Aims <p>Heavy metals delivered through atmospheric deposition represent a major stressor in terrestrial ecosystems. As a living skin at the soil–atmosphere boundary, biological soil crusts (biocrusts) are directly exposed to metal-enriched dust deposition and can serve as sensitive bioindicators of atmospheric metal inputs. However, our understanding of how biocrusts respond to long-term coal-derived atmospheric metal deposition—and the role microorganisms play in this process—remains limited. This study explores how biocrusts functionally respond to persistent inputs of metal-rich dust and elucidates the linkage pathways connecting metal deposition, bacterial communities, and soil multifunctionality.</p> Methods <p>Along the prevailing wind direction, we established a high-deposition region (PLI = 1.68) and a reference region (PLI = 0.92) around a coal-fired power plant in a semi-arid sandy ecosystem in northwest China, with replicated plots for algal, mixed (algal + moss), and moss biocrusts in each region. Bacterial diversity and community composition were characterized using high-throughput sequencing. Random forest analysis was used to identify microbial predictors of soil multifunctionality, and partial least squares path modeling (PLS-PM) was employed to infer causal pathways among metal deposition levels, soil multifunctionality, and microbial community attributes.</p> Results <p>Biocrusts from the high metal-deposition region exhibited significantly higher multifunctionality, with moss biocrusts showing the most pronounced enhancement. Long-term metal deposition increased bacterial richness and diversity in algal biocrusts but reduced both metrics in mixed and moss biocrusts. Bacterial predictors showed taxa-specific responses to metal-rich dust: the relative abundances of Actinobacteria and Proteobacteria increased, while Bacteroidetes and Cyanobacteria declined. PLS-PM revealed that in the reference region, metal inputs directly and positively influenced multifunctionality, whereas in the high deposition region, this direct effect disappeared and was replaced by an indirect pathway whereby metal deposition enhanced multifunctionality by suppressing edaphic factors. Keystone taxa shifted from K-strategist Proteobacteria to stress-tolerant Cyanobacteria and Bacteroidetes under elevated metal deposition.</p> Conclusions <p>Biocrusts act as critical “guardians” of soils in areas affected by long-term atmospheric emissions. By reorganizing the functional roles of dominant microbial groups, they adjust to persistent coal-derived metal inputs and maintain soil multifunctionality. Consequently, biocrusts hold strong potential as both indicators and agents for mitigating heavy metal contamination in degraded industrial landscapes.</p>