Phosphorus and Nitrogen Drive the Seasonal Dynamics of Bacterial Communities in Pinus Forest Rhizospheric Soil of the Qinling Mountains

Abstract

The temporal distribution patterns of bacterial communities, as an important group in mountain soil, are affected by various environmental factors. To improve knowledge regarding the successional seasonal dynamics of the mountain soil bacterial communities, the rhizospheric soil of a 30-year-old natural secondary Pinus tabulaeformis forest, located in the high-altitude (1900 m a.s.l.) of the temperate Qinling Mountains, was sampled and studied during four different seasons. The bacterial community composition and structure in the rhizospheric soil were studied using an Illumina MiSeq Sequencing platform. Furthermore, the edaphic properties and soil enzymatic activities (urease, phosphatase, and catalase) were measured in order to identify the main impact factors on the soil bacterial community. According to the results, all of the edaphic properties and soil enzymatic activities were significantly affected by the seasonal changes, except for the C/N ratio. Although the biomasses of soil bacterial communities increased during the summer and autumn (warm seasons), their Shannon diversity and Pielou's evenness were decreased. Proteobacteria, Acidobacteria, Actinobacteria, Planctomycetes, and Bacteroidetes were the predominant bacterial groups in all of the soil samples, and the genera of Ktedonobacter, Sphingobium as well as an unclassified member of the Ktedonobacteria were the keystone taxa. The composition and structure of soil bacterial communities were strongly impacted by the edaphic properties, especially the temperature, moisture, ammoniacal nitrogen, available phosphorus and total phosphorus which were the crucial factors to drive the temporal distribution of the soil bacterial community and diversity. In conclusion, the soil temperature, moisture and the nutrients N and P were the crucial edaphic factors for shaping the rhizospheric soil bacterial communities as season and climate change in a P. tabulaeformis forest of Qinling Mountains.

Keywords: Pinus; bacterial community; biodiversity; rhizosphere soil; season dynamics.

FIGURE 1

Seasonal changes of the soil microbial enzymatic activities in P. tabulaeformis forest located on Qinling Mountains. (A) urease activity; (B) phosphatase activity; and (C) catalase activity. Error bar denotes standard error. ^∗P < 0.05, ^∗∗P < 0.01, ^∗∗∗P < 0.001.

FIGURE 2

Taxa dynamics and Venn diagram of soil bacterial communities. The reads number (A) and OTUs (B) that are present and shared in at least 0.5% of the population at indicated seasons are aggregated and colored by phylum on a stream-graph; (C) Venn digram showing the different OTU numbers between each two seasons.

FIGURE 3

Ordination analysis of the variation in rhizospheric soil bacterial communities. (A) Non-metric multidimensional scaling (NMDS) plots of the variation in the rhizospheric soil bacterial communities of P. tabulaeformis forest based on the profiles of presence/absence of genus; (B) Principal component analysis (PCA) of the rhizospheric soil bacterial communities of P. tabulaeformis forest based on the genus abundance and soil physicochemical characteristics as variables.

FIGURE 4

Seasonal changes in alpha-diversity of the rhizospheric soil bacterial community in P. tabulaeformis forest located on Qinling Mountains. (A) Shannon; (B) OTU richness; and (C) Evenness. The horizontal bars within boxes represent the median. The tops and bottoms of boxes represent 75th and 25th quartiles, respectively. The upper and lower whiskers extend 1.5× the interquartile range from the upper edge and lower edge of the box, respectively. ^∗P < 0.05, ^∗∗P < 0.01, and ^∗∗∗P < 0.001.

FIGURE 5

Principal component analysis (PCA) based on the soil physicochemical characteristics of P. tabulaeformis forest as variables. Alpha-diversity indices were fitted as factors with significance <0.05 onto the ordination.

FIGURE 6

Network analysis showing the connectedness between the bacterial communities and edaphic factors in P. tabulaeformis forest located on Qinling Mountains. A connection stands for a strong (Spearman’s ρ > 0.6) and significant (P < 0.01) linear relationship. Variables in blue boxes represent various edaphic properties. The maximum connectedness, exhibited on the associations between the edaphic properties (AP, TP, and NH₄⁺) and soil microclimate (ST and SMC) as well as soil pH, are shown separately.

FIGURE 7

Structural equation model (SEM) showing the causal relationships among the soil bacterial community composition, alpha-diversities, enzymatic activities and edaphic properties (ST, SMC, TP, AP, and NH₄⁺) in P. tabulaeformis forest based on the results of Mantel statistics. The final model fits the data well: maximum likelihood, χ² = 0.1, df = 2, P = 0.948, goodness-of-fit index = 0.998, Akaike information criteria = 68.106 and root mean square error of approximation = 0. Red lines mean the positive standardized regression weights and blue lines indicate the negative standard regression weights.