Distinct Patterns of Rhizosphere Microbiota Associated With Rice Genotypes Differing in Aluminum Tolerance in an Acid Sulfate Soil

Abstract

Rhizosphere microbes are important for plant tolerance to various soil stresses. Rice is the most aluminum (Al)-tolerant small grain cereal crop species, but the link between rice Al tolerance and rhizosphere microbiota remains unclear. This study aimed to investigate the microbial community structure of aluminum-sensitive and Al-tolerant rice varieties in acid sulfate soil under liming and non-liming conditions. We analyzed the rice biomass and mineral element contents of rice plants as well as the chemical properties and microbial (archaea, bacteria, and fungi) communities of rhizosphere and bulk soil samples. The results showed that the Al-tolerant rice genotype grew better and was able to take up more phosphorus from the acid sulfate soil than the Al-sensitive genotype. Liming was the main factor altering the microbial diversity and community structure, followed by rhizosphere effects. In the absence of liming effects, the rice genotypes shifted the community structure of bacteria and fungi, which accounted for the observed variation in the rice biomass. The Al-tolerant rice genotype recruited specific bacterial and fungal taxa (Bacillus, Pseudomonas, Aspergillus, and Rhizopus) associated with phosphorus solubilization and plant growth promotion. The soil microbial co-occurrence network of the Al-tolerant rice genotype was more complex than that of the Al-sensitive rice genotype. In conclusion, the bacterial and fungal community in the rhizosphere has genotype-dependent effects on rice Al tolerance. Aluminum-tolerant rice genotypes recruit specific microbial taxa, especially phosphorus-solubilizing microorganisms, and are associated with complex microbial co-occurrence networks, which may enhance rice growth in acid sulfate soil.

Keywords: acid sulfate soil; aluminum toxicity; co-occurrence network; microbial community structure; rice genotypes.

FIGURE 1

Rice shoot and root biomasses. Different lowercase letters within the bottom, middle, and top parts of columns indicate significant differences in root, shoot, and total biomasses among treatments, respectively (P < 0.05). Al-S, Al-sensitive rice; Al-T, Al-tolerant rice; Al-S + Ca, Al-sensitive rice and CaCO₃; Al-T + Ca, Al-tolerant rice and CaCO₃.

FIGURE 2

α-diversity of archaea (A,D), bacteria (B,E), and fungi (C,F) according to the Shannon and richness indices. Different lowercase and uppercase letters above boxplots indicate significant differences among treatments for the bulk soil and rhizosphere soil (P < 0.05), respectively. Al-S, Al-sensitive rice; Al-T, Al-tolerant rice; Al-S + Ca, Al-sensitive rice and CaCO₃; Al-T + Ca, Al-tolerant rice and CaCO₃.

FIGURE 3

Hierarchical cluster analysis and relative abundance of the dominant archaea (A), bacteria (B), and fungi (C) in the bulk and rhizosphere soils under liming and non-liming conditions. Al_S_B, Al-sensitive rice bulk soil; Al_S_R, Al-sensitive rice rhizosphere soil; Al_T_B, Al-tolerant rice bulk soil; Al_T_R, Al-tolerant rice rhizosphere soil; Al_S_Ca_B, Al-sensitive rice and CaCO₃ bulk soil; Al_S_Ca_R, Al-sensitive rice and CaCO₃ rhizosphere soil; Al_T_Ca_B, Al-tolerant rice and CaCO₃ bulk soil; Al_T_Ca_R, Al-tolerant rice and CaCO₃ rhizosphere soil.

FIGURE 4

β-diversity of archaea (A,D), bacteria (B,E), and fungi (C,F) according to the Bray–Curtis dissimilarity matrix in soil samples under liming (+ Ca) and non-liming (−Ca) conditions.

FIGURE 5

Special sets of bacteria (A–C) and fungi (D–F) enriched and depleted in the rhizosphere of the Al-tolerant rice genotype under liming (+ Ca) and non-liming (−Ca) conditions. The MA plots present the average abundance (in log count per million, CPM) and the log-fold change of all ASVs plotted on the x-axis and y-axis, respectively. Differentially enriched and depleted ASVs were determined on the basis of an edgeR analysis (FDR < 0.05, | log₂ fold change| ≥ 2). Green and red, respectively, indicate enriched and depleted bacterial and fungal OTUs. The number of enriched bacterial (C) and fungal (F) ASVs in the Al-tolerant rice genotype is compared between the liming (+ Ca) and non-liming (−Ca) conditions.

FIGURE 6

Predicted factors, soil properties (A), plant mineral elements (B), and rhizosphere microbial properties (C), contributing to the total rice biomass following a random forest regression analysis. R², coefficient of determination; % Var explained, the proportion of variance explained. The microbial diversity and community used in this model were determined according to the Shannon index and the first two axes (#1 and #2) of the non-metric multidimensional scaling analysis, respectively. * Indicates factors with significant effects (P < 0.05).

FIGURE 7

Co-occurrence networks of archaeal, bacterial, and fungal communities for Al-sensitive (A,C) and Al-tolerant (B,D) rice genotypes in acid sulfate soils under liming and non-liming conditions. The size of each node is proportional to the number of connections. The archaeal, bacterial, and fungal ASVs are indicated in orange, purple, and green, respectively.