Identifying microbial candidates for assisted phytoremediation through long-term microbial succession and functional gene shifts across a 50-year chronosequence of vanadium-titanium magnetite tailings.

Abstract

Soil microorganisms are central to vegetation restoration in metalliferous wastes. However, within mine tailings restoration chronosequences, particularly those enriched with vanadium (V), the long-term successional dynamics of microbial communities, their functional potentials, and the functional partitioning between key microbial taxa and lower-abundance microbial lineages remain poorly understood. Here, we utilized metagenomic sequencing across a 50-year restoration chronosequence to investigate changes in the microbial community and functional genes related to plant growth-promotion (phosphorus, nitrogen, and iron acquisition) and V tolerance/bioreduction. The results demonstrated significant shifts in the microbial community after five years of restoration. At the phylum level, Actinobacteria, Acidobacteria, Pseudomonadota, and Gemmatimonadota were dominant. In early stages (< 15 years), nitrogen and phosphorus acquisition genes (e.g., nif, fix, phoD) were 1.3-2.5 times more prevalent than in later stages, whereas functional genes associated with V (e.g., napA, narG, nirS) increased 1.5- to 2-fold over time. Vanadium and nitrogen were the primary environmental factors regulating both community structure and the relative abundance of critical functional genes. Keystone taxa possessed more nitrogen and phosphorus acquisition genes (65% and 45%, respectively), while metagenome-assembled genomes (MAGs) were enriched in genes related to siderophore biosynthesis (71%) and denitrification (potential V bioreduction) (65%). Based on functional gene profiles, Bradyrhizobium, Allosphingosinicella, Baekduia, Sphingomicrobium, and Hylemonella were identified as promising microbial candidates for enhancing restoration in V-contaminated sites. This study enables the development of targeted microbial consortia to mitigate nutrient deficiency and V toxicity, directly informing the design of more efficient, stage-specific phytoremediation strategies in V-rich tailings.