Microbial survival strategies in biological soil crusts of polymetallic tailing wetlands

Abstract

The role of biological soil crusts (biocrusts) in ecological restoration is dominated by microbiota. This has been extensively studied in arid ecosystems characterized by nutrient deficiencies and poor soil substrates, including metal(loid)-rich mining regions. However, in the prior study areas, water constraints obscured the toxicity and restriction of succession by heavy metals, which were essential for soil remediation in mining regions using biocrusts. Accordingly, in the current study, we characterized biocrusts from a typical polymetallic tailing wetland and performed pot incubation to evaluate microbial community succession and microbial co-occurrence patterns. Results showed that adequate water and heavy-metal stress produced thicker and more hydrophobic biocrusts than did arid conditions, promoting stronger microbial activity in tailing wetlands. Moreover, the bioinformatic analyses during pot incubation suggest three potential survival strategies. (1) Cyanobacteria variation improved the succession level of cyanobacterial crusts. Even under heavy-metal stress, succession from light to dark cyanobacterial crusts still occurred, with Coleofasciculaceae decreasing 63% and Scytonema increasing 59% compared with the control groups. (2) Keystone taxa variation maintained high inorganic nitrogen turnover. Organisms potentially capable of inorganic nitrogen turnover, including Chloroflexi A4b and SBR1031, maintained a high relative abundance accounting for 42% (15/36) of the keystone taxa. (3) Variations in the interactions among microbiota created closer-knit microbial networks. Compared with the control groups, fewer nodes (15.2%) maintained higher average clustering coefficient values (1.8%) through 14% more positive interactions in the groups exposed to heavy-metal stress at the end of the incubation experiment. This study provides insights into the distinctive survival strategies of biocrusts in metal-rich extreme environments, offering theoretical support for biocrust-mediated ecological restoration in humid metal-contaminated regions.