Bacterial resistance to arsenic protects against protist killing

Abstract

Protists kill their bacterial prey using toxic metals such as copper. Here we hypothesize that the metalloid arsenic has a similar role. To test this hypothesis, we examined intracellular survival of Escherichia coli (E. coli) in the amoeba Dictyostelium discoideum (D. discoideum). Deletion of the E. coli ars operon led to significantly lower intracellular survival compared to wild type E. coli. This suggests that protists use arsenic to poison bacterial cells in the phagosome, similar to their use of copper. In response to copper and arsenic poisoning by protists, there is selection for acquisition of arsenic and copper resistance genes in the bacterial prey to avoid killing. In agreement with this hypothesis, both copper and arsenic resistance determinants are widespread in many bacterial taxa and environments, and they are often found together on plasmids. A role for heavy metals and arsenic in the ancient predator–prey relationship between protists and bacteria could explain the widespread presence of metal resistance determinants in pristine environments.

Distribution of Arsenic Resistance Genes in Prokaryotes

“…Plasmid PNJST258N1 (143Kb) contains a 20-gene cluster “copper pathogenicity island” that probably aids in survival in macrophages ( Hao et al, 2015 ) and an ars gene cluster also containing arsH which might aid in survival in NK cells. Survival in amoeba was enhanced by the presence of an arsRBC operon in E. coli ( Hao et al, 2017 ). Perhaps this is also true in macrophages.…”

Tolerance to arsenic contaminant among multidrug‐resistant and copper‐tolerant Salmonella successful clones is associated with diverse ars operons and genetic contexts

“…Contrasting with isolates carrying only acr3 genes, those with arsBI/II-type cluster presented highest MIC values in both atmospheres, suggesting a more prominent role of this ars operon for the survival in high arseniccontaminated environments and with different oxygen levels (Tóth et al, 2016;Cui et al, 2017). Also, it was recently demonstrated that arsRBC operon is also crucial to avoid killing by a soil amoeba (Hao et al, 2017), a protozoan that was shown to have a fundamental role for Salmonella Typhimurium survival in the environment (Bleasdale et al, 2009). The WGS analysis of ars operon environments allowed to observe that S. Typhimurium and S. 4,[5],12:i:-carried two arsA and arsD genes (arsD1A1CBA2D2R) in contrast with acr3-type operon in S. Rissen (acr3arsADCR).…”

Whole genome analysis and characterization of Salmonella enterica subsp. enterica serovar Typhimurium strain UPM 260 for mediated genetic manipulation

“…Furthermore, the industrial revolution also contributed to the rapid increase in metal production in the environment. Likewise, the presence of metal resistance genes (MRGs) in bacteria was also premediated by protist predation, in which they exploited metal poisoning to inactivate and kill bacteria (Hao et al, 2017). As a result, bacteria had evolved a new detoxification strategy against metal in order to avoid lethality by protists.…”