Interactive dynamics between rhizosphere bacterial and viral communities facilitate soybean fitness to cadmium stress revealed by time-series metagenomics

Abstract

The distinctive symbiotic relationship between rhizobacteria and soybean (Glycine max) can enhance soil fertility and assist soybean defense heavy metal stress, such as cadmium (Cd), in soils. Soil viruses are critical for modulating microbial activities and enhancing host adaptability to soil contamination by encoding auxiliary metabolic genes (AMGs). However, the community structure, functional diversity and ecological roles of soil viruses and their dynamic interactions with soil-dwelling microbes under Cd stress remain unclear. Here, we characterized the bulk and rhizosphere bacterial community in a Cd-contaminated soybean field at five growth stages and investigated the rhizosphere microbial functional traits and the viral community after flowering using metagenomics. We showed that the rhizosphere bacterial community exhibited a stronger soybean development-dependent diversity pattern relative to bulk soil and had a more critical role in predicting Cd accumulation. The relative abundance of Actinobacteria in the rhizosphere increased with soybean development, particularly in the families Nocardioidaceae and Intrasporangiaceae, which were further identified as the main contributors of amino acid transport E and secondary metabolites Q genes. Viral analysis suggested an interactive and complementary assembly between viral and bacterial communities. Importantly, viruses exhibited a broader host range during the flowering period, and infected specific functional taxa such as Bradyrhizobium and Nocardioides, highlighting their potential impact on the rhizobia-soybean symbiosis and soybean growth and fitness. Furthermore, AMGs related to element cycling and microbial metabolism were identified and functionally and phylogenetically characterized, suggesting the contribution of these virus-encoded genes to biogeochemical cycles and soybean fitness under Cd stress. Together, our results expand our understanding of the ecological functions of rhizosphere viruses in Cd pollution-stressed soils, and provide insights in developing new strategies for bioremediation of contaminated soils.