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Abundant and diverse arsenic-metabolizing microorganisms in peatlands treating arsenic-contaminated mining wastewaters.

ABSTRACT: Mining operations produce large quantities of wastewater. At a mine site in Northern Finland, two natural peatlands are used for the treatment of mining-influenced waters with high concentrations of sulphate and potentially toxic arsenic (As). In the present study, As removal and the involved microbial processes in those treatment peatlands (TPs) were assessed. Arsenic-metabolizing microorganisms were abundant in peat soil from both TPs (up to 108 cells gdw -1 ), with arsenate respirers being about 100 times more abundant than arsenite oxidizers. In uninhibited microcosm incubations, supplemented arsenite was oxidized under oxic conditions and supplemented arsenate was reduced under anoxic conditions, while little to no oxidation/reduction was observed in NaN3 -inhibited microcosms, indicating high As-turnover potential of peat microbes. Formation of thioarsenates was observed in anoxic microcosms. Sequencing of the functional genemarkers aioA (arsenite oxidizers), arrA (arsenate respirers) and arsC (detoxifying arsenate reducers) demonstrated high diversity of the As-metabolizing microbial community. The microbial community composition differed between the two TPs, which may have affected As removal efficiencies. In the present situation, arsenate reduction is likely the dominant net process and contributes substantially to As removal. Changes in TP usage (e.g. mine closure) with lowered water tables and heightened oxygen availability in peat might lead to re-oxidation and re-mobilization of bound arsenite.

SUBMITTER: Kujala K

PROVIDER: S-EPMC7187466 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Abundant and diverse arsenic-metabolizing microorganisms in peatlands treating arsenic-contaminated mining wastewaters.

Kujala Katharina K Besold Johannes J Mikkonen Anu A Tiirola Marja M Planer-Friedrich Britta B

Environmental microbiology 20200206 4

Mining operations produce large quantities of wastewater. At a mine site in Northern Finland, two natural peatlands are used for the treatment of mining-influenced waters with high concentrations of sulphate and potentially toxic arsenic (As). In the present study, As removal and the involved microbial processes in those treatment peatlands (TPs) were assessed. Arsenic-metabolizing microorganisms were abundant in peat soil from both TPs (up to 108 cells gdw -1 ), ...[more]

PMID: 31984582

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Project description:Arsenic contamination in water by natural causes or industrial activities is a major environmental concern, and treatment of contaminated waters is needed to protect water resources and minimize the risk for human health. In mining environments, treatment peatlands are used in the polishing phase of water treatment to remove arsenic (among other contaminants), and peat microorganisms play a crucial role in arsenic removal. The present study assessed culture-independent diversity obtained through metagenomic and metatranscriptomic sequencing and culture-dependent diversity obtained by isolating psychrotolerant arsenic-tolerant, arsenite-oxidizing, and arsenate-respiring microorganisms from a peatland treating mine effluent waters of a gold mine in Finnish Lapland using a dilution-to-extinction technique. Low diversity enrichments obtained after several transfers were dominated by the genera Pseudomonas, Polaromonas, Aeromonas, Brevundimonas, Ancylobacter, and Rhodoferax. Even though maximal growth and physiological activity (i.e., arsenite oxidation or arsenate reduction) were observed at temperatures between 20 and 28°C, most enrichments also showed substantial growth/activity at 2-5°C, indicating the successful enrichments of psychrotolerant microorganisms. After additional purification, eight arsenic-tolerant, five arsenite-oxidizing, and three arsenate-respiring strains were obtained in pure culture and identified as Pseudomonas, Rhodococcus, Microbacterium, and Cadophora. Some of the enriched and isolated genera are not known to metabolize arsenic, and valuable insights on arsenic turnover pathways may be gained by their further characterization. Comparison with phylogenetic and functional data from the metagenome indicated that the enriched and isolated strains did not belong to the most abundant genera, indicating that culture-dependent and -independent methods capture different fractions of the microbial community involved in arsenic turnover. Rare biosphere microorganisms that are present in low abundance often play an important role in ecosystem functioning, and the enriched/isolated strains might thus contribute substantially to arsenic turnover in the treatment peatland. Psychrotolerant pure cultures of arsenic-metabolizing microorganisms from peatlands are needed to close the knowledge gaps pertaining to microbial arsenic turnover in peatlands located in cold climate regions, and the isolates and enrichments obtained in this study are a good starting point to establish model systems. Improved understanding of their metabolism could moreover lead to their use in biotechnological applications intended for bioremediation of arsenic-contaminated waters.

Project description:Selenium (Se) is an essential element for most organisms yet can cause severe negative biological consequences at elevated levels. The oxidized forms of Se, selenate [Se(VI)] and selenite [Se(IV)], are more mobile, toxic, and bioavailable than the reduced forms of Se such as volatile or solid phases. Thus, selenate and selenite pose a greater threat to ecosystems and human health. As current Se remediation technologies have varying efficiencies and costs, novel strategies to remove elevated Se levels from environments impacted by anthropogenic activities are desirable. Some common soil fungi quickly remove Se (IV and VI) from solution by aerobic reduction to solid or volatile forms. Here, we perform bench-scale culture experiments of two Se-reducing Ascomycota to determine their Se removal capacity in growth media conditions containing either Se(IV) or Se(VI) as well as in Se-containing municipal (∼25 μg/L Se) and industrial (∼2000 μg/L Se) wastewaters. Dissolved Se was measured throughout the experiments to assess Se concentration and removal rates. Additionally, solid-associated Se was quantified at the end of each experiment to determine the amount of Se removed to solid phases (e.g., Se(0) nanoparticles, biomass-adsorbed Se, or internal organic selenoproteins). Results show that under optimal conditions, fungi more efficiently remove Se(IV) from solution compared to Se(VI). Additionally, both fungi remove a higher percentage of Se from the filtered municipal wastewater compared to the industrial wastewater, though cultures in industrial wastewater retained a greater amount of solid-associated Se. Additional wastewater experiments were conducted with supplemental carbohydrate- or glycerin-based carbon products and additional nitrogen- and phosphorous-containing nutrients in some cases to enhance fungal growth. Relative to unamended wastewater experiments, supplemental carbohydrates promote Se removal from municipal wastewater but minimally impact industrial wastewater removal. This demonstrates that carbon availability and source impacts fungal Se reduction and removal from solution. Calculations to assess the leaching potential of solid-associated Se from fungal biomass show that wastewater Se release will not exceed regulatory limits. This study highlights the considerable potential for the mycoremediation of Se-contaminated wastewaters.

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Abundant and diverse arsenic-metabolizing microorganisms in peatlands treating arsenic-contaminated mining wastewaters.

Publications

Abundant and diverse arsenic-metabolizing microorganisms in peatlands treating arsenic-contaminated mining wastewaters.

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