Identification of Metabolic Gaps in the Microbial Cycling of Carbon Limiting Soil Formation in Coal Mine Spoil and Degraded Topsoil: Implications for Rehabilitating Open Pit Coal Mines

ABSTRACT Through cycling of carbon, nitrogen, and phosphorus, microorganisms modify soil structure to improve the condition of degraded soils and should therefore be part of the management practices associated with the rehabilitation of mined land. In this study, we investigated microbial communities in poor‐quality coal mine spoil undergoing field‐scale rehabilitation treatments. Metagenomic analyses revealed critical metabolic gaps in spoil, including reduced abundance of glycoside hydrolase (GH) families (e.g., GH5, GH6) essential for cellulose degradation, compared to spoil amended with topsoil and undisturbed reference soil. Notably, bacterial bglU (β‐glucosidase) and cbh (cellobiohydrolase) genes were dominant over fungal counterparts, with Actinobacteria driving carbon cycling in unamended spoil. Despite these adaptations, high pH (> 8) and sodicity (ESP > 15%) constrained microbial enzyme activities (e.g., β‐glucosidase, phosphatase), limiting nutrient cycling. The addition of topsoil did not mitigate pH or sodicity, which are major limitations of spoils during mine rehabilitation. Conversely, the organic carbon in spoil improved over time, reaching ~1% by trial end, as well as phosphorus availability, mirroring undisturbed reference soil levels. The observed changes in organic carbon content in the spoil can be indirectly attributed to a shift in the microbial community and GH gene family compositions, resulting in different carbohydrate utilisation pathways in spoil over time. Microbial community shifts, particularly increased oligotrophic Planctomycetes ( Gemmataceae , Isosphaeraceae ) and drought‐tolerant Actinobacteria, highlighted spoil's resilience under abiotic stress. However, fungal diversity (e.g., Aspergillaceae ) declined with moisture fluctuations, reducing lignocellulose degradation capacity. These findings underscore that water limitation, coupled with persistent geochemical barriers, impedes microbial functions critical for pedogenesis. Pedogenesis in spoil normally takes decades; however, targeted interventions, such as inoculating pH‐tolerant cellulolytic microbes or optimising irrigation to stabilise moisture, could accelerate rehabilitation by closing functional gaps in carbon and nutrient cycling. Integrating microbial management with organic amendments (e.g., mulch) may thus enhance spoil‐to‐soil transformation, offering a scalable strategy for post‐mining rehabilitation.