Paper · 2024 · Applied and Environmental Microbiology

Soybean-mediated suppression of BjaI/BjaR 1 quorum sensing in Bradyrhizobium diazoefficiens impacts symbiotic nitrogen fixation

Fang Han; Huiquan Li; Ermeng Lyu; et al.

10
claims
20
verbatim quotes
5
citations
2
research areas
✓
Open access

Abstract

ABSTRACT The acyl-homoserine lactones (AHLs)-mediated LuxI/LuxR quorum sensing (QS) system orchestrates diverse bacterial behaviors in response to changes in population density. The role of the BjaI/BjaR 1 QS system in Bradyrhizobium diazoefficiens USDA 110, which shares homology with LuxI/LuxR, remains elusive during symbiotic interaction with soybean. Here this genetic system in wild-type (WT) bacteria residing inside nodules exhibited significantly reduced activity compared to free-living cells, potentially attributed to soybean-mediated suppression. The deletion mutant strain ΔbjaR 1 showed significantly enhanced nodulation induction and nitrogen fixation ability. Nevertheless, its ultimate symbiotic outcome (plant dry weight) in soybeans was compromised. Furthermore, comparative analysis of the transcriptome, proteome, and promoter activity revealed that the inactivation of BjaR 1 systematically activated and inhibited genomic modules associated with nodulation and nitrogen metabolism. The former appeared to be linked to a significant decrease in the expression of NodD2, a key cell-density-dependent repressor of nodulation genes, while the latter conferred bacterial growth and nitrogen fixation insensitivity to environmental nitrogen. In addition, BjaR 1 exerted a positive influence on the transcription of multiple genes involved in a so-called central intermediate metabolism within the nodule. In conclusion, our findings highlight the crucial role of the BjaI/BjaR 1 QS circuit in positively regulating bacterial nitrogen metabolism and emphasize the significance of the soybean-mediated suppression of this genetic system for promoting efficient symbiotic nitrogen fixation by B. diazoefficiens . IMPORTANCE The present study demonstrates, for the first time, that the BjaI/BjaR1 QS system of Bradyrhizobium diazoefficiens has a significant impact on its nodulation and nitrogen fixation capability in soybean by positively regulating NodD2 expression and bacterial nitrogen metabolism. Moreover, it provides novel insights into the importance of suppressing the activity of this QS circuit by the soybean host plant in establishing an efficient mutual relationship between the two symbiotic partners. This research expands our understanding of legumes’ role in modulating symbiotic nitrogen fixation through rhizobial QS-mediated metabolic functioning, thereby deepening our comprehension of symbiotic coevolution theory. In addition, these findings may hold great promise for developing quorum quenching technology in agriculture.

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Claims 10

Observationobservedoriginal resultsignificant (as stated)measured

Claim · model-written summary

BjaI/BjaR1 system activity was lower in nodule bacteria than free-living cells.

Taxon
soybeanGlycine maxe0
Interactor
Bradyrhizobium diazoefficiensBradyrhizobium diazoefficienst0symbiont
Outcome
reduced activitye0
Direction
reducede0
Comparator
free-living cellse0

Not reportedGene

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

Glycine max
Glycine max · TaxonPublic domain · Wikimedia Commons ↗
Bradyrhizobium diazoefficiens
Bradyrhizobium diazoefficiens · InteractorNinjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Here this genetic system in wild-type (WT) bacteria residing inside nodules exhibited significantly reduced activity compared to free-living cells, potentially attributed to soybean-mediated suppression.”

✓ located verbatim in the source · abstract, characters 356–559 · show in text ↑
t0

“Bradyrhizobium diazoefficiens”

✓ located verbatim in the source · title, characters 62–91 · show in text ↑
Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

The ΔbjaR 1 strain enhanced nodulation induction.

Taxon
SoybeanGlycine maxt0
Material
ΔbjaR 1e0
Treatment
deletion mutant strain ΔbjaR 1e0
Interactor
Bradyrhizobium diazoefficiensBradyrhizobium diazoefficienst0symbiont
Outcome
nodulation inductione0
Direction
enhancede0

Not reportedComparator

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

Glycine max
Glycine max · TaxonPublic domain · Wikimedia Commons ↗
Bradyrhizobium diazoefficiens
Bradyrhizobium diazoefficiens · InteractorNinjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The deletion mutant strain ΔbjaR 1 showed significantly enhanced nodulation induction and nitrogen fixation ability.”

✓ located verbatim in the source · abstract, characters 560–676 · show in text ↑
t0

“Soybean-mediated suppression of BjaI/BjaR 1 quorum sensing in Bradyrhizobium diazoefficiens”

✓ located verbatim in the source · title, characters 0–91 · show in text ↑
Intervention effectobservedoriginal resultpositivesignificant (as stated)measured

Claim · model-written summary

The ΔbjaR 1 strain enhanced nitrogen fixation ability.

Taxon
SoybeanGlycine maxt0
Material
ΔbjaR 1e0
Treatment
deletion mutant strain ΔbjaR 1e0
Interactor
Bradyrhizobium diazoefficiensBradyrhizobium diazoefficienst0symbiont
Outcome
nitrogen fixation abilitye0
Direction
enhancede0

Not reportedComparator

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

Glycine max
Glycine max · TaxonPublic domain · Wikimedia Commons ↗
Bradyrhizobium diazoefficiens
Bradyrhizobium diazoefficiens · InteractorNinjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The deletion mutant strain ΔbjaR 1 showed significantly enhanced nodulation induction and nitrogen fixation ability.”

✓ located verbatim in the source · abstract, characters 560–676 · show in text ↑
t0

“Soybean-mediated suppression of BjaI/BjaR 1 quorum sensing in Bradyrhizobium diazoefficiens”

✓ located verbatim in the source · title, characters 0–91 · show in text ↑
Intervention effectobservedoriginal resultnegativemeasured

Claim · model-written summary

The ΔbjaR 1 strain compromised soybean plant dry weight.

Taxon
soybeansGlycine maxe0
Treatment
BjaI/BjaR 1t0
Interactor
Bradyrhizobium diazoefficiensBradyrhizobium diazoefficienst0symbiont
Outcome
plant dry weighte0
Direction
compromisede0

Not reportedComparator

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

Glycine max
Glycine max · TaxonPublic domain · Wikimedia Commons ↗
Bradyrhizobium diazoefficiens
Bradyrhizobium diazoefficiens · InteractorNinjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“Nevertheless, its ultimate symbiotic outcome (plant dry weight) in soybeans was compromised.”

✓ located verbatim in the source · abstract, characters 677–769 · show in text ↑
t0

“Soybean-mediated suppression of BjaI/BjaR 1 quorum sensing in Bradyrhizobium diazoefficiens”

✓ located verbatim in the source · title, characters 0–91 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

BjaR 1 inactivation activated genomic modules associated with nodulation.

Taxon
SoybeanGlycine maxt0
Treatment
inactivation of BjaR 1e0
Interactor
Bradyrhizobium diazoefficiensBradyrhizobium diazoefficienst0symbiont
Gene
BjaR 1e0
Outcome
genomic modules associated with nodulatione0
Direction
activatede0

Not reportedComparator

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

Glycine max
Glycine max · TaxonPublic domain · Wikimedia Commons ↗
Bradyrhizobium diazoefficiens
Bradyrhizobium diazoefficiens · InteractorNinjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“the inactivation of BjaR 1 systematically activated and inhibited genomic modules associated with nodulation and nitrogen metabolism.”

✓ located verbatim in the source · abstract, characters 872–1005 · show in text ↑
t0

“Soybean-mediated suppression of BjaI/BjaR 1 quorum sensing in Bradyrhizobium diazoefficiens”

✓ located verbatim in the source · title, characters 0–91 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

BjaR 1 inactivation inhibited genomic modules associated with nitrogen metabolism.

Taxon
SoybeanGlycine maxt0
Treatment
inactivation of BjaR 1e0
Interactor
Bradyrhizobium diazoefficiensBradyrhizobium diazoefficienst0symbiont
Gene
BjaR 1e0
Outcome
genomic modules associated with nodulation and nitrogen metabolisme0
Direction
inhibitede0

Not reportedComparator

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

Glycine max
Glycine max · TaxonPublic domain · Wikimedia Commons ↗
Bradyrhizobium diazoefficiens
Bradyrhizobium diazoefficiens · InteractorNinjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“the inactivation of BjaR 1 systematically activated and inhibited genomic modules associated with nodulation and nitrogen metabolism.”

✓ located verbatim in the source · abstract, characters 872–1005 · show in text ↑
t0

“Soybean-mediated suppression of BjaI/BjaR 1 quorum sensing in Bradyrhizobium diazoefficiens”

✓ located verbatim in the source · title, characters 0–91 · show in text ↑
Associationobservedoriginal resultsignificant (as stated)measured

Claim · model-written summary

Nodulation module activation appeared linked to reduced NodD2 expression.

Taxon
SoybeanGlycine maxt0
Interactor
Bradyrhizobium diazoefficiensBradyrhizobium diazoefficienst0symbiont
Gene
NodD2e0
Outcome
expression of NodD2e0
Direction
decreasee0
Qualifier
appeared to be linkede0

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

Glycine max
Glycine max · TaxonPublic domain · Wikimedia Commons ↗
Bradyrhizobium diazoefficiens
Bradyrhizobium diazoefficiens · InteractorNinjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The former appeared to be linked to a significant decrease in the expression of NodD2, a key cell-density-dependent repressor of nodulation genes”

✓ located verbatim in the source · abstract, characters 1006–1151 · show in text ↑
t0

“Soybean-mediated suppression of BjaI/BjaR 1 quorum sensing in Bradyrhizobium diazoefficiens”

✓ located verbatim in the source · title, characters 0–91 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The nitrogen metabolism change made bacterial growth insensitive to environmental nitrogen.

Taxon
SoybeanGlycine maxt0
Interactor
Bradyrhizobium diazoefficiensBradyrhizobium diazoefficienst0symbiont
Outcome
bacterial growthe0
Qualifier
insensitivity to environmental nitrogene0

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

Glycine max
Glycine max · TaxonPublic domain · Wikimedia Commons ↗
Bradyrhizobium diazoefficiens
Bradyrhizobium diazoefficiens · InteractorNinjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“the latter conferred bacterial growth and nitrogen fixation insensitivity to environmental nitrogen”

✓ located verbatim in the source · abstract, characters 1159–1258 · show in text ↑
t0

“Soybean-mediated suppression of BjaI/BjaR 1 quorum sensing in Bradyrhizobium diazoefficiens”

✓ located verbatim in the source · title, characters 0–91 · show in text ↑
Mechanismauthor interpretationoriginal resultmeasured

Claim · model-written summary

The nitrogen metabolism change made bacterial nitrogen fixation insensitive to environmental nitrogen.

Taxon
SoybeanGlycine maxt0
Interactor
Bradyrhizobium diazoefficiensBradyrhizobium diazoefficienst0symbiont
Outcome
nitrogen fixation insensitivity to environmental nitrogene0
Qualifier
environmental nitrogene0

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

Glycine max
Glycine max · TaxonPublic domain · Wikimedia Commons ↗
Bradyrhizobium diazoefficiens
Bradyrhizobium diazoefficiens · InteractorNinjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“the latter conferred bacterial growth and nitrogen fixation insensitivity to environmental nitrogen”

✓ located verbatim in the source · abstract, characters 1159–1258 · show in text ↑
t0

“Soybean-mediated suppression of BjaI/BjaR 1 quorum sensing in Bradyrhizobium diazoefficiens”

✓ located verbatim in the source · title, characters 0–91 · show in text ↑
Associationobservedoriginal resultpositivemeasured

Claim · model-written summary

BjaR 1 positively affected transcription of central intermediate metabolism genes in nodules.

Taxon
SoybeanGlycine maxt0
Organ / stage
nodulee0
Interactor
Bradyrhizobium diazoefficiensBradyrhizobium diazoefficienst0symbiont
Gene
BjaR 1e0
Outcome
transcription of multiple genes involved in a so-called central intermediate metabolisme0
Direction
positive influencee0

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

Glycine max
Glycine max · TaxonPublic domain · Wikimedia Commons ↗
Bradyrhizobium diazoefficiens
Bradyrhizobium diazoefficiens · InteractorNinjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“BjaR 1 exerted a positive influence on the transcription of multiple genes involved in a so-called central intermediate metabolism within the nodule”

✓ located verbatim in the source · abstract, characters 1273–1421 · show in text ↑
t0

“Soybean-mediated suppression of BjaI/BjaR 1 quorum sensing in Bradyrhizobium diazoefficiens”

✓ located verbatim in the source · title, characters 0–91 · show in text ↑