Genome-resolved metagenomics provides insights into the ecological roles of the keystone taxa in heavy-metal-contaminated soils

Abstract

Microorganisms that exhibit resistance to environmental stressors, particularly heavy metals, have the potential to be used in bioremediation strategies. This study aimed to explore and identify microorganisms that are resistant to heavy metals in soil environments as potential candidates for bioremediation. Metagenomic analysis was conducted using microbiome metagenomes obtained from the rhizosphere of soil contaminated with heavy metals and mineral-affected soil. The analysis resulted in the recovery of a total of 175 metagenome-assembled genomes (MAGs), 73 of which were potentially representing novel taxonomic levels beyond the genus level. The constructed ecological network revealed the presence of keystone taxa, including Rhizobiaceae, Xanthobacteraceae, Burkholderiaceae, and Actinomycetia. Among the recovered MAGs, 50 were associated with these keystone taxa. Notably, these MAGs displayed an abundance of genes conferring resistance to heavy metals and other abiotic stresses, particularly those affiliated with the keystone taxa. These genes were found to combat excessive accumulation of zinc/manganese, arsenate/arsenite, chromate, nickel/cobalt, copper, and tellurite. Furthermore, the keystone taxa were found to utilize both organic and inorganic energy sources, such as sulfur, arsenic, and carbon dioxide. Additionally, these keystone taxa exhibited the ability to promote vegetation development in re-vegetated mining areas through phosphorus solubilization and metabolite secretion. In summary, our study highlights the metabolic adaptability and ecological significance of microbial keystone taxa in mineral-affected soils. The MAGs associated with keystone taxa exhibited a markedly higher number of genes related to abiotic stress resistance and plant growth promotion compared to non-keystone taxa MAGs.