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. 2024 Jul 1:15:1383526.
doi: 10.3389/fmicb.2024.1383526. eCollection 2024.

Differential effects of domesticated and wild Capsicum frutescens L. on microbial community assembly and metabolic functions in rhizosphere soil

Can Wang  1   2 , Yinghua Zhang  1 , Shaoxiang Wang  2 , Xia Lv  1 , Junqiang Xu  1 , Xueting Zhang  2 , Qing Yang  1 , Fanlai Meng  3 , Bin Xu  1
Affiliations

Differential effects of domesticated and wild Capsicum frutescens L. on microbial community assembly and metabolic functions in rhizosphere soil

Can Wang et al. Front Microbiol. .

Abstract

Objective: Rhizosphere microorganisms play crucial roles in the growth and development of plants, disease resistance, and environmental adaptability. As the only wild pepper variety resource in China, domesticated Capsicum frutescens Linn. (Xiaomila) exhibits varying beneficial traits and affects rhizosphere microbial composition compared with its wild counterparts. In this study, we aimed to identify specific rhizosphere microbiome and metabolism patterns established during the domestication process.

Methods: The rhizosphere microbial diversity and composition of domesticated and wild C. frutescens were detected and analyzed by metagenomics. Non-targeted metabolomics were used to explore the differences of metabolites in rhizosphere soil between wild and domesticated C. frutescens.

Results: We found that the rhizosphere microbial diversity of domesticated variety was significantly different from that of the wild variety, with Massilia being its dominant bacteria. However, the abundance of certain beneficial microbes such as Gemmatimonas, Streptomyces, Rambibacter, and Lysobacter decreased significantly. The main metabolites identified in the wild variety included serylthreonine, deoxyloganic acid, vitamin C, among others. In contrast, those identified in the domesticated group were 4-hydroxy-l-glutamic acid and benzoic acid. Furthermore, the differentially enriched pathways were concentrated in tyrosine and tryptophan biosynthesis, histidine and purine-derived alkaloids biosynthesis, benzoic acid family, two-component system, etc.

Conclusion: This study revealed that C. frutescens established specific rhizosphere microbiota and metabolites during domestication, which has important significance for the efficient utilization of beneficial microorganisms in breeding and cultivation practices.

Keywords: Capsicum frutescens L.; Massilia; metabolome; metagenome; rhizosphere soil.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Map of the soil sampling site and overall composition of rhizosphere microorganisms in the wild variety (WV) and domesticated variety (DV) C. frutescens. (A) Map of the soil sampling site in Yanshan City, Yunnan Province, China. (B) Relative abundance of soil microorganisms at the kingdom level. (C) Relative abundance of soil microorganisms of the top 10 phyla.
Figure 2
Figure 2
Alpha diversity of rhizosphere microorganisms in WV and DV C. frutescens. Shannon (A), Simpson (B), ACE (C), and Chao (D) indices in the WV and DV. The level of significance between WV and DV is indicated as ** (p < 0.01) based on Student’s t-test.
Figure 3
Figure 3
Differences in rhizosphere soil microorganisms caused by domestication. (A) Principal co-ordinates analysis (PCoA) showed the differences in soil microorganisms of WV and DV. (B) Differential analysis showing abundance disparities between DV and WV C. frutescens. (C) 15 differential taxa between DV and WV C. frutescens identified by Wilcoxon rank-sum test.
Figure 4
Figure 4
Co-occurrence network of genes in DV and WV C. frutescens. Red circles represent bacteria and green circles represent fungi. Red lines represent positive correlation and green lines represent negative correlation.
Figure 5
Figure 5
Gene functions of rhizosphere microorganisms in DV and WV C. frutescens. (A) Significant enriched pathways are screened based on Wilcox non-parametric test. (B) Differential enrichment of resistance genes between DV and WV.
Figure 6
Figure 6
Composition and distribution of metabolites in DV and WV soils. (A) Overall metabolite distribution in the DV and WV groups. (B) PCA plots of the GC-TOFMS metabolites. (C) Two hundred randomly arranged substitution tests were performed between DV and WV in the OPLS-DA model. (D) Volcano diagram of differential metabolites between the two groups.
Figure 7
Figure 7
Metabolite profiling of DV and WV. The color blocks in different positions represent the relative accumulation of metabolites in corresponding positions. Red indicates a high accumulation of metabolites and blue indicates a low accumulation of metabolites.
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