Critical Reviews in Food Science and Nutrition

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Physiology and Genetics of Listeria Monocytogenes Survival and Growth at Cold Temperatures a

Yvonne C. Chan & Martin Wiedmann

a

a

Department of Food Science , Cornell University , Ithaca, NY, 14853, USA Published online: 17 Dec 2008.

To cite this article: Yvonne C. Chan & Martin Wiedmann (2008) Physiology and Genetics of Listeria Monocytogenes Survival and Growth at Cold Temperatures, Critical Reviews in Food Science and Nutrition, 49:3, 237-253, DOI: 10.1080/10408390701856272 To link to this article: http://dx.doi.org/10.1080/10408390701856272

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Critical Reviews in Food Science and Nutrition, 49:237–253 (2009) C Taylor and Francis Group, LLC Copyright  ISSN: 1040-8398 DOI: 10.1080/10408390701856272

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Physiology and Genetics of Listeria Monocytogenes Survival and Growth at Cold Temperatures YVONNE C. CHAN and MARTIN WIEDMANN Department of Food Science, Cornell University, Ithaca, NY 14853, USA

Listeria monocytogenes is a foodborne pathogen that can cause serious invasive human illness in susceptible patients, notably immunocompromised, pregnant women, and adults >65 years old. Most human listeriosis cases appear to be caused by consumption of refrigerated ready-to-eat foods that are contaminated with high levels of L. monocytogenes. While initial L. monocytogenes levels in contaminated foods are usually low, the ability of L. monocytogenes to survive and multiply at low temperatures allows it to reach levels high enough to cause human disease, particularly if contaminated foods that allow for L. monocytogenes growth are stored for prolonged times under refrigeration. In this review, relevant knowledge on the physiology and genetics of L. monocytogenes’ ability to adapt to and multiply at low temperature will be summarized and discussed, including selected relevant findings on the physiology and genetics of cold adaptation in other Gram-positive bacteria. Further improvement in our understanding of the physiology and genetics of L. monocytogenes cold growth will hopefully enhance our ability to design successful intervention strategies for this foodborne pathogen. Keywords

ready-to-eat refrigerated foods, food safety, foodborne pathogen, cold shock proteins, cold adaptation

INTRODUCTION Listeria monocytogenes is a Gram positive, non-sporulating, facultative anaerobic foodborne pathogen. While human listeriosis is rare with an incidence of 2 to 15 cases per 1 million people per year reported in developed countries (Farber and Peterkin, 1991; Mead et al., 1999), invasive listeriosis generally represents a severe disease with a case mortality rate of 20 to 30% (Farber and Peterkin, 1991; Mead et al., 1999). A study published in 1999 estimated that 2,500 human cases of invasive listeriosis occur annually in the U.S., including 500 cases that result in death (Mead et al., 1999). In pregnant women, L. monocytogenes can cross the placenta causing premature births, stillbirths, miscarriages, or neonatal listeriosis (Evans et al., 1985; McLauchlin, 1990; Mylonakis et al., 2002). Other manifestations of invasive listeriosis include septicemia, meningitis, meningoencephalitis, and less frequently endocarditis (Doganay, 2003). Healthy young individuals rarely acquire invasive L. monocytogenes infections; most listeriosis cases occur in particularly susceptible host populations, which include, in addition to pregnant women, organ Address correspondence to Martin Wiedman, 412 Stocking Hall, Cornell University, Ithaca, NY 14853. Tel.: 607-254-2838 Fax: 607-254-4868 E-mail: [email protected]

transplant recipients, cancer patients, AIDS patients, individuals with other immunocompromising conditions as well as adults over 65 (CDC [Centers for Disease Control and Prevention], 2005; Goulet and Marchetti, 1996; Jurado et al., 1993; Maijala et al., 2001; Safdar and Armstrong, 2003). For example, AIDS patients have been reported to be 145 times more likely to contract listeriosis as compared to the general population (Jurado et al., 1993). In addition to invasive listeriosis, L. monocytogenes infections with mild flu-like symptoms (e.g., nausea, diarrhea, and fever) have been reported (Riedo et al., 1994), including a number of outbreaks of diarrheal listeriosis (Aureli et al., 2000; Carrique-Mas et al., 2003; Dalton et al., 1997; Frye et al., 2002; Miettinen et al., 1999; Salamina et al., 1996; Sim et al., 2002). One specific characteristic of L. monocytogenes that appears to be critical to its ability to cause human foodborne illness is its capacity to grow at low temperatures. L. monocytogenes has been shown to grow at temperatures ranging from −0.4 to 45◦ C (Gray and Killinger, 1966; Junttila et al., 1988; Walker and Stringer, 1987). It is considered a psychrotolerant organism as its optimum growth temperature is in the range of 30 to 37◦ C, while it has the ability to grow at temperatures 1,000 CFU/g at the time of consumption, the number of human listeriosis cases would decrease from 2,500 to approximately 6 (ILSI Research Foundation/Risk Science Institute Expert Panel on Listeria monocytogenes in Foods, 2005; U.S. Department of Health and Human Services/U.S. Department of Agriculture, 2003), further supporting the idea that low numbers of L. monocytogenes present a minimal human health risk. As L. monocytogenes is effectively killed by heat treatments typical for cooking and commercial food preparation (e.g., milk pasteurization), foods positive for this pathogen at point of consumption generally can be traced back to post-processing contamination from environmental sources, including processing plants (Cox et al., 1989;

Gravani, 1999; Hoffman et al., 2003; Pritchard et al., 1995) and retail environments (Elson et al., 2004; Gillespie et al., 2000; Gombas et al., 2003; Humphrey and Worthington, 1990) as well as, most likely, environmental sources in restaurants, institutional kitchens, and consumer homes (Salamina et al., 1996). In general, L. monocytogenes contamination from environmental sources only leads to low levels of L. monocytogenes in foods (Gombas et al., 2003; Wallace et al., 2003); the pathogen numbers found immediately after contamination and prior to bacterial growth are thus extremely unlikely to cause human disease (ILSI Research Foundation/Risk Science Institute Expert Panel on Listeria monocytogenes in Foods, 2005). L. monocytogenes growth subsequent to initial contamination can be substantial though, particularly in refrigerated RTE foods that (i) have general physico-chemical characteristics that permit L. monocytogenes growth, and (ii) are stored for extended times under refrigeration temperature, thus allowing for growth of the psychrotolerant L. monocytogenes, while growth of many competing microorganisms is inhibited. The importance of L. monocytogenes growth in refrigerated RTE foods has been well documented in the USDA/U.S. DHHS L. monocytogenes risk assessment published in 2003 (U.S. Department of Health and Human Services/U.S. Department of Agriculture, 2003) and it is apparent that the number of human listeriosis cases could be considerably reduced if L. monocytogenes growth in contaminated foods could be limited or completely prevented (ILSI Research Foundation/Risk Science Institute Expert Panel on Listeria monocytogenes in Foods, 2005). In addition, a review of selected human listeriosis outbreaks linked to contaminated food products (Billie, 1990; CDC (Centers for Disease Control and Prevention), 1999, 2000, 2002; de Valk et al., 2001; Ericsson et al., 1997; Farber et al., 2000; Ho et al., 1986; James et al., 1985; Linnan et al., 1988; Schlech et al., 1983), also illustrates the importance of L. monocytogenes growth in contaminated foods in many outbreaks (de Valk et al., 2001; Ericsson et al., 1997; Schlech et al., 1983). For example, after several L. monocytogenes outbreaks in France, the shelf-life of RTE rillettes and jellied pork tongue was reduced from 48 days to 28 days due to concerns of prolonged shelflife as a critical factor allowing for L. monocytogenes growth in these food products sufficient to yield bacterial numbers that can cause human disease (de Valk et al., 2001). A human listeriosis outbreak in Sweden with 9 confirmed cases, including 2 fatalities (Ericsson et al., 1997), was linked to contaminated “gravad” rainbow trout; a food product which is generally stored for extended times (3 to 6 weeks) at refrigeration temperature (Ericsson et al., 1997). An investigation of a listeriosis outbreak (with 41 documented cases) linked to consumption of contaminated coleslaw in the Maritime Provinces of Canada, also provided evidence for importance of cold storage and, most likely, concurrent growth of L. monocytogenes in the etiology of listeriosis outbreaks (Schlech et al., 1983). Apparently, the cabbage used for production of the coleslaw implicated as the source of this outbreak was harvested from a field that was fertilized with manure from sheep flock with a history of ovine listeriosis,

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PHYSIOLOGY AND GENETICS OF LISTERIA MONOCYTOGENES

providing for a plausible route of initial contamination (Schlech et al., 1983). The harvested cabbage was subsequently stored under cold temperatures from winter to early spring, which was hypothesized to allow for proliferation of L. monocytogenes to levels that lead to contamination of the finished coleslaw with bacterial numbers sufficient to cause human listeriosis (Schlech et al., 1983). In summary, numerous laboratory studies that have shown the ability of L. monocytogenes to grow on many refrigerated RTE foods (Ben Embarek, 1994; Brackett, 1999; Cox et al., 1999; Farber and Peterkin, 1999; International Commission on Microbiological Specifications for Foods, 1996; Jinneman et al., 1999; Pearson and Marth, 1990; Ryser, 1999a, 1999b; U.S. Department of Health and Human Services/U.S. Department of Agriculture, 2003) as well as risk assessments (U.S. Department of Health and Human Services/U.S. Department of Agriculture, 2003) and outbreaks investigations (de Valk et al., 2001; Ericsson et al., 1997; Schlech et al., 1983) support that the ability of L. monocytogenes to grow during refrigerated storage likely is a major contributing factor to the transmission of this foodborne illness. In particular, RTE food products that support the growth of L. monocytogenes and are stored for extended times at cold temperatures may be at a high risk of allowing for growth of L. monocytogenes to levels causing human disease.

SURVIVAL AND GROWTH OF L. MONOCYTOGENES AT LOW TEMPERATURES Large numbers of laboratory studies have shown that L. monocytogenes is able to grow at low temperatures in a variety of refrigerated foods (Ben Embarek, 1994; Brackett, 1999; Cox et al., 1999; Farber and Peterkin, 1999; International Commission on Microbiological Specifications for Foods, 1996; Jinneman et al., 1999; Pearson and Marth, 1990; Ryser, 1999a, 1999b; U.S. Department of Health and Human Services/U.S. Department of Agriculture, 2003). While growth of L. monocytogenes has been reported at temperatures as low as −0.4◦ C for some foods (International Commission on Microbiological Specifications for Foods, 1996), L. monocytogenes growth at temperatures below 4◦ C is generally very slow (usually with doubling times of 12 to >50 h) (International Commission on Microbiological Specifications for Foods, 1996; Lou and Yousef, 1999). In addition, the lag phase for L. monocytogenes at refrigeration temperatures can be very long (e.g., 59 to 477 h for vacuum and CO2 packed roast beef, respectively, at 3◦ C [Farber and Peterkin, 1999]). As the temperature increases above 4◦ C, L. monocytogenes growth rate increases and lag phase time decreases considerably; consequently storage at slight abuse temperatures (e.g., 7 to 10◦ C) of refrigerated RTE foods that permit L. monocytogenes growth greatly increases the risk that L. monocytogenes, if present, will reach numbers that could cause human disease (ILSI Research Foundation/Risk Science Institute Expert Panel on Listeria monocytogenes in Foods, 2005; International Commission on Microbiological Specifications for

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Foods, 1996). For example, while L. monocytogenes lag phase duration and doubling time in frankfurters stored at 4.4◦ C were 18 days and 43 h, respectively, they were 6.5 days and 10.5 h at 10◦ C (Lu et al., 2005). While this example is provided, a complete review of different studies that evaluated L. monocytogenes growth at cold temperatures is beyond the scope of this review. A comprehensive summary of many studies on L. monocytogenes growth in a variety of foods and under different temperatures is provided in the ICMSF book 5 (International Commission on Microbiological Specifications for Foods, 1996). In addition to temperature, a variety of other factors affect L. monocytogenes growth rate and lag phase duration, including pH (in general L. monocytogenes can grow from pH 4.3 to 9.6 [Seeliger and Jones, 1986]), water activity (L. monocytogenes can grow at aw ≥0.92 [International Commission on Microbiological Specifications for Foods, 1996]), and the presence of inhibitors, including organic acids (Bereksi et al., 2002; Conner et al., 1986; Davis et al., 1996). The presence of different compatible solutes that can be found in foods (Mitchell, 1978; Zeisel et al., 2003), such as carnitine and glycine betaine, can also affect the ability of L. monocytogenes to grow under cold temperatures (Angelidis and Smith, 2003a; Bayles and Wilkinson, 2000; Sleator et al., 2003a). Thus, different refrigerated RTE foods can differ considerably in their ability to support L. monocytogenes growth depending on their physico-chemical properties. Knowledge of the different factors affecting the ability of L. monocytogenes to grow at refrigeration temperatures can also be used to reformulate refrigerated RTE foods to limit their ability to support L. monocytogenes growth during cold storage (ILSI Research Foundation/Risk Science Institute Expert Panel on Listeria monocytogenes in Foods, 2005). In particular, reformulation of RTE deli meats using organic acids (e.g., sodium lactate and sodium diacetate) has shown considerable promise in retarding L. monocytogenes growth by both extending the lag phase and decreasing the growth rate for L. monocytogenes in reformulated foods stored under low temperatures (Bedie et al., 2001; Mbandi and Shelef, 2001; Porto et al., 2002; Tompkin, 2002). In conclusion, while L. monocytogenes can grow at low temperatures in many foods and environments, a variety of factors can affect its growth rate and lag time at low temperature. Consequently, the specific mechanisms that can be used by L. monocytogenes to facilitate its growth at low temperature are likely to differ depending on the food matrix and the environment, representing a considerable challenge as the scientific community tries to develop a better understanding of the mechanisms that facilitate L. monocytogenes growth in different RTE food products under refrigeration temperatures. MECHANISMS CONTRIBUTING TO L. MONOCYTOGENES COLD TEMPERATURE SURVIVAL AND ADAPTATION Bacteria that transition to low temperatures have to overcome a number of well-recognized problems, including (i) decreased

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membrane fluidity, which reduces nutrient uptake capabilities; (ii) increased superhelical coiling of DNA, which may negatively effect a bacterium’s ability to replicate or transcribe DNA, (iii) secondary structures in RNA, affecting translation, (iv) reduced enzyme activities, (v) inefficient or slow protein folding, and (vi) the need to adapt ribosomes to function properly at low temperatures (Graumann and Marahiel, 2000). As the temperature decreases, the metabolic rate of bacterial cells also decreases, and bacteria respond by changing their membrane composition and by altering their gene expression to overcome these problems (Annous et al., 1997; Gounot and Russell, 1999; Inouye and Phadtare, 2004; Liu et al., 2002; Russell, 1990). Adaptation of bacteria to low temperatures can be divided into three phases, including initial cold shock, acclimation, and coldadapted status (Thieringer et al., 1998). When a rapid change from a bacterium’s optimum growth temperature to a lower temperature (i.e., a “cold shock”) occurs, synthesis of non-coldshock proteins is inhibited (including through transient block of translation initiation) while synthesis of cold shock proteins (CSPs), which is at low levels at 37◦ C, increases dramatically in this acclimation phase (Thieringer et al., 1998). These CSPs can facilitate translation initiation by acting as RNA chaperones, binding to single-stranded RNA until the ribosome can initiate translation (Hunger et al., 2006; Jiang et al., 1997), thus assisting in cold adaptation. As bacterial cells become cold-adapted, non-CSPs protein synthesis increases, while CSPs synthesis decreases (Thieringer et al., 1998). The subsequent sections will summarize and review specific mechanisms L. monocytogenes uses to respond to cold shock and to facilitate growth at low temperatures. In addition, a recent review of L. monocytogenes cold stress tolerance by Tasara and Stephan (2006) provides further details on mechanisms L. monocytogenes can use to adapt to low temperatures.

Cold Shock Proteins (CSPs) and Cold Acclimation Proteins (CAPs) Studies on a number of bacteria exposed to a rapid downshift from optimal growth temperature to lower temperatures have revealed induction of synthesis of proteins important for survival or growth at low temperatures (Bayles et al., 1996; Datta and Bhadra, 2003; Goverde et al., 1998; Imbert and Gancel, 2004; Jeffreys et al., 1998; Katzif et al., 2003; Mayr et al., 1996; McGovern and Oliver, 1995; Phan-Thanh and Gormon, 1995). In particular, bacterial proteins whose expression is induced upon temperature downshift have been classified as cold shock proteins (CSPs) or cold acclimation proteins (CAPs) (Graumann and Marahiel, 2000). CSPs are induced rapidly upon exposure to low temperatures, but synthesis of these proteins usually is transient (Thieringer et al., 1998). CAPs, on the other hand, are not only induced upon exposure to cold shock but their expression remains at high levels for a prolonged time (Budde et al., 2006). In fact, cold shock is often defined as a sudden change from the organism’s optimal growth temperature to a lower temperature

that permits growth and causes an immediate, transient synthesis of CSPs (Thieringer et al., 1998). However, some studies and reports have classified CSPs as all proteins induced upon cold shock with CAPs representing a subset of CSPs (Bayles et al., 1996; Graumann and Marahiel, 2000). Thus, nomenclature of different proteins induced upon cold shock is not necessarily consistent between different authors and/or different bacterial species. CSPs have been found in a wide range of bacterial pathogens, including L. monocytogenes, Bacillus cereus, Yersinia enterocolitica, Vibrio vulnificus, Vibrio cholerae, Salmonella enteritidis, Staphylococcus aureus, and Aeromonas hydrophila (Anderson et al., 2006; Bayles et al., 1996; Datta and Bhadra, 2003; Goverde et al., 1998; Imbert and Gancel, 2004; Jeffreys et al., 1998; Katzif et al., 2003; Mayr et al., 1996; McGovern and Oliver, 1995; Phan-Thanh and Gormon, 1995). In particular, CSPs have been extensively studied in the Gram-negative and Gram-positive model organisms Escherichia coli (Jiang et al., 1997; Jones et al., 1987; Phadtare and Inouye, 2004) and Bacillus subtilis (Graumann and Marahiel, 1997; Graumann et al., 1996; Graumann et al., 1997; Kaan et al., 2002; Lottering and Streips, 1995). In E. coli, CSPs have been classified into two categories, Class I and Class II CSPs (Thieringer et al., 1998). Expression of class I CSPs occurs at low or undetectable levels at 37◦ C and is dramatically increased during cold shock (Thieringer et al., 1998). Class II CSPs on the other hand are expressed at 37◦ C and their expression is only moderately increased during cold shock (Thieringer et al., 1998). In B. subtilis, proteins rapidly induced upon temperature downshift have also been classified as cold shock proteins (CSPs) and cold-induced proteins (CIPs) (Graumann and Marahiel, 2000) with CIPs defined as specific small proteins (