Soil salinization alters biogeochemical cycles in agricultural ecosystems by reducing carbon-cycling microorganisms

Salinity stress can decline crop yield in agricultural systems. Beyond the environmental conditions that drive agricultural plant growth, the diverse roles of microbes represent a critical, often overlooked factor in shaping crop health and productivity. Salinization exerts a profound effect on soil microbial communities, with consequences for biogeochemical cycles. However, the salinity adaptation mechanisms of microorganisms participating in biogeochemical cycles remain incompletely understood, which hold considerable promise for microbial solutions in saline agriculture. In this study, metagenomics-based technology was employed to analyze agricultural soils within a region-scale irrigation area characterized by varying degrees of salinization. According to the results of generalized linear models, bell-shaped trends were observed for the diversity and abundance of biogeochemical cycling genes along the soil salinity gradient, all of which peaked at a salinity of approximately 7.5 ‰. Further comparisons indicated reduced total abundance of all biogeochemical cycling genes in high salinity soils (>7.5 ‰) compared to those in low salinity soils (<7.5 ‰). Furthermore, correlation analysis indicated the coupling of different biogeochemical cycling genes, which were observed to be possessed by similar functional microorganisms, with a predominance of Gammaproteobacteria and Alphaproteobacteria. The presence of elevated salt levels resulted in a decline in the abundance of various microorganisms that play roles in biogeochemical cycling, including members of the Alphaproteobacteria, Actinomycetia, Limnocylindira, and Gemmatimonadetes phyla. Concurrently, there was an enrichment of a limited number of salt-tolerant bacteria, predominantly classified under the Bacteroidia and Bacilli taxonomic groups. The coupling of different biogeochemical cycling genes in some metagenome-assembled genomes (MAGs) was confirmed through metagenomics binning. Three MAGs (strains of Methylophaga, Salinimicrobium, and Sediminibacterium, respectively) with diverse biogeochemical cycling functions were recognized as potential plant-growth-promoting bacteria under salinity stress. These findings contribute to the existing body of knowledge on the salinity adaptability of soil microbial communities and offer guidance for the management of saline agriculture.