Elsevier

Journal of Hydrology

Volume 527, August 2015, Pages 221-233
Journal of Hydrology

Characterization and microbial utilization of dissolved lipid organic fraction in arsenic impacted aquifers (India)

https://doi.org/10.1016/j.jhydrol.2015.04.051Get rights and content

Highlights

  • Dissolved organic carbon (DOC) profiles in arsenic contaminated aquifers.

  • DOC consists of terrestrial and predominantly bacterial derived organic matter sources.

  • Occurrence of petroleum derived organic matter in grey sand aquifers.

  • Grey sands have arsenite oxidizing petroleum degrading bacteria.

  • Greater utilization of DOC by indigenous bacteria involved in As cycling in grey sands (than brown sands).

Summary

The coupled role of organic matter (OM) and microbial activity is widely acknowledged in arsenic (As) biogeochemical cycling in sedimentary environments. However, little is known about OM characteristics particularly the dissolved fraction in the Bengal Delta Plain aquifers – one of the worst As impacted regions in the world. Ongoing investigations in As-rich aquifers in Nadia district (West Bengal, India) indicate presence of arsenite {As(III)} oxidizing bacterial communities in the Grey Sand Aquifers (GSA), but absent in Brown Sand Aquifers (BSA). In this study, we investigate the key differences in dissolved organic carbon (DOC) characteristics and its relationship with differences in elemental concentrations, distribution of biomarkers, and utilization of DOC by in situ microbial communities in BSA and GSA. We demonstrate a new approach using ENVI™ C-18 DSK discs to pre-concentrate DOC from large volumes of water, and further extract the OM and separate it into different lipid fractions using the solid phase extraction technique. The aquifers show marked heterogeneity in terms of their DOC characteristics and elemental profiles irrespective of their grey or brown color. DOC indicates variable inputs of terrestrial derived OM sources, and OM derived from decomposition and/or microbial cellular components. DOC in the aquifers consist of predominantly n-alkanoic acids (∼80%) followed by n-alkanes and n-alcohols. The GSAs indicate high iron (Fe) and manganese (Mn) concentrations, and presence of mature petroleum derived hydrocarbons in DOC. BSA has comparatively lower concentrations of Fe and Mn, and shows absence of mature hydrocarbons in DOC. Experiments in presence of indigenous bacteria from groundwater with DOC lipid extracts as the sole carbon source indicate higher growth in the GSA samples implying preferential use of DOC. The potential availability of DOC in these aquifers can influence the community composition of indigenous heterotrophic microbial flora, which in turn can affect elemental cycles including that of As.

Introduction

Dissolved Organic Carbon (DOC) is considered the largest reservoir of reactive organic carbon in the biosphere (Amon and Benner, 1996). DOC provides electron donors, which impact redox conditions and transport of nutrients and/or diffusion of microbial exo-enzymes into the surrounding environment (Thurman, 1985, Metting, 1993, Marschner and Kalbitz, 2013). As a result, DOC affects sub-surface biogeochemical processes by controlling the survival of phylogenetically diverse microbial communities (Judd et al., 2006). Sedimentary organic matter (OM) in soil zone plays an important role in recharging the DOC pool in aquifers, and impacting biogeochemical cycling of different elements (Maldenov et al., 2010). Consistent with this, recent studies indicate that sedimentary OM impacts arsenic (As) contamination in the Bengal Delta Plain (BDP) aquifers of India and Bangladesh (McArthur et al., 2001, Harvey et al., 2002, Akai et al., 2004 Islam et al., 2004, Bauer and Blodau, 2006, Rowland et al., 2006). In particular, the extensive use of groundwater for agriculture, and recharge of labile OM into the sub-surface is suggested to accelerate biogeochemical interactions involving microbial release of As into shallow aquifers (Harvey et al., 2002; Akai et al., 2004). Studying groundwater DOC is however complex because its low concentration involves various pre-concentration methods involving large volumes of water (Routh et al., 2001a, Routh et al., 2001b, Simjouw et al., 2005). These methods are tedious and require special sampling and/or analytical capabilities. Moreover it remains unknown if microbes can actually use the DOC fraction in groundwater for respiration in BDP aquifers.

Previous studies in BDP aquifers suggest that DOC is transported as recharge from base of ponds, wetlands, and/or sub-surface clay/lignite deposits in aquifers (McArthur et al., 2004, Lawson et al., 2013). Hence, it is important to trace its source, chemical reactivity, and potential (bio)-availability in sustaining microbial reactions involved with As cycling in the sub-surface. The current study is part of ongoing investigations on tracing microbial communities and their role in geochemical processes associated with As cycling in aquifers in Nadia district (West Bengal). In order to understand the potential role of indigenous bacterial communities in controlling As and other elemental flux in groundwater, wells were screened and diversity of As(III) oxidizing bacteria were studied using the aioA gene as molecular marker in GSAs which were absent in BSA (Ghosh et al., 2014). The overall bacterial community studied in the GSA wells using 16S rRNA as a molecular marker showed predominance of As(III) oxidizing and As(V) reducing bacterial groups (Ghosh et al., 2014). In this study, we aim to: (1) assess the inorganic characteristics in groundwater, (2) identify diagnostic biomarker suites which contribute to the DOC lipid fractions, and (3) establish the capability of in situ microorganisms to utilize DOC for their growth. The data will be used to identify the potential role of DOC in sustaining/driving microbial processes associated with As cycling. To the best of our knowledge, this is the first study on DOC characteristics in BDP aquifers, which establishes utilization of dissolved lipids by bacteria involved in As cycling. A better understanding of factors controlling As cycling will provide knowledge toward implementing sustainable and long term cost-effective groundwater treatment methodologies.

Section snippets

Study area

The BDP aquifers dating back up to 18 ka BP have been stratigraphically divided into the Pleistocene and Holocene sedimentary deposits (Acharyya et al., 2000). The brown colored iron stained sandy aquifers referred to as the Brown Sand Aquifers (BSA) were deposited during early-mid Pleistocene (Acharyya et al., 2000, Goodbred and Kuehl, 2000). The grey colored micaceous sand bearing aquifers referred to as the Grey Sand Aquifers (GSA) were deposited later during the Holocene (Goodbred and Kuehl,

Groundwater sampling

The sampling locations were: (1) well 28 (N 23°55.064′, E 088°33.350′) and well 204 (N 23°56.352′, E 088°33.814′), which are GSAs located in Karimpur II Block, and (2) a BSA (well Haringhata; N 22°56.401′, E 088°32.389′) located in Haringhata Block in Nadia District, West Bengal (Fig. 1). Groundwater was collected from three pre-installed wells; a 150 m deep BSA well in Haringhata, and 50 m deep GSA wells in Karimpur II (wells 28 and 204; Fig. 1). A large volume of groundwater (roughly 3 times

DOC and total nitrogen analysis

Physical properties, DOC, and TN concentration in groundwater samples collected from the wells are summarized in Table 1. A circum-neutral pH (7.1–7.5) and narrow temperature range (28–29.2 °C) was measured in both types of aquifers. Dissolved oxygen level in the water was 1.2–2.1 mg/l. The DOC level in wells was < 10 mg/l (Table 1). The BSA well had higher dissolved inorganic carbon (DIC) than the GSA wells. Total nitrogen concentration in the wells ranged from 0.7 to 1.7 mg/l; in BSA well 204 the

Discussion

This study discusses inorganic and organic geochemical and microbial characteristics in the BSA and GSA wells in Nadia district. These sites were chosen to represent: (1) wells with high As concentrations, (2) microbial diversity, and (3) different sediment characteristics (GSA vs. BSA lithological and geochemical differences). DOC in these aquifers is derived from multiple sources, and the observed trends in this multi-proxy data imply association between geochemical and microbial processes,

Conclusions

This is the first study in BDP aquifers impacted by high As concentrations, where we characterize and report different lipid fractions in the DOC pool. Although the DOC pool is small it is reactive and readily available for microbial uptake. This study describes a handy procedure to extract and characterize the total lipid fractions in DOC, which can be applied in other aquatic environments in order to understand ongoing biogeochemical processes in the sub-surface. The BDP aquifers show

Acknowledgements

We acknowledge Dr. S.P. Sinha Ray for his suggestions and help. Apurba Mandal helped with drilling the wells. We are grateful to Debaprasad Parai, Tarkeshwar Singh, and Diya Sen for helping us with sample collection. We thank Mårten Dario and Lena Lundman for their assistance in the laboratory. DG acknowledge Department of Science and Technology, Government of India for providing the INSPIRE Ph.D. fellowship. The study was financed by the Swedish Research Link-Asia Program (Grant No

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