Host Lifeform Shapes Phyllospheric Microbiome Assembly in Mountain Lake: Deterministic Selection and Stochastic Colonization Dynamics

Abstract

The phyllosphere microbiome of aquatic macrophytes constitutes an integral component of freshwater ecosystems, serving crucial functions in global biogeochemical cycling and anthropogenic pollutant remediation. In this study, we examined the assembly mechanisms of epiphytic bacterial communities across four phylogenetically diverse macrophyte species (Scirpus validus, Hippuris vulgaris, Nymphoides peltatum, and Myriophyllum spicatum) inhabiting Ningwu Mayinghai Lake (38.87° N, 112.20° E), a vulnerable subalpine freshwater system in Shanxi Province, China. Through 16S rRNA amplicon sequencing, we demonstrate marked phyllospheric microbiome divergence, as follows: Gammaproteobacteria dominated S. validus, H. vulgaris and N. peltatum, while Alphaproteobacteria dominated in M. spicatum. The nitrate, nitrite, and pH value of water bodies and the chlorophyll, leaf nitrogen, and carbon contents of plant leaves are the main driving forces affecting the changes in the β-diversity of epiphytic bacterial communities of four plant species. The partitioning of assembly processes revealed that deterministic dominance governed S. validus and M. spicatum, where niche-based selection contributed 67.5% and 100% to community assembly, respectively. Conversely, stochastic processes explained 100% of the variability in H. vulgaris and N. peltatum microbiomes, predominantly mediated by dispersal limitation and ecological drift. This investigation advances the understanding of microbial community structural dynamics and diversity stabilization strategies in aquatic macrophyte-associated microbiomes, while establishing conceptual frameworks between plant-microbe symbiosis and the ecological homeostasis mechanisms within vulnerable subalpine freshwater ecosystems. The empirical references derived from these findings offer novel perspectives for developing conservation strategies aimed at sustaining biodiversity equilibrium in high-altitude lake habitats, particularly in the climatically sensitive regions of north-central China.

Keywords: assembly mechanisms; diversity; epiphytic bacteria; macrophyte; subalpine lakes.

Figure 1

Four aquatic plants collected from the environment of Mayinghai Lake in Ningwu, Shanxi, China.

Figure 2

Compositions of epiphytic bacterial communities on the leaves of four aquatic plants: (A) dominant bacterial phyla; (B) dominant bacterial genera. LHV refers to the leaves of Hippuris vulgaris; LMS refers to the leaves of Myriophyllum spicatum; LNP refers to the leaves of Nymphoides peltatum; and LSV refers to the leaves of Scirpus validus. The same applies hereinafter.

Figure 3

(A) Distribution characteristics of leaf-surface-associated bacterial communities of four aquatic plants at the OTU level and (B) heatmap of dominant shared OTUs distribution (relative abundance greater than 1%).

Figure 4

Alpha diversity indexes of the epiphytic bacterial communities. * Significance level, p: ** p < 0.01.

Figure 5

Hierarchical clustering analysis of epiphytic bacterial communities at the OTU level based on Bray–Curtis distance. Cluster I represents a group of data points with structurally similar properties (in terms of distances). Cluster II represents another group of data points that share similar internal structures.

Figure 6

Mantel analysis of the plants’ epiphytic bacterial community. Edge widths in the network correspond to Mantel’s r values, and colors denote statistical significance. Edge width corresponds to the Mantel’s r statistic of distance correlation, while edge color denotes statistical significance. Np: nitrogen content in plant leaves; Cp: carbon content in plant leaves; Sp: sulfur content in plant leaves; Chla: chlorophyll a; Chlb: chlorophyll b. * Significance level, p: * p < 0.05, ** p < 0.01, *** p < 0.001.

Figure 7

Construction process and βNTI values of the epiphytic bacterial communities of four aquatic plants. * Significance level, p: * p < 0.05. The diamond represents the value corresponding to the box plot.

Figure 8

Path analysis of the epiphytic bacterial communities of four aquatic plants.