Paper · 2025 · Microbiome

Interactions with native microbial keystone taxa enhance the biocontrol efficiency of Streptomyces

Tianyu Sun; Hongwei Liu; Ningqi Wang; et al.

7
claims
14
verbatim quotes
33
citations
1
research areas
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Open access · cc-by-nc-nd

Abstract

BACKGROUND: Streptomyces spp. are known for producing bioactive compounds that suppress phytopathogens. However, previous studies have largely focused on their direct interactions with pathogens and plants, often neglecting their interactions with the broader soil microbiome. In this study, we hypothesized that these interactions are critical for effective pathogen control. We investigated a diverse collection of Streptomyces strains to select those with strong protective capabilities against tomato wilt disease caused by Ralstonia solanacearum. Leveraging a synthetic community (SynCom) established in our lab, alongside multiple in planta and in vitro co-cultivation experiments, as well as transcriptomic and metabolomic analyses, we explored the synergistic inhibitory mechanisms underlying bacterial wilt resistance facilitated by both Streptomyces and the soil microbiome. RESULTS: Our findings indicate that direct antagonism by Streptomyces is not sufficient for their biocontrol efficacy. Instead, the efficacy was associated with shifts in the rhizosphere microbiome, particularly the promotion of two native keystone taxa, CSC98 (Stenotrophomonas maltophilia) and CSC13 (Paenibacillus cellulositrophicus). In vitro co-cultivation experiments revealed that CSC98 and CSC13 did not directly inhibit the pathogen. Instead, the metabolite of CSC13 significantly enhanced the inhibition efficiency of Streptomyces R02, a highly effective biocontrol strain in natural soil. Transcriptomic and metabolomic analyses revealed that CSC13's metabolites induced the production of Erythromycin E in Streptomyces R02, a key compound that directly suppressed R. solanacearum, as demonstrated by our antagonism tests. CONCLUSIONS: Collectively, our study reveals how beneficial microbes engage with the native soil microbiome to combat pathogens, suggesting the potential of leveraging microbial interactions to enhance biocontrol efficiency. These findings highlight the significance of intricate microbial interactions within the microbiome in regulating plant diseases and provide a theoretical foundation for devising efficacious biocontrol strategies in sustainable agriculture. Video Abstract.

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Claims 7

Observationobservedoriginal resultnegativemeasured

Claim · model-written summary

Direct antagonism by Streptomyces alone was insufficient for biocontrol efficacy against tomato wilt.

Interactor
StreptomycesStreptomycese0biocontrol_agent
Outcome
biocontrol efficacye0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Streptomyces
Streptomyces · Interactor · picture of the genus (one of its species)Public domain · Wikimedia Commons ↗

Verbatim

e0

“direct antagonism by Streptomyces is not sufficient for their biocontrol efficacy”

✓ located verbatim in the source · abstract, characters 921–1002 · show in text ↑
t0

“tomato wilt disease caused by Ralstonia solanacearum”

✓ located verbatim in the source · abstract, characters 498–550 · show in text ↑
Associationobservedoriginal resultpositivemeasured

Claim · model-written summary

Biocontrol efficacy was associated with rhizosphere shifts promoting CSC98 and CSC13.

Interactor
Stenotrophomonas maltophiliaStenotrophomonas maltophiliae0biocontrol_agent
Second interactor
Paenibacillus cellulositrophicusPaenibacillus cellulositrophicuse0biocontrol_agent
Outcome
efficacye0

Not reportedDirection

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Stenotrophomonas maltophilia
Stenotrophomonas maltophilia · InteractorRiraq25 · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“the efficacy was associated with shifts in the rhizosphere microbiome, particularly the promotion of two native keystone taxa, CSC98 (Stenotrophomonas maltophilia) and CSC13 (Paenibacillus cellulositrophicus)”

✓ located verbatim in the source · abstract, characters 1013–1221 · show in text ↑
t0

“tomato wilt disease caused by Ralstonia solanacearum”

✓ located verbatim in the source · abstract, characters 498–550 · show in text ↑
Observationobservedoriginal resultno effectmeasured

Claim · model-written summary

CSC98 did not directly inhibit the tomato wilt pathogen in vitro.

Interactor
CSC98e0biocontrol_agent
Outcome
CSC98 and CSC13 did not directly inhibit the pathogene0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“CSC98 and CSC13 did not directly inhibit the pathogen”

✓ located verbatim in the source · abstract, characters 1273–1326 · show in text ↑
t0

“tomato wilt disease caused by Ralstonia solanacearum”

✓ located verbatim in the source · abstract, characters 498–550 · show in text ↑
Observationobservedoriginal resultno effectmeasured

Claim · model-written summary

CSC13 did not directly inhibit the tomato wilt pathogen in vitro.

Interactor
CSC13e0biocontrol_agent
Outcome
CSC13 did not directly inhibit the pathogene0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“CSC98 and CSC13 did not directly inhibit the pathogen”

✓ located verbatim in the source · abstract, characters 1273–1326 · show in text ↑
t0

“tomato wilt disease caused by Ralstonia solanacearum”

✓ located verbatim in the source · abstract, characters 498–550 · show in text ↑
Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

CSC13 metabolite significantly enhanced the pathogen inhibition efficiency of Streptomyces R02.

Treatment
the metabolite of CSC13e0
Interactor
Streptomyces R02e0biocontrol_agent
Second interactor
CSC13e0biocontrol_agent
Outcome
inhibition efficiency of Streptomyces R02e0
Direction
enhancede0

Not reportedComparator

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“the metabolite of CSC13 significantly enhanced the inhibition efficiency of Streptomyces R02”

✓ located verbatim in the source · abstract, characters 1337–1429 · show in text ↑
t0

“tomato wilt disease caused by Ralstonia solanacearum”

✓ located verbatim in the source · abstract, characters 498–550 · show in text ↑
Mechanismobservedoriginal resultpositivemeasured

Claim · model-written summary

CSC13 metabolites induced Erythromycin E production in Streptomyces R02.

Interactor
Streptomyces R02e0biocontrol_agent
Outcome
production of Erythromycin E in Streptomyces R02e0
Qualifier
CSC13's metabolitese0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗

Verbatim

e0

“CSC13's metabolites induced the production of Erythromycin E in Streptomyces R02”

✓ located verbatim in the source · abstract, characters 1539–1619 · show in text ↑
t0

“tomato wilt disease caused by Ralstonia solanacearum”

✓ located verbatim in the source · abstract, characters 498–550 · show in text ↑
Mechanismobservedoriginal resultpositivemeasured

Claim · model-written summary

Erythromycin E produced by Streptomyces R02 directly suppressed R. solanacearum.

Interactor
R. solanacearumRalstonia solanacearume0pathogen
Second interactor
Streptomyces R02e0biocontrol_agent
Compound
Erythromycin Ee0
Outcome
suppressed R. solanacearume0

Organisms pictured · Representative pictures of the matched species, not figures from the paper.

Solanum lycopersicum
Solanum lycopersicum · TaxonKod B · CC BY-SA 4.0 · Wikimedia Commons ↗
Ralstonia solanacearum
Ralstonia solanacearum · InteractorClemson University - USDA Cooperative Extension Slide Series, Bugwood.org · Public domain · Wikimedia Commons ↗

Verbatim

e0

“Erythromycin E in Streptomyces R02, a key compound that directly suppressed R. solanacearum”

✓ located verbatim in the source · abstract, characters 1585–1676 · show in text ↑
t0

“tomato wilt disease caused by Ralstonia solanacearum”

✓ located verbatim in the source · abstract, characters 498–550 · show in text ↑

metabolite · disease · Solanum lycopersicum (tomato)Results agree

5 papers: 5 positive, 0 negative or no effect

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Claims are grouped by organism, treatment and what was measured or targeted. A paper counts as positive when any of its claims in the group is positive.