Paper · 2024 · Microbiology Spectrum

Integrative analysis of microbiome and metabolome revealed the effect of microbial inoculant on microbial community diversity and function in rhizospheric soil under tobacco monoculture

Xianjun Lai; Wangjun Duan; Wenyou Zhang; et al.

11
claims
12
verbatim quotes
14
citations
3
research areas
✓
Open access · cc-by

Abstract

ABSTRACT Over-application of chemical fertilizers and continuous cropping obstacles seriously restrict the sustainable development of tobacco production. Localized fertilization of beneficial microbes has potential advantages in achieving higher productivity, but the underlying biological mechanisms of interactions between rhizospheric microorganisms and the related metabolic cycle remain poorly characterized. Here, an integrative analysis of microbiomes with non-targeted metabolomics was performed on 30 soil samples of rhizosphere, root surrounding, and bulk soils from flue‐cured tobacco under continuous and non-continuous monocropping systems. The analysis was conducted using UPLC-MS/MS platforms and high-throughput amplicon sequencing targeting the bacterial 16S rRNA gene and fungal ITS gene. The microbial inoculant consisted of Bacillus subtilis , B. velezensis, and B. licheniformis at the ratio of 1:1:1 in effective microbial counts, improved the cured leaf yield and disease resistance of tobacco, and enhanced nicotine and nitrogen contents of tobacco leaves. The bacterial taxa Rhizobium , Pseudomonas , Sphingomonadaceae , and Burkholderiaceae of the phylum Proteobacteria accumulated in high relative abundance and were identified as biomarkers following the application of the microbial inoculant. Under continuous monocropping, metabolomics demonstrated that the application of the microbial inoculant significantly affected the soil metabolite spectrum, and the differential metabolites were significantly enriched to the synthesis and degradation of nicotine (nicotinate and nicotinamide metabolism and biosynthesis of alkaloids derived from nicotinic acid). In addition, microbes were closely related to the accumulation of metabolites through correlation analysis. The interactions between plant roots and rhizospheric microorganisms provide valuable information for understanding how these beneficial microbes affect complex biological processes and the adaption capacity of plants to environments. IMPORTANCE This study elaborated on how the microbial fertilizer significantly changed overall community structures and metabolite spectrum of rhizospheric microbes, which provide insights into the process of rhizosphere microbial remolding in response to continuous monocropping. we verified the hypothesis that the application of the microbial inoculant in continuous cropping would lead to the selection of distinct microbiota communities by establishing models to correlate biomarkers. Through correlation analysis of the microbiome and metabolome, we proved that rhizospheric microbes were closely related to the accumulation of metabolites, including the synthesis and degradation of nicotine. The interactions between plant roots and rhizospheric microorganisms provide valuable information for understanding how these beneficial microbes affect complex biological processes and the adaption capacity of plants to environments.

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Claims 11

Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

The microbial inoculant improved tobacco cured leaf yield.

Treatment
microbial inoculante0
Interactor
Bacillus subtilisBacillus subtilise0symbiont
Outcome
cured leaf yielde0
Direction
improvede0
Qualifier
B. velezensis, and B. licheniformise0

Not reportedComparator

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

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗
Bacillus subtilis
Bacillus subtilis · InteractorY tambe (original uploader) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The microbial inoculant consisted of Bacillus subtilis , B. velezensis, and B. licheniformis at the ratio of 1:1:1 in effective microbial counts, improved the cured leaf yield and disease resistance of tobacco”

✓ located verbatim in the source · abstract, characters 807–1016 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

The inoculant improved tobacco disease resistance.

Treatment
microbial inoculante0
Interactor
Bacillus subtilisBacillus subtilise0symbiont
Outcome
disease resistancee0
Direction
improvede0

Not reportedComparator

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

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗
Bacillus subtilis
Bacillus subtilis · InteractorY tambe (original uploader) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The microbial inoculant consisted of Bacillus subtilis , B. velezensis, and B. licheniformis at the ratio of 1:1:1 in effective microbial counts, improved the cured leaf yield and disease resistance of tobacco”

✓ located verbatim in the source · abstract, characters 807–1016 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

The inoculant enhanced tobacco leaf nicotine content.

Organ / stage
leavese0
Treatment
microbial inoculante0
Interactor
Bacillus subtilisBacillus subtilise0symbiont
Outcome
nicotinee0
Direction
enhancede0

Not reportedComparator

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

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗
Bacillus subtilis
Bacillus subtilis · InteractorY tambe (original uploader) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The microbial inoculant consisted of Bacillus subtilis , B. velezensis, and B. licheniformis at the ratio of 1:1:1 in effective microbial counts, improved the cured leaf yield and disease resistance of tobacco, and enhanced nicotine and nitrogen contents of tobacco leaves.”

✓ located verbatim in the source · abstract, characters 807–1080 · show in text ↑
Intervention effectobservedoriginal resultpositivemeasured

Claim · model-written summary

The inoculant enhanced tobacco leaf nitrogen content.

Organ / stage
leavese0
Treatment
microbial inoculante0
Interactor
Bacillus subtilisBacillus subtilise0symbiont
Outcome
nitrogen contentse0
Direction
enhancede0

Not reportedComparator

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

Nicotiana tabacum
Nicotiana tabacum · TaxonJom / Joachim Müllerchen · CC BY 2.5 · Wikimedia Commons ↗
Bacillus subtilis
Bacillus subtilis · InteractorY tambe (original uploader) · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The microbial inoculant consisted of Bacillus subtilis , B. velezensis, and B. licheniformis at the ratio of 1:1:1 in effective microbial counts, improved the cured leaf yield and disease resistance of tobacco, and enhanced nicotine and nitrogen contents of tobacco leaves.”

✓ located verbatim in the source · abstract, characters 807–1080 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Rhizobium accumulated at high relative abundance after inoculant application.

Taxon
RhizobiumRhizobiume0
Treatment
microbial inoculante0
Outcome
relative abundancee0
Direction
accumulatede0
Setting
tobacco monoculturet0

Not reportedComparator

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

Rhizobium
Rhizobium · Taxon · picture of the genus (one of its species)Ninjatacoshell · CC BY-SA 3.0 · Wikimedia Commons ↗

Verbatim

e0

“The bacterial taxa Rhizobium , Pseudomonas , Sphingomonadaceae , and Burkholderiaceae of the phylum Proteobacteria accumulated in high relative abundance and were identified as biomarkers following the application of the microbial inoculant.”

✓ located verbatim in the source · abstract, characters 1081–1322 · show in text ↑
t0

“tobacco monoculture”

✓ located verbatim in the source · title, characters 166–185 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Pseudomonas accumulated at high relative abundance after inoculant application.

Taxon
PseudomonasPseudomonase0
Treatment
microbial inoculante0
Outcome
relative abundancee0
Direction
accumulatede0

Not reportedComparator

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

Pseudomonas
Pseudomonas · Taxon · picture of the genus (one of its species)CDC · Public domain · Wikimedia Commons ↗

Verbatim

e0

“The bacterial taxa Rhizobium , Pseudomonas , Sphingomonadaceae , and Burkholderiaceae of the phylum Proteobacteria accumulated in high relative abundance and were identified as biomarkers following the application of the microbial inoculant.”

✓ located verbatim in the source · abstract, characters 1081–1322 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Sphingomonadaceae accumulated at high relative abundance after inoculant application.

Taxon
SphingomonadaceaeSphingomonadaceaee0
Treatment
microbial inoculante0
Outcome
relative abundancee0
Direction
accumulatede0

Not reportedComparator

Verbatim

e0

“The bacterial taxa Rhizobium , Pseudomonas , Sphingomonadaceae , and Burkholderiaceae of the phylum Proteobacteria accumulated in high relative abundance and were identified as biomarkers following the application of the microbial inoculant.”

✓ located verbatim in the source · abstract, characters 1081–1322 · show in text ↑
Intervention effectobservedoriginal resultmeasured

Claim · model-written summary

Burkholderiaceae accumulated at high relative abundance after inoculant application.

Taxon
BurkholderiaceaeBurkholderiaceaee0
Treatment
microbial inoculante0
Outcome
relative abundancee0
Direction
accumulatede0

Not reportedComparator

Verbatim

e0

“The bacterial taxa Rhizobium , Pseudomonas , Sphingomonadaceae , and Burkholderiaceae of the phylum Proteobacteria accumulated in high relative abundance and were identified as biomarkers following the application of the microbial inoculant.”

✓ located verbatim in the source · abstract, characters 1081–1322 · show in text ↑
Intervention effectobservedoriginal resultsignificant (as stated)measured

Claim · model-written summary

Inoculant application significantly affected the soil metabolite spectrum under continuous monocropping.

Treatment
microbial inoculante0
Outcome
soil metabolite spectrume0
Qualifier
continuous monocroppinge0

Not reportedTaxonComparatorDirection

Verbatim

e0

“Under continuous monocropping, metabolomics demonstrated that the application of the microbial inoculant significantly affected the soil metabolite spectrum”

✓ located verbatim in the source · abstract, characters 1323–1479 · show in text ↑
Observationobservedoriginal resultsignificant (as stated)measured

Claim · model-written summary

Differential soil metabolites were enriched in nicotine synthesis and degradation pathways.

Outcome
differential metabolitese0
Direction
enrichede0
Qualifier
synthesis and degradation of nicotinee0

Not reportedTaxon

Verbatim

e0

“the differential metabolites were significantly enriched to the synthesis and degradation of nicotine (nicotinate and nicotinamide metabolism and biosynthesis of alkaloids derived from nicotinic acid)”

✓ located verbatim in the source · abstract, characters 1485–1685 · show in text ↑
Associationobservedoriginal resultmeasured

Claim · model-written summary

Microbes were closely correlated with metabolite accumulation.

Taxon
microbese0
Interactor
microbese0symbiont
Outcome
accumulation of metabolitese0
Qualifier
closely relatede0

Not reportedDirection

Verbatim

e0

“microbes were closely related to the accumulation of metabolites through correlation analysis.”

✓ located verbatim in the source · abstract, characters 1700–1794 · show in text ↑