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Removal of Arsenic Using Acid/Metal-Tolerant Sulfate Reducing Bacteria: a New Approach for Bioremediation of High-Arsenic Acid Mine Waters

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Removal of Arsenic Using Acid/Metal-Tolerant Sulfate Reducing Bacteria: a New Approach for Bioremediation of High-Arsenic Acid Mine Waters water Communication Removal of Arsenic Using Acid/Metal-Tolerant Sulfate Reducing Bacteria: A New Approach for Bioremediation of High-Arsenic Acid Mine Waters Jennyfer Serrano 1,2 and Eduardo Leiva 1,2,3,4,* ID 1 Departamento de Química Inorgánica, Facultad de Química, Pontificia Universidad Católica de Chile, Avenida Vicuña Mackenna 4860, Macul, Santiago 7820436, Chile; [email protected] 2 Facultad de Ciencias de la Salud, Universidad Católica Silva Henríquez, General Jofré 462, Santiago 8330225, Chile 3 Departamento de Ingeniería Hidráulica y Ambiental, Pontificia Universidad Católica de Chile, Avenida Vicuña Mackenna 4860, Macul, Santiago 7820436, Chile 4 CEDEUS, Centro de Desarrollo Urbano Sustentable, El Comendador 1916, Providencia, Santiago 7520245, Chile * Correspondence: [email protected]; Tel.: +56-2-2354-7224 Received: 3 October 2017; Accepted: 15 December 2017; Published: 19 December 2017 Abstract: Fluvial sediments, soils, and natural waters in northern Chile are characterized by high arsenic (As) content. Mining operations in this area are potential sources of As and other metal contaminants, due to acid mine drainage (AMD) generation. Sulfate Reducing Bacteria (SRB) has been used for the treatment of AMD, as they allow for the reduction of sulfate, the generation of alkalinity, and the removal of dissolved heavy metals and metalloids by precipitation as insoluble metal sulfides. Thus, SRB could be used to remove As and other heavy metals from AMD, however the tolerance of SRB to high metal concentrations and low pH is limited. The present study aimed to quantify the impact of SRB in As removal under acidic and As-Fe-rich conditions. Our results show that SRB tolerate low pH (up to 3.5) and high concentrations of As (~3.6 mg·L−1). Batch experiments showed As removal of up to 73%, Iron (Fe) removal higher than 78% and a neutralization of pH from acidic to circum-neutral conditions (pH 6–8). In addition, XRD analysis showed the dominance of amorphous minerals, while Scanning Electron Microscopy/Energy Dispersive X-ray Spectroscopy (SEM-EDX) analysis showed associations between As, Fe, and sulfur, indicating the presence of Fe-S-As compounds or interaction of As species with amorphous and/or nanocrystalline phases by sorption processes. These results indicate that the As removal was mediated by acid/metal-tolerant SRB and open the potential for the application of new strains of acid/metal-tolerant SRB for the remediation of high-As acid mine waters. Keywords: Arsenic; sulfate reducing bacteria; acid mine drainage; acidic waters; acid-tolerant; metal-tolerant 1. Introduction Arsenic (As) is a ubiquitous and toxic trace metalloid, which is widely distributed in natural environments [1]. Several groundwaters, sediments and minerals of Northern Chile are enriched in As [2–5]. Specifically, the Chilean Altiplano has high concentrations of As and sulfate in fluvial waters, seriously affecting the quality of water resources and limiting the use of water for consumption, agricultural, and industrial purposes [4]. In the Azufre River sub-basin, the release of contaminants from natural and anthropogenic sources negatively impact the quality of rivers and surface waters. In this area, hydrothermal waters emerge with high concentrations of dissolved As (>3 mg·L−1), iron (Fe) (>80 mg·L−1), and a pH lower than Water 2017, 9, 994; doi:10.3390/w9120994 www.mdpi.com/journal/water Water 2017, 9, 994 2 of 12 3 [4,5]. The As occurrence in fluvial waters is linked to the presence of ferric Fe(III)-oxyhydroxide ores, because As is sorbed onto these minerals [6]. In addition, arid and semiarid climates strongly contribute to the generation of As-rich waters, due to high evaporation rates that concentrate surface runoff [7]. Despite this, little is known about the microbial speciation, precipitation/dissolution, or sorption processes that are involved in the fate of As in these systems and how they could be optimized in treatment systems. The main source of As in the environment comes from its release from As-rich minerals (e.g., arsenopyrite (FeAsS)) [1], but mining operations can accelerate their release to the aqueous phase [8]. Particularly, acid mine drainage (AMD) can enhance the release of As from different minerals [9–11]. AMD is characterized by the release of acidic waters (pH < 4) with high dissolved metals (e.g., Fe and As, among others) and sulfate concentrations [12,13]. AMD has a negative impact on the mobilization of As and can promote the release of As directly through the oxidation of As-bearing sulfide or by dissolution of As-rich mineral phases (i.e., As-rich Fe oxyhydroxides) [10,11]. The removal of As from acid waters is a great challenge, because acidic conditions favor the dissolution of As species and prevent its removal. Nevertheless, microbial communities that are selected under acidic conditions may result in an efficient treatment for As removal. Conventional treatment technologies for As removal, acid neutralization, and salt removal, such as co-precipitation, adsorption, chemical neutralization, or ion exchange processes have several limitations, both economic and operational [14]. Sulfate reduction processes mediated by Sulfate Reducing Bacteria (SRB) allow for the reduction of sulfate concentrations, precipitation of metals, and potentially increase the pH [15]. However, most strains of SRB grow and reduce sulfate optimally at a circum-neutral pH (6–8) [16]. Low pH severely affects the growth of bacteria and sulfate removal rates [17]. Likewise, metal and metalloid concentrations (e.g., Fe and As) have a negative effect on the sulfate removal rates [18]. Particularly, the growth of SRB can decline significantly under high As concentrations, due to its toxicity. Even so, several studies have shown that bacteria can tolerate low pH and can be an alternative for the treatment of acid mine waters [19–22]. Thus, bioremediation systems that are based on acid/metal-tolerant SRB could be used for the treatment of acidic metallic waters, but it is still necessary to study its feasibility of operation under specific conditions. The present study shows the removal of As from AMD waters by biological sulfate reduction processes under acidic and As-rich conditions. The relevance of these findings lies in that new strains of acid/metal-tolerant SRB can potentially be used to optimize As removal and AMD treatment simultaneously through its bacterial activity. 2. Materials and Methods 2.1. Study Site: Aguas Calientes Area in the Upper Section of the Azufre River Sub-Basin The Aguas Calientes area is located in the Azufre River sub-basin near the Tacora volcano, in the Lluta River Watershed (LRW) in northern Chile (18◦000–18◦300 S and 70◦200–69◦220 W). The area is characterized by water scarcity, high altitude (>4000 m a.s.l.), and high evaporation rates (4.9 ± 0.5 mm d−1). The Azufre River originates in the upper section of the LRW in the Altiplano with high concentrations of [As] (3.6 ± 0.46 mg·L−1), [Fe] (81.6 ± 13.5 mg·L−1), [Al] (205.3 ± 25.7 mg·L−1), [Zn] (7.4 ± 1.2 mg·L−1), 2- −1 [SO4 ](4,678 ± 16.9 mg·L ), and a pH less than 2.0 [4,5] due to contributions from hydrothermal springs and acidic metal-rich runoffs. The Aguas Calientes area is impacted by a legacy sulfur mine site on the slopes of the Tacora volcano, where there are mineral deposits of elemental sulfur and at the base of the volcano there is an accumulation of fine elemental sulfur (S0) tailings (Figure1). In addition, there is AMD generation that is associated with S0 tailings, characterized by an acidic pH (1.9 to 4.0), high specific conductivity (1.0 to 5.7 mS·cm−1), and elevated concentrations of dissolved Fe (>10 mg·L−1) and As (>0.4 mg·L−1). The S0 tailings are disposed near a natural wetland, where the decomposition of plant organic Water 2017, 9, 994 3 of 12 matter occurs and generates anaerobic environments, enabling sulfate reduction processes to occur continuously (Figure1). Water 2017, 9, 994 3 of 12 Tacora Elemental Sulfur Deposits Volcano 2- 2-SO4 SO4 S0 Tailings Surface runoff H+ Surface runoff O Azufre Tailings river Wetland Area Symbology Sampling points Azufre river 0 200m Tacora Volcano Flow Direction (a) (b) Figure 1. (a) Schematic representation of the study site in the Aguas Calientes area, Azufre River sub- Figure 1. (basina) Schematic in northern representation Chile. (b) Photograph of the study of the sitewetland in the area Aguas with a Calientes representative area, sulfate Azufre reduction River sub-basin in northern Chile;sediment (b) profile. Photograph of the wetland area with a representative sulfate reduction sediment profile. 2.2. Sampling 2.2. Sampling To evaluate sulfate reduction processes, sediment profiles were sampled at different points that To evaluatewere located sulfate at the interface reduction of S0processes, tailings with the sediment wetland growth profiles zone. were These sampled sediments atreceive different an points that wereAMD located runoff at and the have interface Fe and As of concentrations S0 tailings of withup to 187.2 the wetlandg·kg−1 and 9.5 growth g·kg−1, respectively. zone. These Five sediments receive ansampling AMD points runoff were and selected have for Fe hydrogeochemical and As concentrations analysis, elemental of up analysis to 187.2 in solid g·kg phase,−1 and and 9.5 g·kg−1, cultures of microorganisms in anaerobic reactors. Sampling points were selected based on monitoring respectively.of on-site Five geochemical sampling pointsparameters were (pH, selected Eh, cond foructivity, hydrogeochemical and dissolved oxygen analysis, (DO)) elementalin surface analysis in solid phase,waters andand saturated cultures sediments of microorganisms in the Aguas Caliente in anaerobics area carried reactors.
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