Metagenomic and culture-dependent approaches unveil active microbial community and novel functional genes involved in arsenic mobilization and detoxification in groundwater

Farzana Diba; M Nazmul Hoque; M Shaminur Rahman; Farhana Haque; Khondaker Md Jaminur Rahman; Md Moniruzzaman; Mala Khan; M Anwar Hossain; Munawar Sultana

doi:10.1186/s12866-023-02980-0

Metagenomic and culture-dependent approaches unveil active microbial community and novel functional genes involved in arsenic mobilization and detoxification in groundwater

BMC Microbiol. 2023 Aug 30;23(1):241. doi: 10.1186/s12866-023-02980-0.

Authors

Farzana Diba^{1

2}, M Nazmul Hoque³, M Shaminur Rahman⁴, Farhana Haque¹, Khondaker Md Jaminur Rahman⁵, Md Moniruzzaman⁶, Mala Khan⁶, M Anwar Hossain^{1

7}, Munawar Sultana⁸

Affiliations

¹ Department of Microbiology, University of Dhaka, Dhaka, 1000, Bangladesh.
² Institute of Tissue Banking and Biomaterial Research, Atomic Energy Research Establishment, Savar, Dhaka, 1349, Bangladesh.
³ Department of Gynecology, Obstetrics and Reproductive Health, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, 1706, Bangladesh.
⁴ Department of Microbiology, Jashore University of Science and Technology, Jashore, 7408, Bangladesh.
⁵ Environmental Science Division, National Institute of Biotechnology, Savar, Dhaka, 1349, Bangladesh.
⁶ Bangladesh Reference Institute for Chemical Measurements (BRiCM), Dr. Qudrat-E-Khuda Road, Dhanmondi, Dhaka, 1205, Bangladesh.
⁷ Present address: Jashore University of Science and Technology, Jashore, 7408, Bangladesh.
⁸ Department of Microbiology, University of Dhaka, Dhaka, 1000, Bangladesh. munawar@du.ac.bd.

Abstract

Background: Arsenic (As) and its species are major pollutants in ecological bodied including groundwater in Bangladesh rendering serious public health concern. Bacteria with arsenotrophic genes have been found in the aquifer, converting toxic arsenite [As (III)] to less toxic arsenate [As (V)] that is easily removed using chemical and biological trappers. In this study, genomic and metagenomic approaches parallel to culture-based assay (Graphical abstract) have made it possible to decipher phylogenetic diversity of groundwater arsenotrophic microbiomes along with elucidation of their genetic determinants.

Results: Seventy-two isolates were retrieved from six As-contaminated (average As concentration of 0.23 mg/L) groundwater samples from Munshiganj and Chandpur districts of Bangladesh. Twenty-three isolates harbored arsenite efflux pump (arsB) gene with high abundance, and ten isolates possessing arsenite oxidase (aioA) gene, with a wide range of minimum inhibitory concentration, MIC_As (2 to 32 mM), confirming their role in arsenite metabolism. There was considerable heterogeneity in species richness and microbial community structure. Microbial taxa from Proteobacteria, Firmicutes and Acidobacteria dominated these diversities. Through these combinatorial approaches, we have identified potential candidates such as, Pseudomonas, Acinetobacter, Stenotrophomonas, Achromobacter, Paraburkholderia, Comamonas and Klebsiella and associated functional genes (arsB, acr3, arsD, arsH, arsR) that could significantly contribute to arsenite detoxification, accumulation, and immobilization.

Conclusions: Culture-dependent and -independent shotgun metagenomic investigation elucidated arsenotrophic microbiomes and their functions in As biogeochemical transformation. These findings laid a foundation for further large-scale researches on the arsenotrophic microbiomes and their concurrent functions in As biogeochemical transformation in As-contaminated areas of Bangladesh and beyond.

Keywords: AMRs; Arsenotrophic bacteria; Arsenotrophic genes; Bioremediation; VFGs; Whole-genome shotgun sequencing.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Arsenic*
Arsenites*
Microbiota*
Phylogeny

Substances

Arsenic
arsenite
Arsenites