Exploring microbial dynamics, metabolic functions and microbes–metabolites correlation in a millennium paddy soil chronosequence using metabolome and microbiome

Background

Paddy soil is a typical soil type affected by anthropogenic management and factors related to natural soil formation. The evolution from mudflats to typical paddy soils can significantly affect the soil microecology. Previous studies have reported the evolution of soil physicochemical properties, microbes, and related soil environmental factors in a millennium paddy soil chronosequence. However, the potential biological mechanisms of changes in metabolites and microbes–metabolites interaction are poorly understood. Therefore, a combination of high-throughput sequencing and environmental pseudotargeted metabolomics techniques was adopted to explore the effects of the millennium paddy soil chronosequence on microbial communities, metabolites, and their functions and interactions.

Results

The soil ecology changed greatly in the first 60 years of the transition from mudflat to paddy planting. Among the microbial communities, the response of the bacteria to the chronosequence was more sensitive than that of fungi. Among them, the bacterial communities of Proteobacteria, Bacteroidetes, Acidobacteria, and Nitrospirae exhibited regular succession over the chronosequence, but the fungal communities did not show regular changes. Bacterial function prediction revealed that the beginning of the critical stage of the evolution from mudflat to paddy soil involved the organic matter cycle and energy flow. In contrast, fungi were characterized mainly by pathogenic and saprophytic functions. The results of the principal component analysis of the metabolites revealed a similar pattern of change as that of the microbes. Seventy-five characteristic metabolites exhibited three trends of change during the development of the paddy soil chronosequence. Twenty-five differentially active metabolic pathways, including glyoxylate and dicarboxylate metabolism, starch and sucrose metabolism, and galactose metabolism, were enriched. In addition, correlation analysis revealed that long-chain fatty acids, short-chain fatty acids, phenolic acids, carbohydrates, and polyalcohols significantly regulate the microbial communities in paddy soil.

Conclusions

Combining metabolome and microbiome has expanded the overall understanding of the development of paddy soil under anthropogenic management. During the development of a paddy soil chronosequence, the synergistic regulation of soil physicochemical properties and metabolites in the microbial community results in increased productivity. This study provides a new perspective on microbes and metabolites interaction.

Graphical Abstract