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Magnetic ionic liquids: interactions with bacterial cells, behavior in aqueous suspension, and broader applications

Abstract

Previously, we demonstrated capture and concentration of Salmonella enterica subspecies enterica ser. Typhimurium using magnetic ionic liquids (MILs), followed by rapid isothermal detection of captured cells via recombinase polymerase amplification (RPA). Here, we report work intended to explore the broader potential of MILs as novel pre-analytical capture reagents in food safety and related applications. Specifically, we evaluated the capacity of the ([P66614+][Ni(hfacac)3]) (“Ni(II)”) MIL to bind a wider range of human pathogens using a panel of Salmonella and Escherichia coli O157:H7 isolates, including a “deep rough” strain of S. Minnesota. We extended this exploration further to include other members of the family Enterobacteriaceae of food safety and clinical or agricultural significance. Both the Ni(II) MIL and the ([P66614+][Dy(hfacac)4]) (“Dy(III)”) MIL were evaluated for their effects on cell viability and structure-function relationships behind observed antimicrobial activities of the Dy(III) MIL were determined. Next, we used flow imaging microscopy (FIM) of Ni(II) MIL dispersions made in model liquid media to examine the impact of increasing ionic complexity on MIL droplet properties as a first step towards understanding the impact of suspension medium properties on MIL dispersion behavior. Finally, we used FIM to examine interactions between the Ni(II) MIL and Serratia marcescens, providing insights into how the MIL may act to capture and concentrate Gram-negative bacteria in aqueous samples, including food suspensions. Together, our results provide further characterization of bacteria-MIL interactions and support the broader utility of the Ni(II) MIL as a cell-friendly capture reagent for sample preparation prior to cultural or molecular analyses.

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References

  1. 1.

    Octavia S, Lan R. The Family Enterobacteriaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, editors. The Prokaryotes: Gammaproteobacteria. 4th ed. Berlin: Spring-Verlag; 2014. p. 225–86.

    Google Scholar 

  2. 2.

    Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis. 2011;17(1):7–15.

    Article  Google Scholar 

  3. 3.

    Hoffman S, Maculloch B, Batz M. Economic burden of major foodborne illnesses acquired in the United States. Current Politics and Economics of the United States, Canada and Mexico. 2015;17(4).

  4. 4.

    Brehm-Stecher B, Young C, Jaykus LA, Tortorello ML. Sample preparation: the forgotten beginning. J Food Prot. 2009;72(8):1774–89.

    CAS  Article  Google Scholar 

  5. 5.

    Bisha B, Brehm-Stecher BF. Simple adhesive-tape-based sampling of tomato surfaces combined with rapid fluorescence in situ hybridization for Salmonella detection. Appl Environ Microbiol. 2009;75(5):1450–5.

    CAS  Article  Google Scholar 

  6. 6.

    Weber C, Stephan R, Druggan P, Joosten H, Iversen C. Improving the enrichment procedure for Enterobacteriaceae detection. Food Microbiol. 2009;26(6):565–72.

    CAS  Article  Google Scholar 

  7. 7.

    Soo HS, Brehm-Stecher BF, Jaykus LA. In: Sofos J, editor. Advances in separation and concentration of microorganisms from food samples. Cambridge: Woodhead Publishing; 2013. p. 173–92.

    Google Scholar 

  8. 8.

    Hice SA, Clark KD, Anderson JL, Brehm-Stecher BF. Capture, concentration, and detection of Salmonella in foods using magnetic ionic liquids and Recombinase polymerase amplification. Anal Chem. 2019;91(1):1113–20.

    CAS  Article  Google Scholar 

  9. 9.

    Clark KD, Purslow JA, Pierson SA, Nacham O, Anderson JL. Rapid preconcentration of viable bacteria using magnetic ionic liquids for PCR amplification and culture-based diagnostics. Anal Bioanal Chem. 2017;409(21):4983–91.

    CAS  Article  Google Scholar 

  10. 10.

    Clark KD, Nacham O, Purslow JA, Pierson SA, Anderson JL. Magnetic ionic liquids in analytical chemistry: a review. Anal Chim Acta. 2016;934:9–21.

    CAS  Article  Google Scholar 

  11. 11.

    Clark KD, Varona M, Anderson JL. Ion-tagged oligonucleotides coupled with a magnetic liquid support for the sequence-specific capture of DNA. Angew Chem Int Ed Engl. 2017;56(26):7630–3.

    CAS  Article  Google Scholar 

  12. 12.

    Ding X, Clark KD, Varona M, Emaus MN, Anderson JL. Magnetic ionic liquid-enhanced isothermal nucleic acid amplification and its application to rapid visual DNA analysis. Anal Chim Acta. 2019;1045:132–40.

    CAS  Article  Google Scholar 

  13. 13.

    Merib J, Spudeit DA, Corazza G, Carasek E, Anderson JL. Magnetic ionic liquids as versatile extraction phases for the rapid determination of estrogens in human urine by dispersive liquid-liquid microextraction coupled with high-performance liquid chromatography-diode array detection. Anal Bioanal Chem. 2018;410(19):4689–99.

    CAS  Article  Google Scholar 

  14. 14.

    Mester P, Wagner M, Rossmanith P. Use of ionic liquid-based extraction for recovery of Salmonella Typhimurium and Listeria monocytogenes from food matrices. J Food Prot. 2010;73(4):680–7.

    Article  Google Scholar 

  15. 15.

    Pierson SA, Nacham O, Clark KD, Nan H, Mudryk Y, Anderson JL. Synthesis and characterization of low viscosity hexafluoroacetylacetonate-based hydrophobic magnetic ionic liquids. New J Chem. 2017;41(13):5498–505.

    CAS  Article  Google Scholar 

  16. 16.

    Jett BD, Hatter KL, Huycke MM, Gilmore MS. Simplified agar plate method for quantifying viable bacteria. Biotechniques. 1997;23(4):648–50.

    CAS  Article  Google Scholar 

  17. 17.

    Nikaido H. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev. 2003;67(4):593–656.

    CAS  Article  Google Scholar 

  18. 18.

    Liao CH, Fett WF. Resuscitation of acid-injured Salmonella in enrichment broth, in apple juice and on the surfaces of fresh-cut cucumber and apple. Lett Appl Microbiol. 2005;41(6):487–92.

    Article  Google Scholar 

  19. 19.

    Tecon R, Leveau JH. Symplasmata are a clonal, conditional, and reversible type of bacterial multicellularity. Sci Rep. 2016;6:31914.

    CAS  Article  Google Scholar 

  20. 20.

    CDC. Outbreak of E. coli infections linked to Romaine lettuce. 2019. Available from: https://www.cdc.gov/ecoli/2019/o157h7-11-19/index.html. Accessed 7 Dec 2019

  21. 21.

    CDC. Antibiotic Resistance Threats in the United States, 2019. In: U.S. Department of Health and Human Services C, editor. Atlanta, GA; 2019.

  22. 22.

    Walterson AM, Stavrinides J. Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiol Rev. 2015;39(6):968–84.

    CAS  Article  Google Scholar 

  23. 23.

    Mitchell AM, Srikumar T, Silhavy TJ. Cyclic Enterobacterial Common Antigen Maintains the Outer Membrane Permeability Barrier of Escherichia coli in a Manner Controlled by YhdP. MBio. 2018;9(4).

  24. 24.

    Kalynych S, Morona R, Cygler M. Progress in understanding the assembly process of bacterial O-antigen. FEMS Microbiol Rev. 2014;38(5):1048–65.

    CAS  Article  Google Scholar 

  25. 25.

    Grimont PAD, Weill F-X. Antigenic Formulae of the Salmonella Serovars. WHO Collaborating Center for Reference and Research on Salmonella, Institut Pasteur, Paris, France. 9th ed. 2007.

  26. 26.

    Rosenberg M. Microbial adhesion to hydrocarbons: twenty-five years of doing MATH. FEMS Microbiol Lett. 2006;262(2):129–34.

    CAS  Article  Google Scholar 

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Acknowledgments

BFBS acknowledges financial support from the Midwest Dairy Association (MDA) and Iowa Agriculture and Home Economics Experiment Station Project No. IOW03902, sponsored by Hatch Act and State of Iowa funds. JLA acknowledges funding from the Chemical Measurement and Imaging Program at the National Science Foundation (CHE-1709372). We thank Dr. Gwynn Beattie, Iowa State University Department of Plant Pathology, for supervision of work with plant pathogens and Fluid Imaging Technologies, Inc., for collecting data on MIL droplets and VisualSpreadsheet® analysis advice.

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Correspondence to Byron F. Brehm-Stecher.

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Hice, S.A., Varona, M., Brost, A. et al. Magnetic ionic liquids: interactions with bacterial cells, behavior in aqueous suspension, and broader applications. Anal Bioanal Chem 412, 1741–1755 (2020). https://doi.org/10.1007/s00216-020-02457-3

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Keywords

  • Magnetic ionic liquids
  • Cell capture
  • Cell concentration
  • Gram-negative bacteria
  • Enterobacteriaceae
  • Flow imaging microscopy