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Listeria Monocytogenes Growth Limits and Stress Resistance Mechanisms

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Listeria Monocytogenes Growth Limits and Stress Resistance Mechanisms Listeria monocytogenes growth limits and stress resistance mechanisms Stijn van der Veen Promotoren Prof. Dr. T. Abee Persoonlijk Hoogleraar, Leerstoelgroep Levensmiddelenmicrobiologie Wageningen Universiteit Prof. Dr. W. M. de Vos Hoogleraar Microbiologie Wageningen Universiteit Co-Promotor Dr. Ir. M. H. J. Wells-Bennik Project Manager Health & Safety NIZO food research B.V. Promotiecommissie Prof. Dr. J. Wells Wageningen Universiteit Prof. Dr. O. P. Kuipers Rijksuniversiteit Groningen Prof. Dr. S. A. Brul Universiteit van Amsterdam Prof. Dr. C. Hill University College Cork, Ireland Dit onderzoek is uitgevoerd binnen de onderzoekschool VLAG Listeria monocytogenes growth limits and stress resistance mechanisms Stijn van der Veen Proefschrift ter verkrijging van de graad van doctor op gezag van de rector magnificus van Wageningen Universiteit, Prof. Dr. M. J. Kropff, in het openbaar te verdedigen op dinsdag 9 december 2008 des namiddags te vier uur in de Aula Stijn van der Veen . Listeria monocytogenes growth limits and stress resistance mechanisms. PhD thesis. Wageningen University, Wageningen, The Netherlands (2008). With summary in Dutch. ISBN: 978-90-8585-262-9 Te weten wat men weet en te weten wat men niet weet, dat is kennis Confucius Content Abstract ..........................................................................................................9 1. General introduction and outline of the thesis .........................................11 2. The growth limits of a large number of Listeria monocytogenes strains at combinations of stresses show serotype- and niche-specific traits ..........41 3. Diversity assessment of heat resistance of Listeria monocytogenes strains in a continuous flow heating system.................................................63 4. The heat-shock response of Listeria monocytogenes comprises genes involved in heat-shock, cell division, cell wall synthesis, and the SOS response........................................................................................................77 5. Genome-wide screen for Listeria monocytogenes genes important for growth at high temperatures.......................................................................103 6. The Listeria monocytogenes motility regulator MogR controls expression of clpB and affects stress resistance.........................................117 7. The SOS response of Listeria monocytogenes is involved in stress resistance and mutagenesis ........................................................................133 8. General discussion and conclusions.......................................................153 Samenvatting..............................................................................................165 Nawoord.....................................................................................................169 List of Publications ....................................................................................171 Curriculum Vitae........................................................................................173 VLAG graduate school activities...............................................................175 Abstract The food-borne pathogen Listeria monocytogenes is a Grampositive facultative anaerobic rod, which is the causative agent of listeriosis. Due to the severity of the disease and the fact that its incidence is increasing in numerous European countries, L. monocytogenes is of great public health concern. This bacterium shows relatively high resistance to environmental insults compared with many other non-spore-forming food- borne pathogens. It is able to grow at low pH, at high salt concentrations, and low temperatures. The possibility that this pathogen (cross-) contaminates food products is a major concern for the food industry. Therefore, it is important to investigate the diversity in growth potential and stress resistance (mechanisms) of L. monocytogenes strains at both the serotype as well as the population level, during exposure to commonly used preservation conditions. Several approaches are described in this thesis, including comparison of stress resistance and growth limits of a large collection of natural isolates, screening a mutant library for stress sensitive mutants, and transcription profiling of stress responses. The function of various stress response genes and mechanisms including the so-called SOS response are described in detail. The SOS response in L. monocytogenes appears to be important for stress resistance and for the induction of mutations, resulting in L. monocytogenes variants. The SOS regulon of L. monocytogenes was shown to consist of 29 genes encoding proteins with functions in error-prone DNA synthesis and DNA repair. It also includes the bile extrusion system BilE, which is known to affect virulence properties of L. monocytogenes by conferring resistance to bile. The SOS response may therefore contribute to the generation and persistence of L. monocytogenes variants in food processing environments and in the human host. This thesis provides novel insights in the natural diversity of L. monocytogenes strains, and it has been revealed that specific groups of strains (serotypes) can be more persistent in specific niches such as food processing environments and retail establishments. Functional assessment of specific transcriptional regulators revealed an overlap in target genes and added to further understanding of the activation and function of the complex stress response network in this human pathogen. 9 1. General introduction and outline of the thesis Stijn van der Veen, Tjakko Abee, Marjon H. J. Wells-Bennik Abstract The food-borne pathogen Listeria monocytogenes is a Grampositive facultative anaerobic rod, which is the causative agent of listeriosis. Due to the severity of the disease, the high mortality rate, and the fact that its incidence is increasing in numerous European countries, L. monocytogenes is of great concern to public health. This bacterium shows relatively high resistance to environmental insults compared with many other non-spore- forming food-borne pathogens. It is able to grow at a wide pH range (from pH4.5 to pH 9), at high salt concentrations (up to 13%), and at a wide temperature range (-0.4 to 46 ºC) and it is able to survive more extreme acid conditions, salt concentrations, and temperatures for extended periods of time. The ability of L. monocytogenes to proliferate under adverse conditions and survive environmental insults results from various mechanisms that allow for rapid responses and adaptation to changing environments. Due to consumer’s demands for less heavily preserved foods and more convenience foods, processing conditions in the food industry are becoming milder. L. monocytogenes is able to adapt to such milder conditions, making it of major concern to the food industry. To adequately inactivate L. monocytogenes and/or to prevent growth during storage, more knowledge is required about the stress response mechanisms of this bacterium that determine resistance to stress and about (genetic) diversity between different strains and serotypes. This chapter gives a short history on the food-borne pathogen L. monocytogenes , shows an overview of the current knowledge on the most important stress responses, and provides an outline of this thesis. 11 History The first reports of “listiric” infections go back as far as 1891 when the presence of Gram-positive rods was described in tissue sections of deceased patients. In 1926 E.G.D. Murray et al. (110) was the first to describe this bacterium as a non-spore-forming Gram- positive rod that infects monocytes of the blood, resulting in diseases in rabbits and guinea pigs. This strain was therefore named Bacterium monocytogenes . Notably, a derivative of this strain (EGD-e, after Murray’s initials) later became the first L. monocytogenes strain to be completely sequenced (58).The first confirmed reported case of L. monocytogenes in human was made in 1929 by Nyfeldt (62). In 1940 its present name was given by Pirie (62). After a period in which only sporadic cases of listeriosis were reported, mostly involving workers that had been in contact with diseased animals, interest in L. monocytogenes grew rapidly in the 1980s after reports of several food-borne outbreaks. In one of these outbreaks pasteurised milk was identified as the vehicle, raising the question whether L. L. monocytogenes 4a L. monocytogenes 4c L. monocytogenes 4e L. monocytogenes 4d L. monocytogenes 4b L. monocytogenes 7 L. monocytogenes 1/2b L. monocytogenes 3b Common ancestor L. monocytogenes 1/2a L. monocytogenes 3c L. monocytogenes 1/2c L. monocytogenes 3a Fig. 1. Evolutionary scheme of the L. monocytogenes lineages and serovars based on the antigenic properties and the presence and absence of genes (derived from (43)). 12 monocytogenes was capable of surviving a pasteurisation step (53). The strain ScottA, which was isolated during this outbreak, is still the most researched strain in thermal inactivation studies. Due to the work on pathogenicity following these outbreaks, L. monocytogenes is now regarded as one of the invasive model strains in pathogen research (25). Species L. monocytogenes is part of the Listeria genus together with five other species: the pathogenic species L. ivanovii and the non-pathogenic species L. seeligeri , L. welshimeri , L. innocua , and L. grayi (128). The species L. monocytogenes contains 13 different serotypes, which are divided over three lineages according to the presence of specific
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