Genome-resolved metagenomics reveal soil and viral drivers of keystone bacterial traits shaping nutrient cycling and soybean yield across agroecosystems

Abstract

Soil microbes are crucial for agricultural sustainability, yet the genomic evidence of their interactions with soil abiotic and biotic factors remains unclear. Herein, we evaluated the contribution of soil bacteria to soil functions and soybean yields by analyzing 4281 bacterial metagenomic assembled genomes (MAGs) recovered from 113 natural fields across China, integrated 12 enzymic activities and 58 quantified nutrient-cycling genes. Genome-resolved metagenomics revealed the diverse genic traits of keystone bacteria, and their roles in nutrient accumulation, fungal pathogen suppression, and herbicide biodegradation, thereby promoting soybean yields. Soil pH and C/N content were important abiotic factors that determined the dominant life history strategy of keystone communities, thus affecting nutrient-cycling genes abundance. We proposed agricultural management suggestions based on diversified planting aligned with the soil environmental preferences of keystone bacteria, verified in two long-term cropping fields. By recovering 7803 vMAGs, we found the lysogenic virus-host dynamics could promote keystone bacteria adaptation by providing P-acquisition auxiliary metabolic genes (AMGs), leading to ecological advantages. We reported a novel P-acquisition strategy involving phnA-associated phosphonate hydrolysis employed by viruses, significantly influencing keystone-host phosphorus cycling. Overall, our study significantly advances the understanding of keystone bacteria in supporting crop production, with implications for precision microbiome management in agroecosystems.

Graphical abstract

Keywords

metagenomic assembled genomes / nutrient cycling / crop pathogen suppression / pesticide pollution / sustainable agriculture / virus-host dynamics

Highlight

	● Keystone bacteria’s effect on soil health was found by genome-resolved metagenomics.
	● Soil pH and C/N content were important for affecting keystone communities.
	● Available phosphorus lacked a significant effect on keystone bacteria.
	● Lysogenic virus-host dynamics help keystone bacteria adaption by P-acquisition AMGs.

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