Diversity, metabolic properties and arsenic mobilization potential of indigenous bacteria in arsenic contaminated groundwater of West Bengal, India

• Published in: PloS one 2015-03, Vol.10 (3), p.e0118735-e0118735
• Main Authors: Paul, Dhiraj, Kazy, Sufia K, Gupta, Ashok K, Pal, Taraknath, Sar, Pinaki
• Format: Article
• Language: English
• Subjects: Acid production; Acids; Alluvial aquifers; Aluminum; Analysis; Aquifers; Arsenic; Arsenic - chemistry; Arsenic - metabolism; Arsenic ions; Bacteria; Bacteria - classification; Bacteria - genetics; Bacteria - metabolism; Bacterial Proteins - genetics; Biogeochemistry; Biotechnology; Carbon; Carbon - chemistry; Carbon - metabolism; Carbon sources; Cascade chemical reactions; Communities; Community composition; Detoxification; Drinking water; Efflux; Essential nutrients; Genetic Variation; Groundwater; Groundwater - chemistry; Groundwater - microbiology; Groundwater pollution; Hydrocarbons; India; Inland water pollution; Iron; Manganese; Metabolism; Metals - chemistry; Metals - metabolism; Microcosms; Mineralogy; Minerals; Nutrients; Organic carbon; Oxalic acid; Phylogeny; Pleistocene; Polyaromatic hydrocarbons; Polycyclic aromatic hydrocarbons; Polymerase Chain Reaction; Reductase; Rhodococcus; RNA, Bacterial - genetics; RNA, Ribosomal, 16S - genetics; Sand; Sediment composition; Sediments; Studies; Substrates; Trends; Water Pollutants - metabolism
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0118735

Arsenic (As) mobilization in alluvial aquifers is caused by a complex interplay of hydro-geo-microbiological activities. Nevertheless, diversity and biogeochemical significance of indigenous bacteria in Bengal Delta Plain are not well documented. We have deciphered bacterial community compositions and metabolic properties in As contaminated groundwater of West Bengal to define their role in As mobilization. Groundwater samples showed characteristic high As, low organic carbon and reducing property. Culture-independent and -dependent analyses revealed presence of diverse, yet near consistent community composition mostly represented by genera Pseudomonas, Flavobacterium, Brevundimonas, Polaromonas, Rhodococcus, Methyloversatilis and Methylotenera. Along with As-resistance and -reductase activities, abilities to metabolize a wide range carbon substrates including long chain and polyaromatic hydrocarbons and HCO3, As3+ as electron donor and As5+/Fe3+ as terminal electron acceptor during anaerobic growth were frequently observed within the cultivable bacteria. Genes encoding cytosolic As5+ reductase (arsC) and As3+ efflux/transporter [arsB and acr3(2)] were found to be more abundant than the dissimilatory As5+ reductase gene arrA. The observed metabolic characteristics showed a good agreement with the same derived from phylogenetic lineages of constituent populations. Selected bacterial strains incubated anaerobically over 300 days using natural orange sand of Pleistocene aquifer showed release of soluble As mostly as As3+ along with several other elements (Al, Fe, Mn, K, etc.). Together with the production of oxalic acid within the biotic microcosms, change in sediment composition and mineralogy indicated dissolution of orange sand coupled with As/Fe reduction. Presence of arsC gene, As5+ reductase activity and oxalic acid production by the bacteria were found to be closely related to their ability to mobilize sediment bound As. Overall observations suggest that indigenous bacteria in oligotrophic groundwater possess adequate catabolic ability to mobilize As by a cascade of reactions, mostly linked to bacterial necessity for essential nutrients and detoxification.