Variations in Soil Nutrient Dynamics and Bacterial Communities After the Conversion of Forests to Long-Term Tea Monoculture Systems

Abstract

The soil microbial community is a key indicator to evaluate the soil health and productivities in agricultural ecosystems. Monoculture and conversions of forests to tea plantations have been widely applied in tea plantation globally, but long-term monoculture of tea plantation could lead to soil degradation and yield decline. Understanding how long-term monoculture systems influence the soil health and ecosystem functions in tea plantation is of great importance for soil environment management. In this study, through the comparison of three independent tea plantations across eastern China composed of varying stand ages (from 3 to 90 years after conversion from forest), we found that long-term tea monoculture led to significant increases in soil total organic carbon (TOC) and microbial nitrogen (MBN). Additionally, the structure, function, and co-occurrence network of soil bacterial communities were investigated by pyrosequencing 16S rRNA genes. The pyrosequencing analysis revealed that the structures and functions of soil bacterial communities were significantly affected by different stand ages, but sampling sites and land-use conversion (from forest to tea plantation) had stronger effects than stand age on the diversity and structure of soil bacterial communities. Soil bacterial diversity can be improved with increasing stand ages in tea plantation. Further RDA analysis revealed that the C and N availability improvement in tea plantation soils led to the variation of structure and function in soil bacterial communities. Moreover, co-occurrence network analysis of soil bacterial communities also demonstrated that interactions among soil bacteria taxa were strengthened with increasing stand age. Our findings suggest that long-term monoculture with proper managements could be beneficial to soil ecosystems by increasing the C and N content and strengthening bacterial associations in tea plantations. Overall, this study provides a comprehensive understanding of the impact of land-use change and long-term monoculture stand age on soil environments in tea plantation.

Keywords: co-occurrence network; monoculture system; nutrient availability; pyrosequencing; tea production.

Figure 1

(A) Sampling sites of tea plantations in Zhejiang Province, China (TRI: the Tea Research Institute of the Chinese Academy of Agricultural Sciences; HZ: Wenjiashan village, Hangzhou city; JL: Jingning county, Lishui city). (B) Taxonomic structure of the soil bacterial microbiota at the phylum level. Only the 10 phyla with the highest mean relative abundance are shown, while the other phylum groups are grouped into “others.”

Figure 2

(A) Principal component analysis (PCA) based on soil physicochemical properties as variables. The sampled tea stands from same site are outlined and grouped as the same color. (B,C) show significant linear regression (p < 0.01) between total carbon (TOC) and microbial biological nitrogen (MBN), respectively, in the soil and the stand age across all tea plantations.

Figure 3

(A) The richness of the tea plantation soil bacterial communities at varying stand ages and different sampling sites. (B,C) show significant linear regression (p < 0.001) relationships between total carbon (TOC) and soil pH in the soil, respectively, and the richness of soil bacterial communities across all tea stands. (D) Principal coordinate analysis (based on Bray–Curtis distances) of soil bacterial community composition across varying stand ages and different sampling sites. The samples are separated by sites (TRI, HZ, and JL; represented by different shapes) and stand ages [F (adjacent forest); represented by different colors].

Figure 4

Function predictions of microbial communities in tea plantation soils across varying stand ages and different sampling sites by FAPROTAX. The relative abundance of each functional category is normalized and represented by a Z-score.

Figure 5

(A) The co-occurrence networks visualize the effects of varying stand ages of tea plantations (Y3–20, Y40–50, and Y90) and the adjacent forest (F) on the co-occurrence pattern between soil bacterial taxa at family level. The node size is proportional to the abundance of taxa, and the nodes represent bacterial taxa at the family level. The edges are colored according to interaction types; positive correlations are labeled with green, and negative correlations are colored in pink. (B) CIRCOS plots showing the distribution of links among the top 10 interacting phyla in networks Y3–20, Y40–50, Y90, and F. (C) Linear regression relationships between tea stand ages and key topological parameters (ln-transformed) of all subnetworks (average path length, centralization betweenness, no. of edges, and no. of vertices). (D) Spearman’s correlations between soil physicochemical properties and topological parameters in all subnetworks. Significant correlations are marked by *p < 0.05, **p < 0.01, and ***p < 0.001. (E) Topological parameters of the networks Y3–20, Y40–50, Y90, and F.

Figure 6

(A) Distance-based redundancy analysis (RDA) of the relationships between soil physicochemical properties and bacterial communities at different sites and stand ages. The samples are separated by sites (TRI, HZ, and JL; represented by different shapes) and stand ages [including the adjacent forest (F); represented by different colors]. (B) The effects of stand age and sampling site on soil bacterial communities of tea plantations based on permutation multivariate analysis of variance (PERMANOVA).