Root Niches of Blueberry Imprint Increasing Bacterial-Fungal Interkingdom Interactions along the Soil-Rhizosphere-Root Continuum

Abstract

Plant root-associated microbiomes play critical roles in promoting plant health, productivity, and tolerance to biotic/abiotic stresses. Blueberry (Vaccinium spp.) is adapted to acidic soils, while the interactions of the root-associated microbiomes in this specific habitat under various root microenvironments remain elusive. Here, we investigated the diversity and community composition of bacterial and fungal communities in various blueberry root niches (bulk soil, rhizosphere soil, and root endosphere). The results showed that blueberry root niches significantly affected root-associated microbiome diversity and community composition compared to those of the three host cultivars. Deterministic processes gradually increased along the soil-rhizosphere-root continuum in both bacterial and fungal communities. The co-occurrence network topological features showed that both bacterial and fungal community complexity and intensive interactions decreased along the soil-rhizosphere-root continuum. Different compartment niches clearly influenced bacterial-fungal interkingdom interactions, which were significantly higher in the rhizosphere, and positive interactions gradually dominated the co-occurrence networks from the bulk soil to the endosphere. The functional predictions showed that rhizosphere bacterial and fungal communities may have higher cellulolysis and saprotrophy capacities, respectively. Collectively, the root niches not only affected microbial diversity and community composition but also enhanced the positive interkingdom interactions between bacterial and fungal communities along the soil-rhizosphere-root continuum. This provides an essential basis for manipulating synthetic microbial communities for sustainable agriculture. IMPORTANCE The blueberry root-associated microbiome plays an essential role in its adaptation to acidic soils and in limiting the uptake of soil nutrients by its poor root system. Studies on the interactions of the root-associated microbiome in the various root niches may deepen our understanding of the beneficial effects in this particular habitat. Our study extended the research on the diversity and composition of microbial communities in different blueberry root compartment niches. Root niches dominated the root-associated microbiome compared to that of the host cultivar, and deterministic processes increased from the bulk soil to the endosphere. In addition, bacterial-fungal interkingdom interactions were significantly higher in the rhizosphere, and those positive interactions progressively dominated the co-occurrence network along the soil-rhizosphere-root continuum. Collectively, root niches dominantly affected the root-associated microbiome and the positive interkingdom interactions increased, potentially providing benefits for the blueberry.

Keywords: bacterial and fungal communities; co-occurrence networks; compartment niches; rhizosphere; root-associated microbiome.

FIG 1

(A and B) Alpha diversity (Shannon and Chao1 indices) of bacteria (A) and fungi (B) in different compartment niches of blueberry. Significant differences between the bulk soil, rhizosphere soil, and root endosphere are indicated in each figure panel: *, P < 0.05; **, P < 0.01; ***, P < 0.001. (C and D) NMDS analysis of bacterial (C) and fungal (D) communities along the soil-rhizosphere-root continuum of blueberry based on Bray-Curtis distance metrics.

FIG 2

Taxonomic compositions of bacterial (phylum level) (A) and fungal (class level) (B) communities of blueberry in different compartment niches.

FIG 3

LEfSe analysis of differentially abundant (LDA threshold score of ≥4.0) taxa from phylum to order of bacterial (A) and fungal (B) communities of blueberry among different compartment niches.

FIG 4

Assembly processes of bacterial and fungal communities. (A) Relative contributions of deterministic and stochastic processes in microbiome assembly based on the βNTI values. The percentages above and below the violin plots represent the proportions of the deterministic processes and stochastic processes in the microbiome assembly, respectively. (B) Relative importance of five ecological processes based on both βNTI and Bray-Curtis-based Raup-Crick index (RC_Bray) values.

FIG 5

(A to C) Co-occurrence network analysis showing the different bacterial-fungal interkingdom network patterns in the bulk soil (A), rhizosphere soil (B), and root endosphere (C) of blueberry. (D) The relative abundances of multiple correlations between bacterial and fungal taxa in interkingdom networks in different compartment niches. Connections indicate significant (P < 0.01) correlations, which were divided into positive (Spearman’s P > 0.7; red) or negative (Spearman’s P < −0.7; green) correlations.

FIG 6

(A and B) Functional predictions of bacteria (A) and fungi (B) in the root compartment niches of blueberry. The top 10 functional abundances of the bacterial community are shown, with the vertical axis indicating the functional names and the horizontal axis indicating the percentage values of the different functional abundances. Error bars show standard deviations. *, 0.01 < P < 0.05; **, 0.001 < P < 0.01; ***, P < 0.001. The horizontal axis in the fungal function prediction results indicates the different root compartment niches, and the vertical axis indicates the relative abundances of different functions in each niche. (C) Relative abundances of one taxon in root microbiomes of three cultivars.