Ralstonia solanacearum Infection Drives the Assembly and Functional Adaptation of Potato Rhizosphere Microbial Communities

Abstract

Bacterial wilt caused by Ralstonia solanacearum is a destructive disease that affects potato production, leading to severe yield losses. Currently, little is known about the changes in the assembly and functional adaptation of potato rhizosphere microbial communities during different stages of R. solanacearum infection. In this study, using amplicon and metagenomic sequencing approaches, we analyzed the changes in the composition and functions of bacterial and fungal communities in the potato rhizosphere across four stages of R. solanacearum infection. The results showed that R. solanacearum infection led to significant changes in the composition and functions of bacterial and fungal communities in the potato rhizosphere, with various microbial properties (including α,β-diversity, species composition, and community ecological functions) all being driven by R. solanacearum infection. The relative abundance of some beneficial microorganisms in the potato rhizosphere, including Firmicutes, Bacillus, Pseudomonas, and Mortierella, decreased as the duration of infection increased. Moreover, the related microbial communities played a significant role in basic metabolism and signal transduction; however, the functions involved in soil C, N, and P transformation weakened. This study provides new insights into the dynamic changes in the composition and functions of potato rhizosphere microbial communities at different stages of R. solanacearum infection to adapt to the growth promotion or disease suppression strategies of host plants, which may provide guidance for formulating future strategies to regulate microbial communities for the integrated control of soil-borne plant diseases.

Keywords: functional adaptability; potato; rhizosphere microbial communities.

Fig. 1

Symptoms of potato plants infected by Ralstonia solanacearum. The four infection stages: 1 day post-infection (1d), 3 days post-infection (3d), 7 days post-infection (7d), and 15 days post-infection (15d). The 1-day period following inoculation with the bacterial wilt pathogen is a pivotal time for the interaction between the pathogen and the plant, as well as for the colonization of the pathogen within the plant. On the 3rd day after infection, the stem of the potato plants at the inoculation site exhibits a water-soaked appearance, and there is sap exuding near the inoculation point. On the 7th day after infection, the potato plants exhibit symptoms of lodging, with the internal tissues near the inoculation point of the stems showing signs of rotting. By the 15th day post-infection, the entire plant displays symptoms of lodging, and the stem and leaf tissues begin to decompose and rot.

Fig. 2

The rhizosphere microbial community structure of potatoes at different infection stages of Ralstonia solanacearum. (A, B) The number of unique, shared, and common bacterial (A) and fungal (B) operational taxonomic units at different groups. (C, D) Principal coordinate analysis (PCoA) plots based on the Bray-Curtis dissimilarity matrices with permutational analysis of variance (PERMANOVA), showing the changes in the structure of the bacterial (A) and fungal (B) community composition. OTU, operational taxonomic unit.

Fig. 3

Shannon and Chao1 diversity indices of the rhizosphere bacterial (A, B) and fungal (C, D) communities of potatoes at different infection stages of Ralstonia solanacearum. *P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001.

Fig. 4

Composition of bacterial and fungal communities in the rhizosphere of potatoes at the phylum and genus levels during different infection stages of Ralstonia solanacearum. (A, B) The bar plots of relative abundance illustrate the composition of bacterial (A) and fungal (B) communities at the phylum level under the different groups. (C, D) The Circos plots depicting sample-to-species relationships illustrate the dominant bacterial (C) and fungal (D) communities at the genus level for various treatment groups. Low abundance phyla/genera with less than 1% of the total sequences across all samples are grouped into “Other.”

Fig. 5

Functional profiles of microbiomes in the rhizosphere of potatoes at different infection stages of Ralstonia solanacearum. (A) Nonmetric multidimensional scaling (NMDS) ordinations of functional genes based on Bray-Curtis distance matrices of CAZy functional genes show the distinct functions of microbial communities in the rhizosphere of potatoes at different infection stages of R. solanacearum. (B) The boxplot shows the functional diversity (including Kyoto Encyclopedia of Genes and Genomes Orthology [KO], cluster of orthologous groups of proteins [COG], and CAZy) of the rhizosphere microbiomes of potatoes across four infection stages. (C, D) Differential abundance analysis of CAZy (C) and COG (D) functional genes of the rhizosphere microbiomes of potatoes across four infection stages. *P < 0.05.

Fig. 6

Heatmap exhibiting the relative abundance of functional genes (based on Kyoto Encyclopedia of Genes and Genomes Orthology [KO]) involved in C, N, and P metabolisms which varied among four infection stages. Here: each row of the heatmap corresponds to a specific gene, while each column represents a different sample. The colors in the heatmap, with red representing higher levels of the gene abundance in that sample, and blue representing lower levels, indicate the variation in gene abundance.