Distribution of Arsenic Resistance Genes in Prokaryotes Original paper

What was reviewed?

This comprehensive review examined the distribution, diversity, and genetic organization of arsenic resistance genes in prokaryotes, with a particular focus on the microbiome’s role in arsenic detoxification and biogeochemical cycling. The authors detailed the evolutionary history, molecular mechanisms, and dissemination of arsenic resistance determinants across bacteria and archaea. The review also explored recent advances in understanding microbial resistance to both inorganic and organic arsenic compounds, including novel efflux systems and enzymatic pathways. Key topics included the structure and redundancy of arsenic resistance genes, horizontal gene transfer, adaptive responses in contaminated environments, and the significance of these systems in the context of environmental and public health.

Who was reviewed?

The review encompassed a wide range of prokaryotic organisms, including diverse bacterial and archaeal lineages from environmental, clinical, and industrial settings. It synthesized evidence from studies on model organisms such as Escherichia coli, Staphylococcus aureus, Bacillus subtilis, Pseudomonas aeruginosa, and extremophiles like Halobacterium sp. and Ferroplasma acidarmanus. The analysis drew on data from both cultured isolates and metagenomic studies, covering prokaryotes found in arsenic-contaminated soils, groundwater, mine tailings, animal microbiomes (e.g., gut bacteria), and pristine environments presumed to be arsenic-free. The microbial populations reviewed ranged from those with minimal genetic resistance determinants to those harboring complex, redundant, and horizontally transferred arsenic resistance gene clusters.

Most important findings

The review identified that nearly all prokaryotes possess some form of arsenic resistance genes, reflecting ancient and ongoing selective pressures. The canonical ars operon, typically consisting of arsR (regulator), arsB (arsenite efflux pump), and arsC (arsenate reductase), is ubiquitous and often found on chromosomes, plasmids, transposons, and genomic islands, facilitating horizontal gene transfer and rapid adaptation. Variations and redundancies in ars operon structure are common, with some microbes harboring multiple operons that are differentially expressed depending on environmental conditions, such as arsenic concentration and temperature. The review also highlighted the evolution of additional resistance genes, including acr3 (an alternative arsenite efflux transporter), aqpS (aquaglyceroporin-based transport), mfs (major facilitator superfamily), and genes conferring resistance to organic arsenicals—arsM (arsenic methyltransferase), arsH (organoarsenical oxidase), arsP (organoarsenical efflux permease), and arsI (C-As bond lyase). These broaden the resistance spectrum and demonstrate convergent evolutionary solutions to arsenic toxicity.

The presence of these genes in pathogenic bacteria (e.g., Klebsiella pneumoniae, Yersinia spp., Campylobacter jejuni) and in environmental bacteria from highly contaminated sites underscores their role in both environmental adaptation and potential clinical relevance. Notably, the review recognized that efflux mechanisms, primarily via ArsB, Acr3, ArsP, and associated ATPases, are central to prokaryotic arsenic resistance. Furthermore, the review discussed the impact of microbial methylation and demethylation of arsenic on the global geocycle, influencing arsenic toxicity, mobility, and exposure risks to humans and animals. Metagenomic surveys revealed a remarkable diversity of arsenic resistance genes, with certain gene clusters (e.g., arsP for organoarsenicals) being particularly widespread.

Key implications

The widespread and diverse nature of arsenic resistance genes in prokaryotes has significant implications for environmental microbiology, clinical practice, and public health. Microbial arsenic resistance is a key driver of the global arsenic geocycle, influencing arsenic mobility, bioavailability, and toxicity in various ecosystems, including those affecting human water and food supplies. The detection of arsenic resistance determinants in both environmental and pathogenic bacteria raises concerns about the potential for horizontal gene transfer, which could enhance the survival and virulence of clinically relevant microbes in arsenic-rich environments. For microbiome research and clinical translation, understanding the prevalence and function of these resistance genes is essential for developing microbial signatures for risk assessment, bioremediation strategies, and monitoring the spread of resistance traits. The review also points to the evolutionary arms race between arsenic as an environmental toxin and microbial adaptation, emphasizing the need for continued surveillance of resistance gene dissemination and functional diversity in both environmental and host-associated microbiomes.