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Bacterial resistance to arsenic protects against protist killing

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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.

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References

  • Acland A, Agarwala R, Barrett T, Beck J, Benson DA, Bollin C et al (2014) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 42:D7

    Article  CAS  Google Scholar 

  • Amaro F, Wang W, Gilbert JA, Anderson OR, Shuman HA (2015) Diverse protist grazers select for virulence-related traits in Legionella. ISME J 9:1607–1618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi Fru E, Arvestål E, Callac N, El Albani A, Kilias S, Argyraki A et al (2015) Arsenic stress after the Proterozoic glaciations. Sci Rep 5:17789

    Article  CAS  PubMed Central  Google Scholar 

  • Chi Fru E, Rodriguez NP, Partin CA, Lalonde SV, Andersson P, Weiss DJ et al (2016) Cu isotopes in marine black shales record the Great Oxidation Event. Proc Natl Acad Sci USA 113:4941–4946

    Article  PubMed  PubMed Central  Google Scholar 

  • Cosson P, Soldati T (2008) Eat, kill or die: when amoeba meets bacteria. Curr Opin Microbiol 11:271–276

    Article  CAS  PubMed  Google Scholar 

  • Eppinger M, Radnedge L, Andersen G, Vietri N, Severson G, Mou S et al (2012) Novel plasmids and resistance phenotypes in Yersinia pestis: unique plasmid inventory of strain Java 9 mediates high levels of arsenic resistance. PLoS ONE 7:e32911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • German N, Doyscher D, Rensing C (2013) Bacterial killing in macrophages and amoeba: Do they all use a brass dagger? Future Microbiol 8:1257–1264

    Article  CAS  PubMed  Google Scholar 

  • Hao X, Luthje FL, Qin Y, McDevitt SF, Lutay N, Hobman JL et al (2015) Survival in amoeba—a major selection pressure on the presence of bacterial copper and zinc resistance determinants? Identification of a “copper pathogenicity island”. Appl Microbiol Biotechnol 99:5817–5824

    Article  CAS  PubMed  Google Scholar 

  • Hao X, Luthje F, Ronn R, German NA, Li X, Huang F et al (2016) A role for copper in protozoan grazing—two billion years selecting for bacterial copper resistance. Mol Microbiol 102:628–641

    Article  CAS  PubMed  Google Scholar 

  • Kapetanovic R, Bokil NJ, Achard ME, Ong CL, Peters KM, Stocks CJ et al (2016) Salmonella employs multiple mechanisms to subvert the TLR-inducible zinc-mediated antimicrobial response of human macrophages. FASEB J Off Publ Feder Am Soc Exp Biol 30:1901–1912

    CAS  Google Scholar 

  • Metchnikoff E (1887) Sur la lutte des cellules de l’organisme contre l’invasion des microbes. Ann Inst Pasteur 1:321–336

    Google Scholar 

  • Neyt C, Iriarte M, Thi VH, Cornelis GR (1997) Virulence and arsenic resistance in Yersiniae. J Bacteriol 179:612–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pal C, Bengtsson-Palme J, Rensing C, Kristiansson E, Larsson DG (2014) BacMet: antibacterial biocide and metal resistance genes database. Nucleic Acids Res 42:D737–D743

    Article  CAS  PubMed  Google Scholar 

  • Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DG (2015) Co-occurrence of resistance genes to antibiotics, biocides and metals reveals novel insights into their co-selection potential. BMC Genomics 16:964

    Article  PubMed  PubMed Central  Google Scholar 

  • Pal C, Bengtsson-Palme J, Kristiansson E, Larsson DG (2016) The structure and diversity of human, animal and environmental resistomes. Microbiome 4:54

    Article  PubMed  PubMed Central  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D et al (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tosetti F (2014) On arsenic and plague. Clin Infect Dis Off Publ Infect Dis Soc Am 59:1806–1808

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This Project was financially supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020402, XDB15020302), the International Postdoctoral Exchange Fellowship Program (No. 20150079), the Swedish Research Council for Environment, Agriculture and Spatial Planning (FORMAS), and the Centre for Sea and Society at University of Gothenburg. BPR was supported by National Institutes of Health Grants GM55425 and ES023779. Authors would like to thank Twasol Research Excellence Program (TRE Program), King Saud University, Saudi Arabia for support.

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    Authors and Affiliations

    1. Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, 361021, China

      Xiuli Hao, Yong-Guan Zhu & Christopher Rensing

    2. Department of Biology, University of Copenhagen, Copenhagen, Denmark

      Xuanji Li

    3. Department of Infectious Diseases, Institute for Biomedicine, Sahlgrenska Academy, University of Gothenburg, Göteborg, Sweden

      Chandan Pal & D. G. Joakim Larsson

    4. Center for Antibiotic Resistance Research (CARe) at the University of Gothenburg, Göteborg, Sweden

      Chandan Pal & D. G. Joakim Larsson

    5. School of Biosciences, The University of Nottingham, Sutton Bonington Campus, Sutton Bonington, Leicestershire, LE12 5RD, UK

      Jon Hobman

    6. Zoology Department, College of Science, King Saud University, Riyadh, Saudi Arabia

      Quaiser Saquib

    7. A.R. Al-Jeraisy Chair for DNA Research, Zoology Department, College of Science, King Saud University, Riyadh, Saudi Arabia

      Quaiser Saquib

    8. Botany & Microbiology Department, College of Science, King Saud University, Riyadh, Saudi Arabia

      Hend A. Alwathnani

    9. Herbert Wertheim College of Medicine, Florida International University, Miami, FL, USA

      Barry P. Rosen

    10. J. Craig Venter Institute, San Diego, CA, USA

      Christopher Rensing

    11. Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China

      Christopher Rensing

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    1. Xiuli Hao
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    Correspondence to Yong-Guan Zhu or Christopher Rensing.

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    The authors declare no conflict of interest.

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    Xiuli Hao, Xuanji Li and Chandan Pal have contributed equally.

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    Hao, X., Li, X., Pal, C. et al. Bacterial resistance to arsenic protects against protist killing. Biometals 30, 307–311 (2017). https://doi.org/10.1007/s10534-017-0003-4

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