Microbial Community Structure and Arsenic Biogeochemistry in Two Arsenic-Impacted Aquifers in Bangladesh

Abstract

Long-term exposure to trace levels of arsenic (As) in shallow groundwater used for drinking and irrigation puts millions of people at risk of chronic disease. Although microbial processes are implicated in mobilizing arsenic from aquifer sediments into groundwater, the precise mechanism remains ambiguous. The goal of this work was to target, for the first time, a comprehensive suite of state-of-the-art molecular techniques in order to better constrain the relationship between indigenous microbial communities and the iron and arsenic mineral phases present in sediments at two well-characterized arsenic-impacted aquifers in Bangladesh. At both sites, arsenate [As(V)] was the major species of As present in sediments at depths with low aqueous As concentrations, while most sediment As was arsenite [As(III)] at depths with elevated aqueous As concentrations. This is consistent with a role for the microbial As(V) reduction in mobilizing arsenic. 16S rRNA gene analysis indicates that the arsenic-rich sediments were colonized by diverse bacterial communities implicated in both dissimilatory Fe(III) and As(V) reduction, while the correlation analyses involved phylogenetic groups not normally associated with As mobilization. Findings suggest that direct As redox transformations are central to arsenic fate and transport and that there is a residual reactive pool of both As(V) and Fe(III) in deeper sediments that could be released by microbial respiration in response to hydrologic perturbation, such as increased groundwater pumping that introduces reactive organic carbon to depth.IMPORTANCE The consumption of arsenic in waters collected from tube wells threatens the lives of millions worldwide and is particularly acute in the floodplains and deltas of southern Asia. The cause of arsenic mobilization from natural sediments within these aquifers to groundwater is complex, with recent studies suggesting that sediment-dwelling microorganisms may be the cause. In the absence of oxygen at depth, specialist bacteria are thought able to use metals within the sediments to support their metabolism. Via these processes, arsenic-contaminated iron minerals are transformed, resulting in the release of arsenic into the aquifer waters. Focusing on a field site in Bangladesh, a comprehensive, multidisciplinary study using state-of-the-art geological and microbiological techniques has helped better understand the microbes that are present naturally in a high-arsenic aquifer and how they may transform the chemistry of the sediment to potentially lethal effect.

Keywords: arsenic; biogeochemistry; geomicrobiology; metagenomics.

FIG 1

Chemical and microbial ecology analysis of sediments and water from the site F aquifer. (A) Sediment (Sed) arsenic and iron concentration and reflectance curve (blue, red, and green) along the sediment depths with the presence of dissimilatory arsenic-respiring bacteria (brown) and iron-reducing members of the Geobacteraceae (lines). (B) As(V), As(III), and AS₂S₃ species in the sediment (XANES) at site F. (C) Arsenic X-ray absorption near the edge structure (XANES) spectra along various depths of sediments. (D) Fraction of the Fe phases in relation to the Fe minerals along various depths. (E) As, Fe concentration (blue and green) in wells (aqueous phase), and groundwater tritium age (red). (F) 16S rRNA gene analysis for the microbial communities. Bar diagrams indicate the percentage of each class of the bacterial kingdom.

FIG 2

Chemical and microbial ecology analysis of sediments and water from the site B aquifers. (A) Sediment (Sed) arsenic and iron concentration and reflectance curve (blue, red, and green) along the sediment depths with the presence of dissimilatory arsenic-reducing bacteria (brown) and iron-reducing members of the Geobacteraceae (lines). (B) As(V), As(III), and AS₂S₃ species in the sediment (XANES) at site B. (C) Arsenic X-ray absorption near the edge structure (XANES) spectra along various depths of sediments. (D) Fraction of Fe phases in relation to the Fe minerals along various depths. (E) As, Fe concentration (blue and green) in wells (aqueous phase), and groundwater tritium age (red). (F) 16S rRNA gene analysis for the microbial communities. The bar diagram indicates the percentage of each class of the bacterial kingdom.

FIG 3

Top Spearman rank correlation (P = 0.01) plots relating microbial communities to mineral species. (A, D, and G) As(III) correlation with the microbial communities at site B, site F, and at combined sites. (B, E, and H) Fe(III) correlation with the microbial communities at site B, site F, and at combined sites. (C, F, and I) Aqueous As correlation with the microbial communities.