Geochemical, metagenomic, and physiological characterization of the multifaceted interaction between microbiome of an arsenic contaminated groundwater and aquifer sediment

Balaram Mohapatra^a,1, Anumeha Saha^a, Atalanta N. Chowdhury^b, Amlanjyoti Kar^b, Sufia K. Kazy^c, Pinaki Sar^a

Environmental Microbiology and Genomics Laboratory, Department of Biotechnology, Indian Institute of Technology Kharagpur, Kharagpur 721302, West Bengal, India.

Abstract

Geomicrobiological details of the interactions between groundwater microbiome (GWM) and arsenic (As)-rich aquifer sediment of Bengal basin was investigated through microcosm incubations. Role of key microorganisms and their specific interactions with As-bearing minerals was demarcated under organic carbon- amended and -unamended conditions. Acinetobacter (50.8 %), Brevundimonas (7.9 %), Sideroxydans (3.4 %), Alkanindiges (3.0 %) dominated the GWM. The microbiome catalysed considerable alterations in As-bearing mineral [Fe-(hydr)oxide and aluminosilicate] phases resulting in substantial changes in overall geochemistry and release of As (65 μg/L) and Fe (118 μg/L). Synergistic roles of autotrophic, NH₄^+-oxidizing Archaea (Thaumarchaeota) and chemoheterotrophic bacteria (Stenotrophomonas, Pseudomonas, Geobacter) of diverse metabolic abilities (NH₄^+-oxidizing, NO₄^-, As/Fe-reducing) were noted for observed changes. Organic carbon supported enhanced microbial growth and As mobilization (upto 403.2 μg As/L) from multiple mineral phases (hematite, magnetite, maghemite, biotite, etc.). In presence of high organic carbon, concerted actions of anaerobic, hydrocarbon-utilizing, As-, Fe-reducing Rhizobium, fermentative Escherichia, anaerobic Bacillales, metal-reducing and organic acid-utilizing Pseudomonas and Achromobacter were implicated in altering sediment mineralogy and biogeochemistry. Increase in abundance of arrA, arsC, bssA genes, and dissolution of Fe, Ca, Mg, Mn confirmed that dissimilatory-, cytosolic-As reduction, and mineral weathering fuelled by anaerobic (hydro)carbon metabolism are the predominant mechanisms of As release in aquifers of Bengal basin.

Keywords: Arsenic, Bengal basin, Groundwater microbiome, Aquifer sediment, Mineral-microbe interaction, Microbial community, Organic carbon, Taxa recruitment, Metabolic interplay.