Soil pH Filters the Association Patterns of Aluminum-Tolerant Microorganisms in Rice Paddies

Abstract

Soil microbes are considered the second genome of plants. Understanding the distribution and network of aluminum (Al)-tolerant microorganisms is helpful to alleviate Al toxicity to plants in acidic soils. Here, we examined soluble Al³⁺ and bacterial communities carrying Al resistance genes in paddy soils with a soil pH range of 3.6 to 8.7. In the acidic soil with pH <5.1, the content of Al³⁺ increased significantly. There were abundant and diverse Al-tolerant microorganisms in acidic soils, including Clostridium, Bacillus, Paenibacillus, Desulfitobacterium, and Desulfosporosinus, etc. Moreover, compared with neutral and alkaline soils, the network structure of Al-tolerant microorganisms was more complex. The potential roles of major Al-tolerant microbial taxa on each other in the ecological network were identified by a directed network along 0.01 pH steps. The influential taxa in the network had a broader niche and contained more antioxidant functional genes to resist Al stress, indicating their survival advantage over the sensitive taxa. Our study is the first to explore the distribution of Al-tolerant microorganisms in continental paddies and reveal their potential associations mediated by pH, which provides a basis for further utilization of microbial resources in acidic agricultural soils. IMPORTANCE Aluminum (Al) toxicity is the primary limiting factor of crop production in acidic soils with pH <5.0. Numerous studies have focused on the mechanism of Al toxicity and tolerance in plants; however, the effects of Al toxicity on soil microorganisms and their tolerance remain less studied. This study investigated the distribution and association patterns of Al-tolerant microorganisms across continental paddy fields with a soil pH range of 3.6 to 8.7. The results showed that soil pH filters exchangeable Al³⁺ content, diversity, and potential associations of Al-tolerant microbial community. The influential taxa in community network play an important role in Al tolerance and have potential applications in mitigating Al toxicity and promoting crop growth in acidic soils.

Keywords: Al-tolerant bacteria; aluminum toxicity; directed network; functional genes; niche breadth.

FIG 1

Hypothesis of this study. Reassembly of the soil microbial communities and prediction of the roles in microbial associations in acidic and highly exchangeable Al³⁺ soils.

FIG 2

Distribution of Al-tolerant microorganisms in paddy soils. (a) Al content in 39 typical paddy fields from north to south China. (b and c) Shannon index (b) and richness (c) of Al-tolerant bacteria. The horizontal bars within the boxes indicate median values. The tops and bottoms of the boxes indicate the 75th and 25th percentiles, respectively. (d) Redundancy analysis of the Al-tolerant bacterial community structure. MAT, mean annual temperature; MAP, mean annual precipitation; DON, dissolved organic nitrogen; DTN, dissolved total nitrogen; TN, total nitrogen; OM, organic matter; DOC, dissolved organic carbon; TP, total phosphorus; AP, available phosphorus; TK, total potassium; AK, available potassium; CEC, cation exchange capacity.

FIG 3

Associations between Al-tolerant microorganisms and Al-resistant genes in three pH ranges. (a) Intensity of Al-resistant functional genes at the different pH values. (b) Networks between Al-tolerant microorganisms and Al-resistant functional genes at different pH values. A connection indicates a strong (Spearman’s r > 0.6) and significant (false discovery rate-corrected P < 0.01) correlation. The size of each node is proportional to the degree; the thickness of a connection between two nodes (i.e., an edge) is proportional to the value of Spearman’s correlation coefficient. Yellow indicates the bacterial OTUs, and purple indicates the Al-resistant functional genes. Some Al-resistant functional genes without specific region names were labeled with their potential source strains, which belong to the other Al-resistant functional genes. The red lines indicate the connections between genes and species, and the gray lines indicate the connections between genes and genes and/or species and species.

FIG 4

Roles and diversity of the three microbial taxa in the directed network. (a) Inferred potential microbial interdependent associations in acidic soils. The nodes are the OTUs labeled with their genus-level taxon name, and the directed edges are the nonzero entries in the inferred interaction matrix. The directed positive and negative edges are colored in red and blue, respectively. Orphan nodes are not shown. (b) Alpha diversity (Shannon index, richness, and relative abundance) of three functional taxa. The horizontal bars within the boxes indicate median values. The tops and bottoms of the boxes indicate the 75th and 25th percentiles, respectively. (c) Redundancy analysis of community compositions of three functional taxa. MAT, mean annual temperature; MAP, mean annual precipitation; DON, dissolved organic nitrogen; DTN, dissolved total nitrogen; TN, total nitrogen; OM, organic matter; DOC, dissolved organic carbon; TP, total phosphorus; AP, available phosphorus; TK, total potassium; AK, available potassium; CEC, cation exchange capacity.

FIG 5

Niche breadth of three functional taxa and their relationship with antioxidant functional genes. (a) Comparison of mean habitat niche breadths (Bcom) of different functional taxa in bacterial community in all samples and in samples with different pH conditions (nonsignificant [n.s.], P > 0.05; *, P < 0.05; Duncan’s test). (b) Pairwise comparisons of the antioxidant function genes are shown, with a color gradient denoting the Spearman correlation coefficient. The taxonomic community composition is related to each antioxidant function gene via partial Mantel tests. The edge width corresponds to Mantel’s r statistic for the corresponding distance correlation, and the edge color denotes the statistical significance based on 9,999 permutations.