Plant Growth Stage Drives the Temporal and Spatial Dynamics of the Bacterial Microbiome in the Rhizosphere of Vigna subterranea

Abstract

Bambara groundnut (BGN) is an underutilized legume commonly found in sub-Saharan Africa. It thrives in marginal soils and is resistant to drought stress. Several studies have been carried out on the nutritional properties of BGN, but very little is known about the effects of plant growth changes and development on rhizosphere bacterial dynamics and function. This study reports on the bacterial dynamics and function in the bulk and rhizosphere soils of BGN at different growth stages (vegetative, flowering, pod-filling, and maturation stages). Aside from the maturation stage that shows distinct community structure from the other growth stages, results obtained showed no significant differences in bacterial community structure among the other growth stages. At a closer level, Actinobacteria, Proteobacteria, and Acidobacteria were dominant in rhizosphere soils at all growth stages. The bulk soil had the least average phyla abundance, while the maturity stage was characterized by the highest average phyla abundance. Rubrobacter, Acidobacterium, and Skermanella were the most predominant genus. It was observed from the analysis of operational taxonomic units that there was significant change in the bacterial structure of the rhizosphere with a higher abundance of potential plant growth-promoting rhizobacteria, at the different growth stages, which include the genera Bacillus and Acidobacterium. Biomarker analysis revealed 7 and 4 highly significant bacterial biomarkers by linear discriminant analysis effect size and random forest analysis at the maturation stage, respectively. The results obtained in this study demonstrated that the bacterial communities of BGN rhizosphere microbiome dynamics and function are influenced by the plant's growth stages.

Keywords: Bambara groundnut; PGPR biomarkers; functional microbiome; microbiome function; pattern analysis; plant microbe interaction; plant-growth dynamics; underutilized legume.

FIGURE 1

Rhizobacterial community assembly of Bambara groundnut plants during their growth cycle. (A) Taxonomic distribution of bacterial communities in the rhizosphere soils at different growth stages and in the bulk soil. (B) Alpha diversity of 16S rRNA rhizosphere bacterial sequences of Bambara groundnut in the rhizosphere soils at different growth stages. Shannon and Chao 1 diversity indices were calculated with Total Sum Scaling (TSS) normalized counts. (C) Principal Coordinate Analysis (PCoA) of 16S rRNA diversity in the rhizosphere of the Bambara groundnut growth stages and the bulk soil.

FIGURE 2

Heatmap of the core bacterial genera. x-axis, relative abundance; colors indicate the prevalence in the sample. (A) Rhizosphere soil, (B) bulk soil [0], (C) vegetative growth stage [4WAP], (D) flowering stage [8WAP], (E) pod-filling stage [12WAP], and (F) maturation stage [16WAP].

FIGURE 3

Bacterial biomarkers associated with bulk soil and plant growth stages. (A) LDA analysis indicating the differences in bacterial taxa among the growth stages (B) Random forest analysis indicating the differences in bacterial taxa among the growth stages. (C) Correlation pattern network analysis indicating the differences in bacterial taxa among the growth stages. Only predictors with significant effects are shown. Color from blue to red indicates from low to high level of significance.

FIGURE 4

(A) Heatmap of the bacterial biota in the bulk and rhizosphere soil at the different developmental stages at the class level. (B) Phylogenetic tree showing the relationship between the bulk soil and rhizosphere soil samples at the class level.