Mechanism of bacterial inactivation by (+)-limonene and its potential use in food preservation combined processes

PLoS One. 2013;8(2):e56769. doi: 10.1371/journal.pone.0056769. Epub 2013 Feb 12.

Abstract

This work explores the bactericidal effect of (+)-limonene, the major constituent of citrus fruits' essential oils, against E. coli. The degree of E. coli BJ4 inactivation achieved by (+)-limonene was influenced by the pH of the treatment medium, being more bactericidal at pH 4.0 than at pH 7.0. Deletion of rpoS and exposure to a sub-lethal heat or an acid shock did not modify E. coli BJ4 resistance to (+)-limonene. However, exposure to a sub-lethal cold shock decreased its resistance to (+)-limonene. Although no sub-lethal injury was detected in the cell envelopes after exposure to (+)-limonene by the selective-plating technique, the uptake of propidium iodide by inactivated E. coli BJ4 cells pointed out these structures as important targets in the mechanism of action. Attenuated Total Reflectance Infrared Microspectroscopy (ATR-IRMS) allowed identification of altered E. coli BJ4 structures after (+)-limonene treatments as a function of the treatment pH: β-sheet proteins at pH 4.0 and phosphodiester bonds at pH 7.0. The increased sensitivity to (+)-limonene observed at pH 4.0 in an E. coli MC4100 lptD4213 mutant with an increased outer membrane permeability along with the identification of altered β-sheet proteins by ATR-IRMS indicated the importance of this structure in the mechanism of action of (+)-limonene. The study of mechanism of inactivation by (+)-limonene led to the design of a synergistic combined process with heat for the inactivation of the pathogen E. coli O157:H7 in fruit juices. These results show the potential of (+)-limonene in food preservation, either acting alone or in combination with lethal heat treatments.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacterial Proteins / genetics
  • Beverages / microbiology
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Cell Membrane Permeability
  • Cyclohexenes / metabolism
  • Cyclohexenes / pharmacology*
  • Electricity
  • Escherichia coli O157 / cytology
  • Escherichia coli O157 / drug effects*
  • Escherichia coli O157 / genetics
  • Escherichia coli O157 / physiology*
  • Food Preservation / methods*
  • Food Safety
  • Fruit / microbiology
  • Gene Deletion
  • Hot Temperature
  • Hydrogen-Ion Concentration
  • Limonene
  • Microbial Viability / drug effects*
  • Sigma Factor / deficiency
  • Sigma Factor / genetics
  • Terpenes / metabolism
  • Terpenes / pharmacology*

Substances

  • Bacterial Proteins
  • Cyclohexenes
  • Sigma Factor
  • Terpenes
  • sigma factor KatF protein, Bacteria
  • Limonene

Grants and funding

This study was financially supported by the Comisón Interministerial de Ciencia y Tecnolog?a (CICYT) (Projects AGL2009-11660 and AGL2012-32165), Gobierno de Aragón, European Social Fund and Departament Quimica of Universitat Rovira i Virgili. Spanish Ministerio de Ciencia e Innovación provided LE with a grant to carry out this investigation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.