Abstract
Bacteria are essential in arsenic cycling. However, few studies have addressed 16S rRNA and arsenic-related functional gene diversity in long-term arsenic-contaminated tropical sediment. Here, using culture-based, metagenomic and computational approaches, we describe the diversity of bacteria, genes and enzymes involved in AsIII and AsV transformation in freshwater sediment and in anaerobic AsIII- and AsV-enrichment cultures (ECs). The taxonomic profile reveals significant differences among the communities. Arcobacter, Dechloromonas, Sedimentibacter and Clostridium thermopalmarium were exclusively found in ECs, whereas Anaerobacillus was restricted to AsV-EC. Novel taxa that are both AsV-reducers and AsIII-oxidizers were identified: Dechloromonas, Acidovorax facilis, A. delafieldii, Aquabacterium, Shewanella, C. thermopalmarium and Macellibacteroides fermentans. Phylogenic discrepancies were revealed among the aioA, arsC and arrA genes and those of other species, indicating horizontal gene transfer. ArsC and AioA have sets of amino acids that can be used to assess their functional and structural integrity and familial subgroups. The positions required for AsV reduction are conserved, suggesting strong selective pressure for maintaining the functionality of ArsC. Altogether, these findings highlight the role of freshwater sediment bacteria in arsenic mobility, and the untapped diversity of dissimilatory arsenate-reducing and arsenate-resistant bacteria, which might contribute to arsenic toxicity in aquatic environments.
Highlights
Arsenic (As), a toxic metalloid, is naturally found in Earth’s crust and is recognized by the World Health Organization as one of the ten chemicals of major public health concern[1]
The arr operon is a respiratory system that leads to energy gain via dissimilatory reduction of AsV to AsIII in anaerobiosis; such microorganisms are referred to as dissimilatory arsenate-reducing prokaryotes (DARPs)[2]
Our group identified aerobic As-transforming bacterial isolates in Mina Stream’s sediment, and characterized the microbial community’s As-related genes through metagenomic analysis[16]. We have broadened those findings by combining molecular and computational approaches to obtain a comprehensive insight into anaerobic bacterial taxonomy and their arsenic-related genes and enzymes diversity, which are of special environmental concern
Summary
Arsenic (As), a toxic metalloid, is naturally found in Earth’s crust and is recognized by the World Health Organization as one of the ten chemicals of major public health concern[1]. As is widespread in the environment; there, bacteria play an important role in its biogeochemical cycling, directly taking part in As speciation or doing so indirectly through redox interactions with other metals and nutrients, e.g., iron and nitrogen[2] Such intricate ecological interactions remain to be investigated, in anaerobic conditions[3]. The asrC gene of the ars operon codes for an arsenate reductase protein that can be structurally diverse; in prokaryotes, the best-characterized family is that of the Escherichia coli R773 plasmid, which uses reduced glutathione (GSH) to convert AsV to AsIII and possesses a cysteine residue in the catalytic site[10]. Metagenomics provides comprehensive information about bacterial community structure, it does not yield direct evidence of the relationship between these organisms and the functions that they play in the environment, in contrast to culture-based techniques; using only these latter techniques cannot provide a broad picture of the structure, functionality and phylogeny of the proteins encoded by the genes under scrutiny
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