Biogenic manganese oxides promote metal(loid) remediation by shaping microbial communities in biological aqua crust.

Biological aqua crust (biogenic aqua crust-BAC) is a potentially sustainable solution for metal(loid) bioremediation in global water using solar energy. However, the key geochemical factors and underlying mechanisms shaping microbial communities in BAC remain poorly understood. The current study aimed at determining the in situ metal(loid) distribution and the key geochemical factors related to microbial community structure and metal(loid)-related genes in BAC of a representative Pb/Zn tailing pond. Here we showed that abundant metal(loid)s (e.g. Pb, As) were co-distributed with Mn/Fe-rich minerals (e.g. biogenic Mn oxide, FeOOH) in BAC. Biogenic Mn oxide (i.e. Mn) was the most dominant factor in shaping microbial community structure in BAC and source tailings. Along with the fact that keystone species (e.g. Burkholderiales, Haliscomenobacter) have the potential to promote Mn ion oxidization and particle agglomeration, as well as Mn is highly associated with metal(loid)-related genes, especially genes related to As redox (e.g. arsC, aoxA), and Cd transport (e.g. zipB), biogenic Mn oxides thus effectively enhance metal(loid) remediation by accelerating the formation of organo-mineral aggregates in biofilm-rich BAC system. Our study indicated that biogenic Mn oxides may play essential roles in facilitating in situ metal(loid) bioremediation in BAC of mine drainage.

Mechanism of arsenic immobilization and biotransformation in the biological aqua crust of mine drainage.

Biological aqua crust (BAC), as a novel biological crust with high arsenic (As) immobilization capacity, might be an ideal nature-based solution for As removal in mine drainage. This study examined the As speciation, binding fraction and biotransformation genes in the BACs to find out the underlying mechanism of As immobilization and biotransformation. Results showed that the BACs could immobilize As from mine drainage up to 55.8 g/kg, and their As immobilization concentrations were 1.3-6.9 times higher than that of sediments. Extremely high As immobilization capacity was attributed to the processes of bioadsorption/absorption and biomineralization driven by Cyanobacteria. The high abundance of As(III) oxidation genes (27.0 %) enhanced microbial As(III) oxidation, resulting in >90.0 % of As(V) with low toxicity and mobility in the BACs. The increase in abundances of aioB, arsP, acr3, arsB, arsC and arsI with As was the key process for microbiota in the BACs for resistance to the As toxicity. In conclusion, our findings innovatively confirmed the potential mechanism of As immobilization and biotransformation mediated by the microbiota in the BACs and highlighted the important role of BACs for As remediation in mine drainage.

Novel biological aqua crust enhances in situ metal(loid) bioremediation driven by phototrophic/diazotrophic biofilm.

BACKGROUND: Understanding the ecological and environmental functions of phototrophic biofilms in the biological crust is crucial for improving metal(loid) (e.g. Cd, As) bioremediation in mining ecosystems. In this study, in combination with metal(loid) monitoring and metagenomic analysis, we systematically evaluated the effect of biofilm in a novel biological aqua crust (biogenic aqua crust-BAC) on in situ metal(loid) bioremediation of a representative Pb/Zn tailing pond. RESULTS: We observed strong accumulation of potentially bioavailable metal(loid)s and visible phototrophic biofilms in the BAC. Furthermore, dominating taxa Leptolyngbyaceae (10.2-10.4%, Cyanobacteria) and Cytophagales (12.3-22.1%, Bacteroidota) were enriched in biofilm. Along with predominant heterotrophs (e.g. Cytophagales sp.) as well as diazotrophs (e.g. Hyphomonadaceae sp.), autotrophs/diazotrophs (e.g. Leptolyngbyaceae sp.) in phototrophic biofilm enriched the genes encoding extracellular peptidase (e.g. family S9, S1), CAZymes (e.g. CBM50, GT2) and biofilm formation (e.g. OmpR, CRP and LuxS), thus enhancing the capacity of nutrient accumulation and metal(loid) bioremediation in BAC system. CONCLUSIONS: Our study demonstrated that a phototrophic/diazotrophic biofilm constitutes the structured communities containing specific autotrophs (e.g. Leptolyngbyaceae sp.) and heterotrophs (e.g. Cytophagales sp.), which effectively control metal(loid) and nutrient input using solar energy in aquatic environments. Elucidation of the mechanisms of biofilm formation coupled with metal(loid) immobilization in BAC expands the fundamental understanding of the geochemical fate of metal(loid)s, which may be harnessed to enhance in situ metal(loid) bioremediation in the aquatic ecosystem of the mining area. Video Abstract.

The interplay between microalgae and toxic metal(loid)s: mechanisms and implications in AMD phycoremediation coupled with Fe/Mn mineralization.

Acid mine drainage (AMD) is low-pH with high concentration of sulfates and toxic metal(loid)s (e.g. As, Cd, Pb, Cu, Zn), thereby posing a global environmental problem. For decades, microalgae have been used to remediate metal(loid)s in AMD, as they have various adaptive mechanisms for tolerating extreme environmental stress. Their main phycoremediation mechanisms are biosorption, bioaccumulation, coupling with sulfate-reducing bacteria, alkalization, biotransformation, and Fe/Mn mineral formation. This review summarizes how microalgae cope with metal(loid) stress and their specific mechanisms of phycoremediation in AMD. Based on the universal physiological characteristics of microalgae and the properties of their secretions, several Fe/Mn mineralization mechanisms induced by photosynthesis, free radicals, microalgal-bacterial reciprocity, and algal organic matter are proposed. Notably, microalgae can also reduce Fe(III) and inhibit mineralization, which is environmentally unfavorable. Therefore, the comprehensive environmental effects of microalgal co-occurring and cyclical opposing processes must be carefully considered. Using chemical and biological perspectives, this review innovatively proposes several specific processes and mechanisms of Fe/Mn mineralization that are mediated by microalgae, providing a theoretical basis for the geochemistry of metal(loid)s and natural attenuation of pollutants in AMD.

Biological aqua crust mitigates metal(loid) pollution and the underlying immobilization mechanisms.

Biocrust-mediated in situ bioremediation could be an alternative strategy to mitigate metal(loid) pollution in aquatic habitats. To better understand the roles of biocrusts in regulating the fate of metal(loid)s, we examined the morphology, composition and structure of biological aqua crusts (BAC) developed in the mine drainage of a representative Pb/Zn tailing pond, and tested their effectiveness for immobilizing typical metal(loid)s. Unlike terrestrial biocrusts, BAC results from an assembly of compounds produced by the strong microbial activity and mineral compounds present in the aquatic environment. The BAC exhibited a unique flexible, spongy and porous structure with a specific surface area of 12-22 m2 g-1, and was able to effectively concentrate various metal(loid)s (e.g. Cd, 0.26-0.60 g kg-1; Pb, 0.52-0.66 g kg-1; As, 10.4-24.3 g kg-1). The concentrations of metal(loid)s (e.g. Cd and As) in the BAC were even three to seven times higher than those in the source tailings, and more than 98% of immobilized metal(loid)s were present as the highly stable non-EDTA-exchangeable fraction. Adsorption on the well distributed micro-particles of the clay minerals (e.g. kaolinite) and the organic matters (2.0-2.7 wt.%) were found to be the major mechanisms for BAC to bind metal cations, whereas adsorption and coprecipitation on Fe/Mn oxide (e.g. FeOOH), was proposed to be the dominant pathway for accumulating metal(loid)s, especially As. The decrease in aqueous concentrations of the metal(loid)s along the drainage could be attributed in part to the scavenging effects of the BAC. These findings therefore provide new insights into the possible and efficient strategy for metal(loid) removal from water bodies, and highlighted the important role of BAC as a nature-based solution to benefit the bioremediation of mining area.

Mobility of metal(loid)s in Pb/Zn tailings under different revegetation strategies.

Metal tailings are potential sources of strong environmental pollution. In situ remediation involves the installation of a plant cover to stabilize materials and pollutants. Whether metal(loid)s are effectively immobilized in remediated tailing ponds submitted to heavy rainfall remains uncertain. In this study, tailing materials were collected from bare tailings (control), grass-planted (G) and grass-shrub planted (GS) areas on a former Pb/Zn mine site. Batch column experiments were performed with three rainfall intensities of 0.36, 0.48, and 0.50 mL min-1 for 18 d in the lab. The pH, Eh, Cd, Pb, Zn and As concentration in leachate were recorded. Selected leached tailing materials were finally characterized. Results showed that leachates from control were strongly acidic (pH 3.11-4.65), and that Cd, Pb, Zn and As were quickly released at high rate (e.g., 945 mg L-1 Zn). During the experiment up to 4% Cd present in the material was released and almost 1% Zn. With material collected from the G area, leachates were even more acidic (2.16-2.84) with a rainfall intensity of 0.50 mL min-1 and exhibited a high redox potential (588-639 mV). However, concentrations of metals in leachates were much lower than that in the control, except for Zn (e.g., 433 mg L-1), and they tended to decrease with time. Cumulative leaching rate was still relatively high (e.g., 0.68% Cd; 0.75% Zn) during the first eight days (stage I). However, with the GS treatment, leachate pH gradually raised from acid to alkaline values (3.9-8.2) during stage I, then remained high until the end of the experiment (stage II). Also, amounts of elements released during the 18 d were low in general. The releasing ratios of Cd (R2 > 0.95), Pb (R2 > 0.95), As (R2 > 0.87), and Zn (R2 > 0.90) fitted well with a two-constant model. In conclusion, under subtropical climate with heavy rainfall, phytostabilization is effective but immobilization of metals is higher with a combination of grass and shrub than with only grass to reduce leaching of As and Zn.