutamic acid.

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A mutualistic interaction between Streptomyces bacteria, strawberry plants and pollinating bees

Cited by 115 publications

References 42 publications

Investigating the role of root exudates in recruitingStreptomycesbacteria to theArabidopsis thalianaroot microbiome

Investigating the role of root exudates in recruitingStreptomycesbacteria to theArabidopsis thalianaroot microbiome

Microbial Diversity Associated with the Pollen Stores of Captive-Bred Bumble Bee Colonies

Glutamic Acid Reshapes The Phytobiome To Protect Plants Against Pathogens

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