Listeria monocytogenes Behaviour in Presence of Non-UV-Irradiated Titanium Dioxide Nanoparticles

Listeria monocytogenes is the agent of listeriosis, a food-borne disease. It represents a serious problem for the food industry because of its environmental persistence mainly due to its ability to form biofilm on a variety of surfaces. Microrganisms attached on the surfaces are a potential source of contamination for environment and animals and humans. Titanium dioxide nanoparticles (TiO2 NPs) are used in food industry in a variety of products and it was reported that daily exposure to these nanomaterials is very high. Anti-listerial activity of TiO2 NPs was investigated only with UV-irradiated nanomaterials, based on generation of reactive oxigen species (ROS) with antibacterial effect after UV exposure. Since both Listeria monocytogenes and TiO2 NPs are veicolated with foods, this study explores the interaction between Listeria monocytogenes and non UV-irradiated TiO2 NPs, with special focus on biofilm formation and intestinal cell interaction. Scanning electron microscopy and quantitative measurements of biofilm mass indicate that NPs influence both production and structural architecture of listerial biofilm. Moreover, TiO2 NPs show to interfere with bacterial interaction to intestinal cells. Increased biofilm production due to TiO2 NPs exposure may favour bacterial survival in environment and its transmission to animal and human hosts.

[1]  D. Passeri,et al.  Oral, short-term exposure to titanium dioxide nanoparticles in Sprague-Dawley rat: focus on reproductive and endocrine systems and spleen , 2014, Nanotoxicology.

[2]  Cesar Pulgarin,et al.  Bactericidal action of illuminated TiO2 on pure Escherichia coli and natural bacterial consortia: post-irradiation events in the dark and assessment of the effective disinfection time , 2004 .

[3]  G. Di Bonaventura,et al.  Influence of temperature on biofilm formation by Listeria monocytogenes on various food‐contact surfaces: relationship with motility and cell surface hydrophobicity , 2008, Journal of applied microbiology.

[4]  Kyung Bin Song,et al.  Disinfection of iceberg lettuce by titanium dioxide-UV photocatalytic reaction. , 2009, Journal of food protection.

[5]  P. Cossart,et al.  L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein , 1992, Cell.

[6]  R. P. Thompson,et al.  Immune potentiation of ultrafine dietary particles in normal subjects and patients with inflammatory bowel disease. , 2000, Journal of autoimmunity.

[7]  Soohyun Kim,et al.  Bacterial inactivation in water, DNA strand breaking, and membrane damage induced by ultraviolet-assisted titanium dioxide photocatalysis. , 2013, Water research.

[8]  C. Hedberg,et al.  Food-related illness and death in the United States. , 1999, Emerging infectious diseases.

[9]  George-John E. Nychas,et al.  Probabilistic Model for Listeria monocytogenes Growth during Distribution, Retail Storage, and Domestic Storage of Pasteurized Milk , 2010, Applied and Environmental Microbiology.

[10]  J. Lazzaroni,et al.  Photocatalysis and disinfection of water: Identification of potential bacterial targets , 2011 .

[11]  B. Finlay,et al.  The varied lifestyles of intracellular pathogens within eukaryotic vacuolar compartments. , 1995, Trends in microbiology.

[12]  P. Cossart,et al.  E-Cadherin Is the Receptor for Internalin, a Surface Protein Required for Entry of L. monocytogenes into Epithelial Cells , 1996, Cell.

[13]  P. Bowen,et al.  Catalytic activity of commercial of TiO2 powders for the abatement of the bacteria (E. coli) under solar simulated light: Influence of the isoelectric point , 2006 .

[14]  The bactericidal effect of TiO2 photocatalysis involves adsorption onto catalyst and the loss of membrane integrity. , 2006, FEMS microbiology letters.

[15]  J Böckmann,et al.  [Blood titanium levels before and after oral administration titanium dioxide]. , 2000, Die Pharmazie.

[16]  J. Swanson,et al.  Cytolysin‐dependent delay of vacuole maturation in macrophages infected with Listeria monocytogenes , 2006, Cellular microbiology.

[17]  P. Westerhoff,et al.  Titanium dioxide nanoparticles in food and personal care products. , 2012, Environmental science & technology.

[18]  M. Pucciarelli,et al.  Remodeling of the Listeria monocytogenes cell wall inside eukaryotic cells , 2012, Communicative & integrative biology.

[19]  Pedro J J Alvarez,et al.  Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. , 2006, Water research.

[20]  J. Yates,et al.  Photocatalysis on TiO2 Surfaces: Principles, Mechanisms, and Selected Results , 1995 .

[21]  R. Briandet,et al.  Listeria monocytogenes Scott A: Cell Surface Charge, Hydrophobicity, and Electron Donor and Acceptor Characteristics under Different Environmental Growth Conditions , 1999, Applied and Environmental Microbiology.

[22]  C. Longhi,et al.  Heterogeneity of Virulence-Related Properties in Listeria Monocytogenes Strains Isolated from Patients with Haematological Malignancies , 2003, International journal of immunopathology and pharmacology.

[23]  J. Blanco,et al.  Application of the colloidal stability of TiO2 particles for recovery and reuse in solar photocatalysis. , 2003, Water research.

[24]  I. Mackay,et al.  Listeria faecal carriage by renal transplant recipients, haemodialysis patients and patients in general practice: its relation to season, drug therapy, foreign travel, animal exposure and diet , 1991, Epidemiology and Infection.

[25]  A. Kohler,et al.  Complex Phenotypic and Genotypic Responses of Listeria monocytogenes Strains Exposed to the Class IIa Bacteriocin Sakacin P , 2009, Applied and Environmental Microbiology.

[26]  A. Amoresano,et al.  Protease treatment affects both invasion ability and biofilm formation in Listeria monocytogenes. , 2008, Microbial pathogenesis.

[27]  G. Nychas,et al.  Listeria monocytogenes Attachment to and Detachment from Stainless Steel Surfaces in a Simulated Dairy Processing Environment , 2009, Applied and Environmental Microbiology.

[28]  J. Powell,et al.  Fine Particles That Adsorb Lipopolysaccharide Via Bridging Calcium Cations May Mimic Bacterial Pathogenicity Towards Cells , 2007, Experimental biology and medicine.

[29]  D. Roy,et al.  Characterization of physicochemical forces involved in adhesion of Listeria monocytogenes to surfaces , 1991, Applied and environmental microbiology.

[30]  Dohwan Kim,et al.  Bactericidal effect of TiO2 photocatalyst on selected food-borne pathogenic bacteria. , 2003, Chemosphere.

[31]  Olivier Cerf,et al.  Review--Persistence of Listeria monocytogenes in food industry equipment and premises. , 2011, International journal of food microbiology.

[32]  Pascale Cossart,et al.  Bacterial Invasion: The Paradigms of Enteroinvasive Pathogens , 2004, Science.

[33]  F. Toldrá,et al.  Opinion of the Scientific Panel on Food Additives, Flavourings, Processing Aids and Materials in contact with Food (AFC) on a request from the Commission , 2005 .

[34]  G. Nychas,et al.  Microbial ecology of food contact surfaces and products of small-scale facilities producing traditional sausages. , 2008, Food microbiology.

[35]  Alexander T. Florence,et al.  Titanium dioxide (rutile) particle uptake from the rat GI tract and translocation to systemic organs after oral administration , 1994 .

[36]  J. Powell,et al.  Fine and ultrafine particles of the diet: influence on the mucosal immune response and association with Crohn’s disease , 2002, Proceedings of the Nutrition Society.

[37]  F Allerberger,et al.  Listeriosis: a resurgent foodborne infection. , 2010, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[38]  M. Woolhouse,et al.  Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157 , 2008, Nature Reviews Microbiology.

[39]  J. Powell,et al.  Dietary sources of inorganic microparticles and their intake in healthy subjects and patients with Crohn's disease. , 2004, The British journal of nutrition.

[40]  M. Wiedmann,et al.  Markov chain approach to analyze the dynamics of pathogen fecal shedding--example of Listeria monocytogenes shedding in a herd of dairy cattle. , 2007, Journal of theoretical biology.

[41]  C. Rhee,et al.  Dispersion properties of TiO2 nano-powder synthesized by homogeneous precipitation process at low temperatures , 2003 .

[42]  F. Allerberger,et al.  Incidence of Fecal Carriage of Listeria monocytogenes in Three Healthy Volunteers: A One-Year Prospective Stool Survey , 2003, European Journal of Clinical Microbiology and Infectious Diseases.

[43]  Marie Carrière,et al.  Size-, composition- and shape-dependent toxicological impact of metal oxide nanoparticles and carbon nanotubes toward bacteria. , 2009, Environmental science & technology.

[44]  J. Böckmann,et al.  Titan-Blutspiegel vor und nach Belastungsversuchen mit Titandioxid , 2000 .

[45]  S. Guadagnini,et al.  ActA Promotes Listeria monocytogenes Aggregation, Intestinal Colonization and Carriage , 2013, PLoS pathogens.

[46]  James P. Folsom,et al.  Chlorine resistance of Listeria monocytogenes biofilms and relationship to subtype, cell density, and planktonic cell chlorine resistance. , 2006, Journal of food protection.

[47]  Efstathios Z Panagou,et al.  Use of titanium dioxide (TiO2) photocatalysts as alternative means for Listeria monocytogenes biofilm disinfection in food processing. , 2011, Food microbiology.

[48]  Z. Chai,et al.  Acute toxicity and biodistribution of different sized titanium dioxide particles in mice after oral administration. , 2007, Toxicology letters.

[49]  Jesse T. Myers,et al.  Localized Reactive Oxygen and Nitrogen Intermediates Inhibit Escape of Listeria monocytogenes from Vacuoles in Activated Macrophages 1 , 2003, The Journal of Immunology.

[50]  Kurt Straif,et al.  Carcinogenicity of carbon black, titanium dioxide, and talc. , 2006, The Lancet Oncology.

[51]  A. Arsenault,et al.  Pigment resembling atmospheric dust in Peyer's patches. , 1989, Modern pathology : an official journal of the United States and Canadian Academy of Pathology, Inc.

[52]  J. Powell,et al.  Dietary microparticles implicated in Crohn’s disease can impair macrophage phagocytic activity and act as adjuvants in the presence of bacterial stimuli , 2007, Inflammation Research.

[53]  M. Doyle,et al.  Reducing the carriage of foodborne pathogens in livestock and poultry. , 2006, Poultry science.

[54]  C. Hill,et al.  An in vitro cell-culture model demonstrates internalin- and hemolysin-independent translocation of Listeria monocytogenes across M cells. , 2006, Microbial pathogenesis.