Comparative Metagenomics Reveals Microbial Signatures of Sugarcane Phyllosphere in Organic Management

Abstract

Converting conventional farms to organic systems to improve ecosystem health is an emerging trend in recent decades, yet little is explored to what extent and how this process drives the taxonomic diversity and functional capacity of above-ground microbes. This study was, therefore, conducted to investigate the effects of agricultural management, i.e., organic, transition, and conventional, on the structure and function of sugarcane phyllosphere microbial community using the shotgun metagenomics approach. Comparative metagenome analysis exhibited that farming practices strongly influenced taxonomic and functional diversities, as well as co-occurrence interactions of phyllosphere microbes. A complex microbial network with the highest connectivity was observed in organic farming, indicating strong resilient capabilities of its microbial community to cope with the dynamic environmental stressors. Organic farming also harbored genus Streptomyces as the potential keystone species and plant growth-promoting bacteria as microbial signatures, including Mesorhizobium loti, Bradyrhizobium sp. SG09, Lactobacillus plantarum, and Bacillus cellulosilyticus. Interestingly, numerous toxic compound-degrading species were specifically enriched in transition farming, which might suggest their essential roles in the transformation of conventional to organic farming. Moreover, conventional practice diminished the abundance of genes related to cell motility and energy metabolism of phyllosphere microbes, which could negatively contribute to lower microbial diversity in this habitat. Altogether, our results demonstrated the response of sugarcane-associated phyllosphere microbiota to specific agricultural managements that played vital roles in sustainable sugarcane production.

Keywords: agricultural shift; farming practices; microbial signatures; phyllosphere; sugarcane.

FIGURE 1

Microbial taxonomic composition of sugarcane phyllosphere. Relative abundance at (A) domain and (B) phylum levels in conventional (CP), organic (OP), and transition (TP) farming practices.

FIGURE 2

Effect of farming practices on taxonomic α-diversity determined using (A) the Shannon index and (B) Pielou evenness, and (C) microbial gene diversity estimated with the Shannon index. Statistical analysis was performed on one-way ANOVA.

FIGURE 3

Unconstrained principal coordinate analysis (PCoA) based on Bray–Curtis distance for the effect of agricultural practices on (A) taxonomic diversity and (B) gene function.

FIGURE 4

The impacts of farming practices on metabolic processes at the second and third levels of KEGG hierarchy. The statistical test was performed using one-way ANOVA in which p-values < 0.05 were considered significant as represented by the (*) symbol, while the (.) character reflected p-value < 0.1.

FIGURE 5

Farming-specific co-occurrence networks of (A) organic, (B) transition, and (C) conventional farming practices. Green and red colors of the edges represent positive and negative relationships, respectively, while the color of nodes demonstrates network modules. The shape of vertices reflects microbial domains (i.e., circle: bacteria; square: fungi; and diamond: archaea), and the size of nodes refers to abundances. In addition, the nodes with black borders were assigned as hub taxa, and the width of the border reflects the node degree score. Note: only nodes with at least 1 connection are visualized. (D) Network connectivity or node degree represents the number of edges connected to a node. The symbol (***) represents statistical significance of p-value < 0.0001.

FIGURE 6

LEfSe analysis of taxonomic abundance among organic (green), transition (blue), and conventional (red) farming practices at the species level.

FIGURE 7

LEfSe analysis of functional abundance based on the KEGG pathway in all farming practices.