Microbiodiversity Landscape Present in the Mine-Tailings of the “Sierra de Huautla” Biosphere Reserve, Mexico

Abstract

Large-scale mining activities generate significant amounts of waste that accumulates in the environment. These wastes, known as mine tailings, contain high levels of heavy metals, posing risks to human health and causing severe damage to ecosystems. In this study, we determined the heavy metal content of mine tailings in the Sierra de Huautla Biosphere Reserve (REBIOSH), Mexico, and investigated their effect on microbial composition. One of the sites historically contaminated with metals was sampled in three different locations, labeled S1, S2, and S3. A fourth site free of heavy metals (S4) was also used as a control. Our results showed high levels of As, Pb, Cd, and Ag, potentially dangerous metals that exceed thresholds set by international regulatory agencies. Metal contamination indices indicated moderate to extreme enrichment for As, Cd, and Pb, posing potential ecological risks. A metagenomic study of mine tailings showed a core specie-specific microbiome covered by Sinimarinibacterium flocculans, Jiangella anatolica, Thiobacillus denitrificans, Fontimonas thermophile, Sphingomonas koreensis. These may be associated with the processing of heavy metals. A comparative study using the ALDEx2 revealed that less represented species like Variovorax paradoxus, Usitatibacter rugosus, Usitatibacter palustris, Sphingosinicella microcystinivorans, Sphingobium yanoikuyae, and Stella humosa may serve as microbial markers in metal-contaminated environments. In addition, we detected rare or low-abundance species belonging to the phylum Armatimonadota, Candidatus Melainobacteriota, Candidatus Saccharimonadota, Chlamydiota, Deinococcota, Elusimicrobiota, Bacillota, Rhodothermota and Verrucomicrobiota, which could play an important role in ecosystems contaminated with heavy metals. Also, we found site-specific taxonomic representatives such as Nitrososphaera gargensis and Nitrospira nitrificans dominating the S3 ecosystem; Ensifer aridi (S2 and S1), N. nitrificans (S2), while Reyranella soli dominate the S1 soil. These organisms could be crucial for nitrogen access in oligotrophic environments and underscore the adaptability of microbial life to extreme conditions. This is the first comprehensive study of the microbial composition in this important ecological site of the Mexican geography and can provide future guidance for the management and biological treatment of mining wastes.