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Applied and Environmental Microbiology
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Food Microbiology

Behavior of foodborne pathogens, Listeria monocytogenes and Staphylococcus aureus, in mixed-species biofilm exposed to biocides

Virginie Oxaran, Karen Kiesbye Dittmann, Sarah H. I. Lee, Luíza Toubas Chaul, Carlos Augusto Fernandes de Oliveira, Carlos Humberto Corassin, Virgínia Farias Alves, Elaine Cristina Pereira De Martinis, Lone Gram
Virginie Oxaran
Department of Biotechnology and Biomedicine, Technical University of Denmark, Denmark
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Karen Kiesbye Dittmann
Department of Biotechnology and Biomedicine, Technical University of Denmark, Denmark
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Sarah H. I. Lee
FZEA/USP, Faculty of Animal Science and Food Engineering, University of São Paulo, Brazil
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Luíza Toubas Chaul
FF/UFG, Faculty of Pharmacy, Federal University of Goiás, Brazil
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Carlos Augusto Fernandes de Oliveira
FZEA/USP, Faculty of Animal Science and Food Engineering, University of São Paulo, Brazil
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Carlos Humberto Corassin
FZEA/USP, Faculty of Animal Science and Food Engineering, University of São Paulo, Brazil
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Virgínia Farias Alves
FF/UFG, Faculty of Pharmacy, Federal University of Goiás, Brazil
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Elaine Cristina Pereira De Martinis
FCFRP/USP, Faculty of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo Brazil.
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Lone Gram
Department of Biotechnology and Biomedicine, Technical University of Denmark, Denmark
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  • For correspondence: gram@bio.dtu.dk
DOI: 10.1128/AEM.02038-18
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ABSTRACT

In nature and man-made environments, microorganisms reside in mixed-species biofilm where behavior is modified compared to the single-species biofilms. Pathogenic microorganisms may be protected against adverse treatments in mixed-species biofilms leading to health risk for humans. Here, we developed two mixed-five-species biofilms that included the foodborne pathogens Listeria monocytogenes or Staphylococcus aureus, respectively. The five species, including the pathogen, were isolated from a single food-processing environmental sample thus mimicking the environmental community. In mature mixed five-species biofilms on stainless steel, the two pathogens remained at a constant level of ∼105 CFU/cm2. The mixed-five-species biofilms as well as the pathogens in mono-species biofilms were exposed to biocides to determine any pathogen-protective effect of the mixed biofilm. Both pathogens and their associate microbial communities were reduced by peracetic acid treatments. S. aureus decreased 4.6 log cycles in mono-species biofilm, but the pathogen was protected in the five-species biofilm and decreased only 1.1 log cycles. Sessile cells of L. monocytogenes were affected equally as a mono-biofilm or as a member in the mixed-species biofilm; decreasing by three log cycles when exposed to 0.0375 % peracetic acid. When the pathogen was exchanged in each associate microbial community, S. aureus was eradicated while there was no significant effect of the biocide on L. monocytogenes or the mixed community. This indicates that particular members or associations in the community offered the protective effect. Further studies are needed to clarify the mechanisms of biocide protection, and the species playing the protective role in microbial communities of biofilms.

Importance This study demonstrates that foodborne pathogens can be established in mixed species biofilms and that this can protect them from biocide action. The protection is not due to specific characteristics of the pathogen, here S. aureus and L. monocytogenes, but likely caused by specific members or associations in the mixed species biofilm. Biocide treatment and resistance is a challenge for many industries and biocide efficacy should be tested on microorganisms growing in biofilms, preferably mixed systems, mimicking the application environment.

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Behavior of foodborne pathogens, Listeria monocytogenes and Staphylococcus aureus, in mixed-species biofilm exposed to biocides
Virginie Oxaran, Karen Kiesbye Dittmann, Sarah H. I. Lee, Luíza Toubas Chaul, Carlos Augusto Fernandes de Oliveira, Carlos Humberto Corassin, Virgínia Farias Alves, Elaine Cristina Pereira De Martinis, Lone Gram
Appl. Environ. Microbiol. Oct 2018, AEM.02038-18; DOI: 10.1128/AEM.02038-18

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Behavior of foodborne pathogens, Listeria monocytogenes and Staphylococcus aureus, in mixed-species biofilm exposed to biocides
Virginie Oxaran, Karen Kiesbye Dittmann, Sarah H. I. Lee, Luíza Toubas Chaul, Carlos Augusto Fernandes de Oliveira, Carlos Humberto Corassin, Virgínia Farias Alves, Elaine Cristina Pereira De Martinis, Lone Gram
Appl. Environ. Microbiol. Oct 2018, AEM.02038-18; DOI: 10.1128/AEM.02038-18
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