Effects of microbially induced transformations and shift in bacterial community on arsenic mobility in arsenic-rich deep aquifer sediments
Graphical abstract
Introduction
The natural occurrence of arsenic (As)-rich groundwater has been documented in many parts of the world, including the alluvial Chianan Plain, southwestern Taiwan. Elevated concentration of As in groundwater of Chianan Plain is historically associated with unique cases of endemic black-foot disease (BFD) (i.e., gangrene), a peripheral vascular disease caused by long-term ingestion of As-contaminated groundwater [1]. As-rich groundwater, which is commonly extracted for drinking, irrigation and aquaculture purposes, has endangered the health of tens of million of people worldwide. Decades of experimentation on source, mobility and enrichment of As have implications for the employment of deeper aquifers as possible sources of As-free water [2]. However, in recent years, elevated concentrations of As in deep aquifers subjected to intensive pumping were reported in parts of Bangladesh, West Bengal, India, southern Vietnam and Chianan plain, southwestern Taiwan [3], [4], [5], [6]. This led scientists to attempt to discover the underlying causes for this phenomenon.
Arsenic mobilization from sediment to groundwater has been linked to the complex interactions between microbial activities and biogeochemical processes associated with specific sediment compositions [7], [8]. Several mechanisms have been proposed to reveal As-mobilization in As-rich aquifers [9], [10], [11], [12], [13]. Among them, the reductive dissolution of As-bearing Fe-(oxyhydr) oxides has gained significant attention, with a number of studies providing evidence on the role of metal reducing bacteria in As release into groundwater [8], [9], [14]. The mechanisms underpinning As-mobilization in the deep aquifer of Chianan Plain and the identity of the microorganisms involved were not previously investigated.
Arsenic in the solid phase of Chianan Plain aquifer material mostly occurs as a precipitate or adsorbed onto various Fe- and Mn-rich mineral phases [15]. The release of adsorbed As into groundwater in Chianan Plain is likely due to microbially mediated reductive dissolution of host mineral phases. The occurrence of elevated concentrations of Fe and bicarbonate, low concentrations of sulfate and low redox potential of these groundwater [6], [16], led us to hypothesize that microbially-mediated reductive dissolution of Fe-(oxyhydr) oxides may be the primary mechanism controlling the mobilization of As therein. However the high negative correlation between the dissolved As and Fe concentrations in the Chianan Plain groundwater [6], advocated that the hypothesis of microbially mediated reductive dissolution of As-bearing Fe-(oxyhydr) oxides for As release might be an oversimplification. Nonetheless, the fate of released As may be significantly affected by the changes in solid-phase of As-hosting minerals [17]. Arsenic-rich aquifers of Chianan Plain and other areas of similar hydrology are often found in nutrient limiting condition [8], [14], [15]. In particular, the total organic carbon contents in the sediments of this region are very low (<1%) [15]. Previously conducted microcosm experiments consisting of slurry sediments from As-enriched shallow aquifers from this region revealed that the release of sedimentary As into groundwater was not limited by the presence of reactive organic carbon [14]. In addition, it was observed that inorganic electron donors (e.g., As, Fe, Mn etc.) could also fuel microbial dissimilatory As(V) reduction, thereby highlighting the involvement of chemolithotrophic processes in the release of As into solution [18]. These earlier investigations focused on the shallow aquifers of this region. The study site in this report is from an As-rich deep aquifer.
In this work on the deep aquifer material from the Chianan Plain, we aimed to (i) investigate the reductive dissolution of As(V) in relation to Fe(III) reduction, (ii) characterize the microbial redox cycling of Fe, Mn and S relevant to As mobilization. (iii) confirm the role of organic matter in fueling microbially mediated reductive dissolution of As-bearing minerals, and (iv) detect the shifts in the bacterial population with exogenously supplied carbon.
Section snippets
Collection and physicochemical analysis of sediment
The sampling site was located at Budai (23° 20′ 33.75″ N and 120° 10′ 25.24″ E) in Chianan Plain of southwestern (SW) Taiwan (Fig. S1, Supporting Information). The site has been documented as a severely As-enriched area, with groundwater As concentration exceeded 500 μg L−1 [15]. The lithology and hydrology of the site was presented by Jean et al. [19]. Sediment cores from Budai boreholes were sampled at depths up to150 m (10 piezometers from 15 to 150 m deep with approximately 15 m increment in
Sediment characteristics
The sediment samples were sandy (69%) in texture with high total As content (32.6 mg kg−1) and low total organic carbon (0.38%) content. Manganese and iron contents were typically high, whereas sulfur content was only 0.06% (Table 1). Results of sequential extraction analysis revealed that only a small (0.6%) fraction of As was present in ionically bound form (MG extract), whereas strongly adsorbed As (PHOS extract) accounted for 22.2% and As co-precipitated with carbonate, Mn oxides and
Sediment geochemistry and As mobility
The collected core sediment is characterized as circum-neutral pH and moderately reducing [24]. The sandy texture and low sulfate content of the sediment may prevent the aquifer from becoming very reducing [24], [28]. As a major fraction of the As (51.5%) in sediment is associated with recalcitrant solids (crystalline silicates), the dissolved As loads in groundwater may only represent small fraction of total As present in the sediment [21]. The reactivity of this aquifer sediment to microbial
Conclusions
Based on our study, we could conclude that As reduction was independent of Fe reduction and a modest rate of sedimentary As release into aqueous phase occurred at the expense of the native low organic carbon in the deep aquifer of Budai, SW Taiwan. This is consistent with observations from aquifers with low organic matter at other widespread locations. An important prerequisite for reduction and enhanced mobilization of As in this deep aquifer is a moderate to strongly reducing redox potential,
Acknowledgements
This work was supported by the National Science Council of Taiwan (NSC 100-2116-M-006-009). Due appreciation is given to Prof. Hsing-I Hsiang, Department of Resource Engineering, NCKU for helping with the analysis of XRD and XRF data. We thank the Molecular Medicine Core Lab, Research Center of Clinical Medicine, National Cheng Kung University for providing services in 454 GS Junior Next Generation Sequencing.
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