Although arsenic (As) groundwater contamination in South and Southeast Asia is a threat to human health, mechanisms of its release from sediment to groundwater are still not fully understood. In many aquifers, Fe(III) minerals are often the main hosting phases for As and their stability is crucial for As mobility. Recently, a new mechanism for As mobilization into groundwater was proposed with methane (CH4) serving as an electron donor for microbially mediated reductive dissolution of As-bearing Fe(III) minerals. To provide unequivocal evidence for the occurrence of Fe(III)-coupled methanotrophy, we incubated sediments from an As-contaminated aquifer in Hanoi (Vietnam) anoxically with isotopically labeled ¹³CH4. Up to 35% of the available Fe(III) was reduced within 232 days with simultaneous production of ¹³CO2 demonstrating anaerobic oxidation of ¹³CH4 with Fe(III) as the electron acceptor. The microbial community at the end of the incubation was dominated by archaea affiliating with Candidatus Methanoperedens, implying its involvement in Fe(III)-dependent CH4 oxidation. These results suggest that methanotrophs can contribute to dissolution of As-bearing Fe(III) minerals, which eventually leads to As-release into groundwater.
Fe(III) minerals play a crucial role for arsenic (As) mobility in aquifers as they usually represent the main As-bearing phases. Microbial reductive dissolution of As-bearing Fe(III) minerals is responsible for the release of As and the resulting groundwater contamination in many sites worldwide. So far, in most studies mainly abiogenic iron minerals have been considered. Yet, biogenic minerals that possess different properties to their abiogenic counterparts are also present in the environment. In some environments they dominate the iron mineral inventory but so far, it is unclear what this means for the As mobility. We, therefore, performed an in-situ aquifer Fe(III) minerals exposure experiment i) to evaluate how different biogenic and abiogenic Fe(III) minerals are transformed in a strongly reducing, As-contaminated aquifer (25 m) compared to As-free moderately reducing aquifer (32 m) and ii) to assess which microbial taxa are involved in these Fe(III) minerals transformations. We found that higher numbers of bacteria and archaea were associated with the minerals incubated in the As-contaminated compared to the non-contaminated aquifer and that all Fe(III) minerals were mainly colonized by Fe(III)-reducing bacteria, with Geobacter being the most abundant taxon. Additionally, fermenting microorganisms were abundant on minerals incubated in the As-contaminated aquifer, while methanotrophs were identified on the minerals incubated in the As-free moderately reducing aquifer, implying involvement of these microorganisms in Fe(III) reduction. We observed that biogenic Fe(III) minerals generally tend to become more reduced and when incubated in the As-contaminated aquifer sorbed more As than the abiogenic ones. Most of abiogenic and biogenic Fe(III) minerals were transformed into magnetite while biogenic more crystalline mixed phases were not subjected to visible transformation. This in-situ Fe(III) minerals incubation approach shows that biogenic minerals are more prone to be colonized by (Fe(III)-reducing) microorganisms and bind more As, although ultimately produce similar minerals during Fe(III) reduction.
High arsenic (As) concentrations in groundwater are a worldwide problem threatening the health of millions of people. Microbial processes are central in the (trans)formation of the As-bearing ferric and ferrous minerals, and thus regulate dissolved As levels in many aquifers. Mineralogy, microbiology and dissolved As levels can vary sharply within aquifers, making high-resolution measurements particularly valuable in understanding the linkages between them. We conducted a high spatial resolution geomicrobiological study in combination with analysis of sediment chemistry and mineralogy in an alluvial aquifer system affected by geogenic As in the Red River delta in Vietnam. Microbial community analysis revealed a dominance of fermenters, methanogens and methanotrophs whereas sediment mineralogy along a 46 m deep core showed a diversity of Fe minerals including poorly crystalline Fe (II/III) and Fe(III) (oxyhydr)oxides such as goethite, hematite, and magnetite, but also the presence of Fe(II)-bearing carbonates and sulfides which likely formed as a result of microbially driven organic carbon (OC) degradation. A potential important role of methane (CH4) as electron donor for reductive Fe mineral (trans)formation was supported by the high abundance of Candidatus Methanoperedens, a known Fe(III)-reducing methanotroph. Overall, these results imply that OC turnover including fermentation, methanogenesis and CH4 oxidation are important mechanisms leading to Fe mineral (trans)formation, dissolution and precipitation, and thus indirectly affecting As mobility by changing the Fe-mineral inventory.
Arsenic groundwater contamination threatens the health of millions of people worldwide, particularly in South and Southeast Asia. In most cases, the release of arsenic from sediment was caused by microbial reductive dissolution of arsenic-bearing iron(III) minerals with organic carbon being used as microbial electron donor. Although in many arsenic-contaminated aquifers high concentrations of methane were observed, its role in arsenic mobilization is unknown. Here, using microcosms experiments and hydrogeochemical and microbial community analyses, we demonstrate that methane functions as electron donor for methanotrophs, triggering the reductive dissolution of arsenic-bearing iron(III) minerals, increasing the abundance of genes related to methane oxidation, and ultimately mobilizing arsenic into the water. Our findings provide evidence for a methane-mediated mechanism for arsenic mobilization that is distinct from previously described pathways. Taking this together with the common presence of methane in arsenic-contaminated aquifers, we suggest that this methane-driven arsenic mobilization may contribute to arsenic contamination of groundwater on a global scale.
The fate of arsenic (As) in groundwater is determined by multiple interrelated microbial and abiotic processes that contribute to As (im)mobilization. Most studies to date have investigated individual processes related to As (im)mobilization rather than the complex networks present in situ. In this study, we used RNA-based microbial community analysis in combination with groundwater hydrogeochemical measurements to elucidate the behavior of As along a 2 km transect near Hanoi, Vietnam. The transect stretches from the riverbank across a strongly reducing and As-contaminated Holocene aquifer, followed by a redox transition zone (RTZ) and a Pleistocene aquifer, at which As concentrations are low. Our analyses revealed fermentation and methanogenesis as important processes providing electron donors, fueling the microbially mediated reductive dissolution of As-bearing Fe(III) minerals and ultimately promoting As mobilization. As a consequence of high CH4 concentrations, methanotrophs thrive across the Holocene aquifer and the redox transition zone. Finally, our results underline the role of SO42--reducing and putative Fe(II)-/As(III)-oxidizing bacteria as a sink for As, particularly at the RTZ. Overall, our results suggest that a complex network of microbial and biogeochemical processes has to be considered to better understand the biogeochemical behavior of As in groundwater.
Natural organic matter (NOM) can contribute to arsenic (As) mobilization as an electron donor for microbially-mediated reductive dissolution of As-bearing Fe(III) (oxyhydr)oxides. However, to investigate this process, instead of using NOM, most laboratory studies used simple fatty acids or sugars, often at relatively high concentrations. To investigate the role of relevant C sources, we therefore extracted in situ NOM from the upper aquitard (clayey silt) and lower sandy aquifer sediments in Van Phuc (Hanoi area, Vietnam), characterized its composition, and used 100-day microcosm experiments to determine the effect of in situ OM on Fe(III) mineral reduction, As mobilization, and microbial community composition. We found that OM extracted from the clayey silt (OMC) aquitard resembles young, not fully degraded plant-related material, while OM from the sandy sediments (OMS) is more bioavailable and related to microbial biomass. Although all microcosms were amended with the same amount of C (12 mg C/L), the extent of Fe(III) reduction after 100 days was the highest with acetate/lactate (43 ± 3.5% of total Fe present in the sediments) followed by OMS (28 ± 0.3%) and OMC (19 ± 0.8%). Initial Fe(III) reduction rates were also higher with acetate/lactate (0.53 mg Fe(II) in 6 days) than with OMS and OMC (0.18 and 0.08 mg Fe(II) in 6 days, respectively). Although initially more dissolved As was detected in the acetate/lactate setups, after 100 days, higher concentrations of As (8.3 ± 0.3 and 8.8 ± 0.8 μg As/L) were reached in OMC and OMS, respectively, compared to acetate/lactate-amended setups (6.3 ± 0.7 μg As/L). 16S rRNA amplicon sequence analyses revealed that acetate/lactate mainly enriched Geobacter, while in situ OM supported growth and activity of a more diverse microbial community. Our results suggest that although the in situ NOM is less efficient in stimulating microbial Fe(III) reduction than highly bioavailable acetate/lactate, it ultimately has the potential to mobilize the same amount or even more As.
Elevated concentrations of As in groundwater leading to a serious health risk for millions of people have been reported at many places all over the world. Most existing investigations are limited to a uni-disciplinary research approach, thereby neglecting the interactions between hydrochemistry, geochemistry, mineralogy, microbiology and groundwater flow. A comprehensive and highly interdisciplinary approach is necessary to reveal the complex mechanisms of As behavior, in particular for its mobilization, and the controlling factors at the redox transition zone. Therefore, the AdvectAs project seeks to bring together scientists from different research disciplines in order to understand and predict the large-scale and long-term mobility of As in groundwater at VanPhuc village in the Hanoi area (Vietnam) under advective flow conditions associated with extensive pumping rates. The overall goal of the project is to identify the decisive microbial, geochemical, mineralogical, hydrological and hydrochemical processes that govern the As mobilization and integrate all these processes in a reactive-transport model. In October 2017, a first sampling campaign was carried out. During this campaign aquifer sediments (0-45 m) were obtained using different coring techniques and groundwater as well as surface water was collected. Microbiological and molecular biological analyses focusing on Fe-and As-metabolizing bacteria, potential key players for As cycling were performed. Additionally, mineralogical and geochemical analyses of sediments, hydrochemical characterization of the groundwater as well as dating of the