Ecological Processes of Bacterial and Fungal Communities Associated with Typha orientalis Roots in Wetlands Were Distinct during Plant Development

Abstract

Root-associated microbiomes are essential for the ecological function of the root system. However, their assembly mechanisms in wetland are poorly understood. In this study, we explored and compared the ecological processes of bacterial and fungal communities in water, bulk soil, rhizosphere soil, and root endosphere niches for 3 developmental stages of Typha orientalis at different wetland sites, and assessed the potential functions of root endosphere microbiomes with function prediction. Our findings suggest that the microbial diversity, composition, and interaction networks along the water-soil-plant continuum are shaped predominantly by compartment niche and developmental stage, rather than by wetland site. Source tracking analysis indicated that T. orientalis' root endosphere is derived primarily from the rhizosphere soil (bacteria 39.9%, fungi 27.3%) and water (bacteria 18.9%, fungi 19.1%) niches. In addition, we found that the assembly of bacterial communities is driven primarily by deterministic processes and fungal communities by stochastic processes. The interaction network among microbes varies at different developmental stages of T. orientalis, and is accompanied by changes in microbial keystone taxa. The functional prediction data supports the distribution pattern of the bacterial and fungal microbiomes, which have different ecological roles at different plant developmental stages, where more beneficial bacterial taxa are observed in the root endosphere in the early stages, but more saprophytic fungi in the late stages. Our findings provide empirical evidence for the assembly, sources, interactions, and potential functions of wetland plant root microbial communities and have significant implications for the future applications of plant microbiomes in the wetland ecosystem. IMPORTANCE Our findings provide empirical evidence for the assembly, sources, interactions, and potential functions of wetland plant root microbial communities, and have significant implications for the future applications of plant microbiomes in the wetland ecosystem.

Keywords: Typha orientalis; developmental stage; ecological process; root endosphere; root-associated microbiome; wetland.

FIG 1

Temporal dynamics of diversity and distribution patterns of microbiomes. (a) Alpha diversity of bacterial and fungal communities in water, bulk soils, rhizosphere soils, and root endosphere. (b) Alpha diversity of bacterial and fungal communities in water, bulk soils, rhizosphere soils, and root endosphere across 3 plant developmental stages. (c) NMDS ordinations based on Bray-Curtis dissimilarity matrices depicting the distribution patterns of bacterial and fungal communities along the water-soil-plant continuum (n = 162). (d) NMDS ordinations based on Bray-Curtis dissimilarity matrices of bacterial and fungal communities in each compartment niche (water: n = 27; other niches: n = 45).

FIG 2

Taxonomic composition and potential sources of bacterial and fungal microbiomes. Temporal dynamics of (a) bacterial communities and (b) fungal communities in water, bulk soils, rhizosphere soils, and root endosphere at 3 sampling sites. Potential source and contribution of the root-associated (c) bacterial community and (d) fungal community.

FIG 3

Deterministic and stochastic processes in microbiome assembly. (a and b) Relative contributions of determinism (|βNTI| ≥ 2) and stochasticity (|βNTI| < 2) on microbiome assembly along the water-soil-plant root continuum under a null model. The percentage above and below the violin plot represents the proportion of deterministic and stochastic processes in microbiome assembly, respectively. (c and d) The relative importance of 5 ecological processes along the water-soil-plant root continuum: heterogeneous selection (βNTI < -2), homogeneous selection (βNTI > 2), dispersal limitation (|βNTI| < 2 and RC_Bray > 0.95), homogenizing dispersal (|βNTI| < 2 and RCBray < -0.95), and undominated (|βNTI| < 2 and |RC_Bray| < 0.95).

FIG 4

Temporal dynamics of bacterial-fungal interaction networks. Co-occurrence network analysis of the full data set (n = 162) of microbial interaction network patterns across the three developmental stages.

FIG 5

Functional profiles of root endosphere microbiomes. (a) NMDS ordinations based on Bray-Curtis dissimilarity matrices of functional taxa in bacterial and fungal communities in the root endosphere across the 3 plant developmental stages (n = 45). (b) The temporal dynamics of functional taxa compositions of bacterial and fungal communities based on FAPROTAX (bacteria) and FUNGuild (fungi) in the root endosphere.