Salmonella Cold Stress Response: Mechanisms and Occurrence in Foods

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Salmonella Cold Stress Response: Mechanisms and Occurrence in Foods Steven C. Ricke*,†,‡,1, Turki M. Dawoud*,†,§,2, Sun Ae Kim†,‡,§,3, Si Hong Park*,†,‡,4, Young Min Kwon*,†,§ *Cell and Molecular Biology Program, University of Arkansas, Fayetteville, AR, United States † Center for Food Safety, University of Arkansas, Fayetteville, AR, United States ‡ Department of Food Science, University of Arkansas, Fayetteville, AR, United States § Department of Poultry Science, University of Arkansas, Fayetteville, AR, United States 1 Corresponding author: e-mail address: [email protected]

Contents 1. Introduction 2. Molecular Mechanisms to Counter Cold Shock 2.1 General Concepts on Environmental Stress 2.2 Cold Stress: Physiological Responses 2.3 Cold Shock Response: Molecular Profiles 2.4 Cell Membrane Modification 2.5 DNA Supercoiling Modification 2.6 CIP Synthesis 3. Salmonella–Cold Shock Interaction With Other Stress Responses 3.1 Cross-Protection 3.2 Interaction With Virulence Responses 4. Salmonella Responses to Cold Temperatures in Food Production 4.1 Salmonella Growth, Survival, and Influential Factors 4.2 Beef Products 4.3 Chicken Meat Products 4.4 Other Food Products 5. Conclusions Acknowledgments References

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Current address: Botany and Microbiology Department, Science College, King Saud University, Riyadh 11451, Saudi Arabia Current address: Department of Food Science and Engineering, Ewha Womans University, Seoul, South Korea Current address: Department of Food Science and Technology, Oregon State University, Corvallis, OR, USA 97331

Advances in Applied Microbiology ISSN 0065-2164 https://doi.org/10.1016/bs.aambs.2018.03.001

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2018 Elsevier Inc. All rights reserved.

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Abstract Since bacteria in foods often encounter various cold environments during food processing, such as chilling, cold chain distribution, and cold storage, lower temperatures can become a major stress environment for foodborne pathogens. Bacterial responses in stressful environments have been considered in the past, but now the importance of stress responses at the molecular level is becoming recognized. Documenting how bacterial changes occur at the molecular level may help to achieve the in-depth understanding of stress responses, to predict microbial fate when they encounter cold temperatures, and to design and develop more effective strategies to control pathogens in food for ensuring food safety. Microorganisms differ in responding to a sudden downshift in temperature and this, in turn, impacts their metabolic processes and can cause various structural modifications. In this review, the fundamental aspects of bacterial cold stress responses focused on cell membrane modification, DNA supercoiling modification, transcriptional and translational responses, cold-induced protein synthesis including CspA, CsdA, NusA, DnaA, RecA, RbfA, PNPase, KsgA, SrmB, trigger factors, and initiation factors are discussed. In this context, specific Salmonella responses to cold temperature including growth, injury, and survival and their physiological and genetic responses to cold environments with a focus on cross-protection, different gene expression levels, and virulence factors will be discussed.

1. INTRODUCTION Foodborne agents are responsible for numerous infectious diseases in humans as a result of ingestion of contaminated foods. Contaminated food and water with various pathogens have been the main vehicles of infection for diarrheal diseases worldwide and their contamination can take place at multiple points during all stages of food production and subsequent processing and retail (Cairncross et al., 2010; Crandall et al., 2013; Finstad, O’Bryan, Marcy, Crandall, & Ricke, 2012; Howard, O’Bryan, Crandall, & Ricke, 2012; O’Ryan, Prado, & Pickering, 2005; Podewils, Mintz, Nataro, & Parashar, 2004; Santosham et al., 2010; Schmidt & Cairncross, 2009). Foodborne agents have been estimated to cause nearly 48 million illnesses in the United States with 128,000 hospitalizations and over 3000 deaths, which means that approximately 15% of the total US population will annually experience a foodborne infection (Scallan et al., 2011). Thus their contamination in food is considered a major public concern for both consumers and related industries. Salmonella is a leading source of foodborne outbreaks throughout the world and is typically associated with the consumption of poultry, beef, lamb, seafood, vegetables, fruits, and their food products (Brands et al., 2005;

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Davies et al., 2004; de Freitas Neto, Penha Filho, Barrow, & Berchieri Junior, 2010; Foley, Johnson, Ricke, Nayak, & Danzeisen, 2013; Foley et al., 2011; Hanning, Nutt, & Ricke, 2009; Heaton & Jones, 2008; Heinitz, Ruble, Wagner, & Tatini, 2000; Lynch, Tauxe, & Hedberg, 2009; MartinezUrtaza, Peiteado, Lozano-Leo´n, & Garcia-Martin, 2004; Pires, Viera, Hald, & Cole, 2014; Rajashekara et al., 2000; Ricke, 2017). The infections caused by Salmonella represent a considerable cost to the US economy annually (McClinden, Sargeant, Thomas, Papadopoulos, & Fazil, 2014; Scharff, 2012), and it is estimated that over 1 million people annually contract Salmonella in the United States (Scallan et al., 2011). Despite some success in limiting Salmonella in the past few years, it remains a fairly prevalent foodborne pathogen. In general, foodborne pathogenic bacteria can grow rapidly in temperatures ranging from 5°C (40°F) to 60°C (140°F), and this temperature zone is referred to as the “danger zone” (United States Department of Agriculture Food Safety and Inspection Service, 2013). Controlling temperature of food to avoid this danger zone is a traditional measure to ensure food safety and to extend the shelf life of food by limiting microbial growth. Foods such as fresh produce, animal carcasses, and their corresponding products are typically required to be chilled to lower temperatures throughout food processing mainly during storage, transportation, and distribution (Archer, 2004; Buncic & Sofos, 2012; Galiş et al., 2013; Guillard, MauricioIglesias, & Gontard, 2010; Hanning et al., 2009; McDonald & Sun, 2000; Russell, 2002). Some procedures are performed at cold temperatures, such as cooling and/or freezing, to serve as preservation processes for effectively reducing the bacterial burden of contaminated food (Dinc¸er & Baysal, 2004; Loretz, Stephan, & Zweifel, 2010). Though these preservation procedures using cold temperature are effective in limiting bacterial growth, exposure to low temperatures can also lead to some concerns in regards to cold adaptation, cross-protection, and unexpected modification of food-associated microorganisms composed predominantly of spoilage microorganisms and foodborne pathogens (Abee & Wouters, 1999; Alzamora, Tapia, & Chanes, 1998; Beales, 2004; Berry & Foegeding, 1997). To better apply control measures with cold temperature, an in-depth understanding of bacterial behavior and the corresponding response when they are exposed to cold environments are essential. There is limited mechanisms-based information on specific cold stress responses of Salmonella, research on survival, injury, and growth of Salmonella in cold temperatures. This review includes an overview of studies

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investigating general mechanisms associated with bacterial cold stress responses, including cell membrane modification, DNA topology, transcriptional and translational responses with a discussion on cold-induced protein (CIP) synthesis. In addition, the physiological and genetic responses of Salmonella in food products held at cold temperatures will be discussed, and implications related to pathogenesis will be described.

2. MOLECULAR MECHANISMS TO COUNTER COLD SHOCK 2.1 General Concepts on Environmental Stress During the life cycle of a foodborne pathogen in food production such as Salmonella, it typically encounters a multitude of less than optimal if not downright hostile environmental conditions. This includes environments that are prevalent during live animal production, transportation, at the processing plant, retail, and homes of consumers. The types of harsh environments that Salmonella and other pathogens can encounter during food production include a wide range of physiologically challenging factors such as low water activity/ desiccation, high osmolarity, low pH/high acid concentrations, presence of a variety of antimicrobials, and low nutrient availability leading to starvation, just to name a few (Boor, 2006; Foster, 1999; Gyles, 2008; Park et al., 2008; Ricke, 2003a, 2003b; Ricke, Kundinger, Miller, & Keeton, 2005; Rowley, Spector, Kormanec, & Roberts, 2006; Spector, 1998). Not surprisingly, most organisms possess several mechanism(s) that enable them to counter these stresses whether they occur suddenly or more gradually allowing the organism to transition to the most challenging environmental condition. Certainly, temperature extremes outside optimal growth requirements whether thermal or cold are a challenge to organisms such as Salmonella and have been detailed over the past decades (Barria, Malecki, & Arraiano, 2013; Dawoud et al., 2017; Eriksson, Hurme, & Rhen, 2002; Gualerzi, Giuliodori, & Pon, 2003; Jarvis et al., 2016; Panoff, Thammavongs, Gu
eguen, & Boutibonnes, 1998; Ramos et al., 2001; Russell, 1990; Singh, Sarin, & Tandon, 1997; Thieringer, Jones, & Inouye, 1998). Such environmental conditions represent stress to the organism and most microorganisms including Salmonella have the capability to counter with an array of resistance and tolerance mechanisms.

2.2 Cold Stress: Physiological Responses For organisms such as Salmonella, sudden encounters with cold temperatures that occur with refrigeration and freezing in food processing/storage

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represent a major physiological challenge to the organism. This exposure results in a halting of growth, adaptation for survival, followed by renewal of growth under the reduced ambient temperatures (Gualerzi et al., 2003). In general, bacterial cells exposed to cold or low temperature depending on the microorganism’s optimal growth temperature, go through three stages (Thieringer et al., 1998; Weber & Marahiel, 2003). The first stage is the transient response immediately after the exposure is known as acclimatization postshock phase and the time duration for this response may vary with regards to growth rate reduction and the gene expression and subsequent synthesis of proteins for cold survival response. The cells next enter the second stage known as a recovery phase, with bacterial cells growing more rapidly and gradually resuming cellular protein biosynthesis. In the last stage, the cells become permanently adapted to cold temperature with gene expression modification, and this occurs when the bacterial cells reach stationary growth phase. At lowered temperatures occurring during cold shock, transcriptional and translational processes are essentially leading the ribosome to become ineffective followed by inadequate protein folding along with cellular protein biosynthesis decreases, and eventually a potentially adverse influence on growth rate (Chattopadhyay, 2006; Ermolenko & Makhatadze, 2002; Phadtare, 2004). Physiologically, adaptation to these harsh temperatures is manifested in several ways, and these mechanisms have been summarized by Barria et al. (2013). As expected membrane integrity is impacted by a sudden decrease in external temperatures and part of the adaptation adjustment elicited by the bacterial cell is to adjust the membrane composition by desaturating fatty acids to optimize the fluidity for growth at lower temperatures (Thieringer et al., 1998). Intracellularly, bacterial cells adjust their transcription and translation functions in the presence of lower temperatures by optimizing RNA processing in conjunction with changes in DNA supercoiling and continued transcription of cold-induced genes and production of cold-inducible proteins (Barria et al., 2013). Once cold temperature adapted, bacterial cells begin growing again, and CIPs decrease as growth-related protein synthesis resumes (Barria et al., 2013). Bacteria can also protect cellular functions by accumulating low molecular weight solutes, including glycine betaine, carnitine, and trehalose among others to retain the integrity of cell proteins exposed to external stresses such as cold temperatures which Shivaji and Prakash (2010) referred to collectively as “chemical chaperones.”

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2.3 Cold Shock Response: Molecular Profiles Several transcriptional analysis (gene expression) studies of the Escherichia coli cold shock responses have been conducted leading to the detection of the primary cold shock proteins (CSPs) and other genes that are involved in this response coming from different categories of functional groups such as motility-associated genes (flagellar-coding genes), and proteins of sugar metabolism and transport. The CSPs, CspA, CspB, CspG, and CspE, are mainly expressed at the acclimation phase. A study by White-Ziegler et al. (2008) conducted a microarray analysis on E. coli K-12 MC4100 and demonstrated that approximately 7% of the genome (297 genes) exhibited increased expression at low temperature (23°C) in comparison to their optimal growth temperature of 37°C. Of those genes, 122 genes (41%) are under the regulation of the general stress response rpoS. Proteins expressed by the genes, otsA and otsB, respectively, revealed the synthesis of the osmoprotectant, trehalose that plays a role in improving cell viability at cold shock conditions. In particular, 107 genes (36%) were not specifically related to any COG (Clusters of Orthologous Groups) functional group and roughly 50% (149 genes) of the increased expressed genes at low temperature were either hypothetical or with unknown functions signifying the need of more research to understand the adaptation of microorganisms to low/cold temperature. Responses to cold shock for Salmonella have been documented and characterized to some extent. Using both global proteome and gene expression profiling, Shah, Desai, Chen, Stevens, and Weimer (2013) identified the primary and significant genes expressed by Salmonella Typhimurium during cold stress exposure as being cspA, cspB, cspC, cspD, and cspE, commonly referred to as CSPs. Fifty-seven ribosomal-associated proteins were detected in the profile analysis after the cold stress with 44 (77%) of the expressed proteins persisting throughout cold stress. The genes recA and ssB that are involved in recombination, SOS response, and repair, were among the genes significantly expressed during cold stress. They are known to regulate the expression of numerous genes of membrane biogenesis and transcription. Other genes significantly induced due to cold stress belonged to various functional groups, such as oxidative stress, amino acid transport and metabolism, tricarboxylic acid cycle, and complex I (NADH dehydrogenase of electron transfer chain). Functions and details of the genes that most likely contribute directly to cold shock will be discussed in the following sections in general terms and where pertinent, Salmonella specifically.

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2.4 Cell Membrane Modification The microbial cell membrane is the first cellular barrier of the external environment. In general, the membrane consists mainly of fatty acids that adjust and maintain membrane fluidity. Bacterial adaptation to cold shock/stress produces some cellular changes at different levels from the cell membrane that serves as an initial sensing barrier to the DNA encoding the genetic information (Panoff et al., 1998; Phadtare, 2004; Shapiro & Cowen, 2012). A sudden temperature downshift leads to decreased membrane fluidity and as a result, disrupts its function. Under these conditions, the membrane fluidity can revert from its liquid-phase state to more of a gel-phase state if left unchecked. To retain membrane fluidity in response to cold shock, Shivaji and Prakash (2010) stated that bacterial cells can change the quantities of saturated and unsaturated fatty acids, modify the chain length of fatty acids, adjust the cis to trans fatty acid and anteiso to iso fatty acid proportionalities, as well as adjust membrane protein quantity and modify concentrations of carotenoid types. Marr and Ingraham (1962) observed an increase of unsaturated fatty acids synthesis in cell membrane with fatty acid isomerization modifications when E. coli was exposed to low temperature. The content of unsaturated fatty acids is synthesized through three enzymes FabA, FabB, and FabF, of which fabF is the main gene encoding a beta-ketoacyl-acyl carrier protein synthase II with increased activity of Fabf at low temperature (Mansilla, Cybulski, Albanesi, & de Mendoza, 2004). Sinensky (1974) also documented this mechanism in E. coli and suggested a homeostatic process that regulates the viscosity of membrane phospholipids (Chattopadhyay, 2006; Los & Murata, 2004). The genetics of regulation of these alterations in desaturation of membrane fatty acids has been characterized to some extent. Based on their previous work with the cyanobacterium Synechocystis (Los, Horvath, Vigh, & Murata, 1993; Vigh, Los, Horvath, & Murata, 1993), Los and Murata (2004) have pointed out that the genetic control of the enzymes involved in fatty acid desaturation appears to be responsive to the temperature shift extent and not the absolute temperature. While fatty acid desaturation mechanisms have been well documented, certain bacteria may emphasize different mechanisms to alter membrane composition in response to cold temperature shock (Los & Murata, 2004). Specific Salmonella cell membrane compositional changes in response to cold temperatures have been documented as well. Wollenweber, Schlecht, Luderritz, and Riftschel (1983) compared the fatty acid composition of the

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lipid A component of lipopolysaccharide in S. Typhimurium or S. Minnesota recovered after growth at either 37°C or 12°C under an aerobic atmosphere in a complex medium. They identified the fatty acid and unsaturated fatty acids in these serovars using gas–liquid chromatography and gas–liquid chromatography/mass spectrometry, respectively. In response to the lower temperature presumably as a means to alter membrane fluidity, the authors observed a decrease in hexadecanoic and dodecanoic acids, the disappearance of 2-hydroxytetradecanoic acid, and an increase in tetradecanoic acid, accompanied by the emergence of a new fatty acid, palmitoleic acid in lipid A mostly as a replacement of dodecanoic acid. Growth phase and differences in membrane composition may be a factor as well. For example, Kim et al. (2005) using gas chromatography/mass spectrometry determined that cyclopropane fatty acids increased in S. Typhimurium upon initiation of stationary phase. By generating cyclopropane synthase gene mutants which became acid sensitive, the authors demonstrated that cyclopropane modification of the membrane phospholipids imparted acid resistance to stationary phase S. Typhimurium. Whether such modifications would elicit cold shock resistance in stationary phase Salmonella would be of interest, particularly when food is stored at refrigeration temperatures or frozen. It is conceivable since the Salmonella alternative sigma factor RpoS which is generally induced as a stress-response gene activator during stationary phase influences cyclopropane fatty acid production is also known to be involved in survival of Salmonella during refrigeration particularly at high salt concentrations (Boor, 2006; Kim et al., 2005; McMeechan et al., 2007).

2.5 DNA Supercoiling Modification DNA characteristics (structure and shape) have an impact on DNA functions. DNA supercoiling is the shape of DNA packed inside viable cells in a very high DNA helix coiled with interwound supercoiling in prokaryotic organisms. The state of DNA supercoiling can be either positive “overtwist” or negative “unwind” (Mirkin, 2001). DNA supercoiling has been shown to play numerous roles in genome functions with the resulting changes in chromosomal topology generating a global impact on the respective gene expression in the corresponding bacterial cell (Cameron, Stoebel, & Dorman, 2011; Dorman, 1991, 2006). It assures that DNA is not damaged through the integration of DNA chains as a requirement for replication, initiation, transcription, and recombination (Mirkin, 2001).

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DNA topoisomerases are the enzymes which function in all DNAassociated topological states including DNA supercoiling. Negative DNA supercoiling state is regulated by DNA gyrase and topoisomerase IV, while positive DNA supercoiling is regulated by topoisomerases I and III (Lo´pezGarcı´a, 1999; Terekhova, Gunn, Marko, & Mondrago´n, 2012). In each DNA supercoiling state, the enzymes function to relax negative to positive supercoiling and vice versa (Champoux, 2001). As described in detail elsewhere (Cameron et al., 2011; Dorman, 1991, 2006; Hatfield & Benham, 2002; Travers & Muskhelishvili, 2005), DNA supercoiling in pathogenic bacteria such as E. coli and Salmonella is extensively influenced by environmental conditions. However, despite their similarities, these two organisms do appear to differ in their DNA supercoiling responses. Cameron et al. (2011) characterized DNA supercoiling in E. coli and Salmonella enterica under exponential and stationary growth phase conditions as well as their respective responses to osmotic stress and exposure to novobiocin. Based on comparisons of the DNA topology of the two organisms, the authors concluded that S. enterica was much less variable in changing the level of DNA supercoiling under these growth and environmental conditions than E. coli. Furthermore, the FIS (factor for inversion stimulation) protein that regulates DNA supercoiling exhibited less impact in S. enterica than E. coli. The association of DNA negative supercoiling and cold temperature has been previously demonstrated (Prakash et al., 2009; Shivaji & Prakash, 2010). When DNA supercoiling increases in its negative state, it indicates that DNA gyrase and topoisomerase IV were induced at high levels to effectively maintain the cellular functions of DNA replication, transcription, and recombination (Mizushima, Kataoka, Ogata, Inoue, & Sekimizu, 1997; Shapiro & Cowen, 2012).

2.6 CIP Synthesis When cells are shifted to cold temperatures, numerous proteins are upregulated in response to the cold shock. They are designated as CSPs, CIPs, and cold acclimatization proteins (CAPs). The first two groups can accumulate and become associated with most of the housekeeping genes being repressed following the cold temperature exposure. It has been suggested that CSPs are small expressed proteins with sizes less than 10kDa and CSPs larger than that should fall within the CIP group. However, CAPs are proteins characterized by very high synthesis occurring primarily during extended exposure and subsequent growth at cold temperature

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(Hebraud & Potier, 1999; Neuhaus, Rapposch, Francis, & Scherer, 2000; Panoff et al., 1998; Phadtare, 2004; Polissi et al., 2003). CSPs are small response proteins involved in several molecular functional activities, such as DNA replication, transcription, translation, and other mechanisms yet to be identified (Golovlev, 2003). Collectively, they are referred to as nucleic acid chaperones and they essentially act to inhibit secondary RNA structure formation (Barria et al., 2013). These proteins have been identified as being conserved in numerous Gram-positive and -negative bacteria sharing a similarity of more than 45% with CSP families with some consisting of up to nine members. In some bacteria, these csp genes are organized in chromosomal clusters (Neuhaus, Francis, Rapposch, G€ org, & Scherer, 1999; Wouters et al., 1998; Yang et al., 2009). Other cold-associated proteins, CIPs vary in numbers from bacterial species to another, and Barria et al. (2013) have summarized a list of these proteins along with functions in their review. Over 25 cold-induced genes have been described previously (Barria et al., 2013; Phadtare & Severinov, 2010). The following sections will briefly touch on some of these proteins and which have been characterized in Salmonella. 2.6.1 Cold Shock Proteins Cold shock genes generate a group of proteins, collectively designated as Csp proteins, some of which have been better characterized from a functional standpoint than others. Based on these in-depth characterizations, definitive cold shock mechanistic properties can be established that conform with what is generally known about bacterial responses to cold shock at the cellular level. In E. coli, the Csp group consists of nine known proteins with genes for proteins CspA, CspB, CspG, and CspI being considered cold shock inducible (Bae, Xia, Inouye, & Severinov, 2000; Giuliodori et al., 2010; Yamanaka, Fang, & Inouye, 1998). The CspA protein is considered the most extensively studied of all CSPs, and much of what is known is based on studies with E. coli. The protein consists of 70 amino acids and can bind either single-stranded DNA or mRNA, thus acting as a gene-expression regulator potentially impacting both transcriptional and translational properties of the bacterial cell. In addition, it possesses the ability to bind mRNA by acting as a chaperone, thus forcing RNA into a single-stranded form, and subsequent degradation (Barria et al., 2013). Two genes, gyrA and hns, are transcriptionally activated by CspA by stabilizing the RNA polymerase (Jones, Krah, Tafuri, & Wolffe, 1992; La Teana et al., 1991; Panoff et al., 1998). GyrA and H-NS have

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previously been demonstrated to be involved in the negative DNA supercoiling (Gualerzi et al., 2003; Phadtare & Severinov, 2010; Stella, Falconi, Lammi, Gualerzi, & Pon, 2006). Early work by Fang, Jiang, Bae, and Inouye (1997) using mutational substitution analyses of the cspA gene in E. coli demonstrated that the cspA gene is constitutively transcribed at 37°C, but the resulting RNA is unstable at the higher temperature, thus preventing translation into a functional protein. Instead, cspA RNA becomes stable as the temperature is lowered to 37°C and resulting in a fully functional CspA protein (Fang et al., 1997). In more recent studies, Giuliodori et al. (2010) expanded on this concept of changes in RNA structural integrity by demonstrating that the cspA mRNA structures were not only different at 37°C compared to their corresponding counterparts at cold temperatures, but that this was probably due to stabilization of an RNA intermediate at the low temperature. In addition, they were also able to show that the cspA mRNA was more efficiently translated at the colder temperatures. As an overall conclusion, they proposed that the cspA mRNA served as some form of thermosensor that could detect temperature downshifts and contained components that improved translational efficiency at these lower temperatures. Bae et al. (2000) demonstrated that CspA-family proteins also function as CSPs at the transcriptional level by serving as transcription antiterminators. Using a combination of in vitro addition of the respective Csp proteins and in vivo overexpression of cloned Csp proteins in E. coli incubated at 37°C, they concluded that CspA, CspC, and CspE could induce transcription of nusA, infB, rbf, and pnp genes via antitermination, thus suggesting that cold shock activation of these genes occurs by transcription antitermination. Salmonella possesses several of the Csp proteins known to occur in E. coli, and some of these have been characterized. Jeffreys, Hak, Steffan, Foster, and Bej (1998) noted that S. Enteritidis could survive freezing temperatures for increased periods of time if initially exposed to 10°C. Further characterization by Jeffreys et al. (1998) using Western blotting with an E. coli CspA antibody and identification of radiolabeled proteins in cold shocked S. Enteritidis led to the isolation of a protein that was similar in size and promoter nucleotide sequences as its counterpart in E. coli. However, the authors concluded that sufficient differences in sequences in other regions of the gene could explain its expression in S. Enteritidis under less stringent temperatures. In a follow-up study with S. Typhimurium using similar approaches, Horton, Hak, Steffan, Foster, and Bej (2000) identified a CspA protein in this serovar as well, but unlike S. Enteritidis induction required a

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substantial decrease in temperature for induction of the S. Typhimurium cspA gene to occur. Salmonella serovar differences in responses to stresses and other physiological functions are not surprising and have been noted when different serovars and in some cases even the individual strains of the same serovar are exposed to certain environmental conditions or exhibit different infectious phenotypes (Andino & Hanning, 2015; Gonza´lez-Gil et al., 2012; Heithoff et al., 2012; Ricke, 2017; Shah, 2014; Shah et al., 2012). Other Csp proteins have been identified and characterized in Salmonella. Craig, Boyle, Francis, and Gallagher (1998) constructed a series of S. Typhimurium Mudlux gene fusion insertion mutants and isolated a series of lux expression mutants that were luminescent at different rates as the temperature was dropped from 30°C to 10°C. From this set of mutants one mutant was isolated that responded with a high level of induction at 10°C and was identified as cspB next to the umuDC operon. Further characterization revealed that luminescence could only be detected at 22°C or below and the cspB mRNA proved to be stable at 10°C but destabilizes as the temperature was increased. This is consistent with the later observations made for E. coli cspA mRNA and corresponds to an RNA-based thermal sensing role for these the mRNA generated from these csp genes. Not all Csps in Salmonella exhibit this pattern. For example, Kim et al. (2001) examined the expression of the cspH gene in S. Typhimurium and found that it was activated at 37°C and its mRNA was more stable than other csp mRNAs at this temperature. They confirmed this with cspH–lacZ gene fusion constructs that demonstrated that lacZ expression was also induced at 37°C. Based on these results, they concluded that the S. Typhimurium cspH gene possesses a broad temperature range (30–10°C) for induction and can respond to relatively small changes in external temperature. In a follow-up study Kim et al. (2004) further demonstrated that cspH induction occurred during early log phase growth. They observed an increase in cspH when stationary phase S. Typhimurium cells were given a nutrient upshift at 37°C, but not in the presence of a gyrase inhibitor or in a fis-deficient mutant. More recently, Morgan, Wear, McNae, Gallagher, and Walkinshaw (2009) structurally characterized the CspE protein from S. Typhimurium by crystallizing purified protein and conducting X-ray crystallography analyses of the protein structure. The authors concluded that the three-dimensional model of the S. Typhimurium CspH protein analyzed in their study proved to be similar to the structure of other previously characterized Csps.

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2.6.2 CsdA Cold-shock DEAD box protein A (CsdA), previously known as “DeaD,” is one of five members of the DEAD-box family, a branch of the helicases superfamily 2 (Kaberdin & Bl€asi, 2013). This protein is involved in several cellular mechanisms, including ribosome biosynthesis, translational initiation, and mRNA decay by stabilizing the cspA mRNA for the major cold shock protein A (CspA). During cold shock conditions, it binds the RNA degradosome with RNase E and is required for riboregulation of rpoS mRNA (Horne, Kottom, Nolan, & Young, 1997; Kaczanowska & Ryd
enAulin, 2007; Peil, Virum€ae, & Remme, 2008; Shajani, Sykes, & Williamson, 2011; Weber & Marahiel, 2003). Limited work on CsdA has been conducted on Salmonella. Li, Meng, Wang, and Sun (2012) used an mRNA differential-display reverse transcription—polymerase chain reaction (PCR) approach to screen for genes involved in viable nonculturable (VBNC) Salmonella Pullorum. Their interest stemmed from the need to detect this particular serovar in its VBNC state because of its poultry infection capability even when it was not recoverable in traditional culturing methods. They transferred 37°C grown S. Pullorum cells into medium held at 4°C to generate VBNC physiological state and used mRNA differential amplification to screen for cDNA fragments only present in the VBNC cells. Based on sequence analyses of the isolated cDNA that was unique to the VBNC cells they aligned this fragment with an ATP-dependent RNA helicase rh1B gene and contained conserved regions of the DEAD-box helicase. They concluded that the rh1B gene potentially functioned in cold shock survival in a similar manner as the DEAD-box RNA helicases described previously by Cordin, Banroques, Tanner, and Linder (2006). Their proposed use of this gene as a marker for detection of VBNC S. Pullorum could potentially be applied to foodborne Salmonella that are in a VBNC physiological state during refrigeration or frozen storage. 2.6.3 NusA The NusA protein is a component of an antitermination complex and induced earlier at DNA transcription to bind RNA polymerase and influences pausing and/or termination of transcription. It also influences transcriptional antitermination and stabilizes the RNA polymerase process. It was identified to be induced under cold temperature conditions (Bae et al., 2000; Mah, Kuznedelov, Mushegian, Severinov, & Greenblatt, 2000). In Salmonella,

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the NusA protein may impact pathogenesis as well. Van Immerseel et al. (2008) used transposon mutagenesis to identify S. Enteritidis genes potentially involved in direct or indirect transcriptional regulation of the hilA gene that encodes the transcriptional activator of Salmonella Pathogenicity Island-1 and nusA was identified as one of the genes that impacted hilA expression. They noted that deletion of the nusA gene caused reduction in hilA expression and they speculated that this could have resulted from the inefficient HilA protein translation or of the hilA regulators but the interactions of other potential factors precluded definitive conclusions. 2.6.4 DnaA The dnaA gene which encodes for DnaA protein is considered a coldinducible protein and possesses both DNA binding/replication initiator properties and acts as a global regulator of transcription (Barria et al., 2013; Gualerzi et al., 2003). The DnaA protein is centrally involved in the initiation of chromosomal and mini-chromosomal DNA replication on oriC and appears to be important in the timing control of cell-cycle initiation (Atlung, Clausen, & Hansen, 1985; Messer & Weigel, 1997). It also autoregulates the dnaA gene and influences cell membrane structural properties (Atlung et al., 1985; Atlung & Hansen, 1999; Braun, O’Day, & Wright, 1985; Kaguni, 2006; Messer & Weigel, 1997; Wegrzyn & Wegrzyn, 2002; Węgrzyn, Wrobel, & Węgrzyn, 1999). Messer and Weigel (1997) have summarized the role of DnaA protein as a transcription factor which depending on the target gene promoter location can serve as a transcriptional activator, repressor, or terminator. Atlung and Hansen (1999) concluded that DnaA was involved in cold shock after demonstrating the levels of DnaA protein when E. coli was shifted from 37°C to 14°C were twofold higher even though there were indications some of the synthesized protein was irreversibly inactive or that all present at the lower temperature generally exhibited irreversible low activity. Less is known about DnaA in Salmonella, but when the dnaA sequences were compared between E. coli and S. Typhimurium they were relatively homologous and functionally were presumed to behave in a similar fashion by the authors (Skovgaard & Hansen, 1987). Further work on regulatory mechanisms associated with Salmonella dnaA has been done more recently. When Dadzie et al. (2013) conducted transcriptomic deep sequencing profiles of S. Typhi they identified a cis-encoded antisense RNA expressed primarily during stationary phase and contributed to the stability of dnaA mRNA. Expression of this antisense RNA was also observed in the presence of iron limitation and osmotic stress but cold shock was not examined in this study.

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2.6.5 RecA When Shah et al. (2013) exposed S. Typhimurium to 5°C cold stress, they detected induction of the RecA protein. RecA is considered a CSP that is involved in the recombination and the SOS response for DNA repair (Barria et al., 2013; Gualerzi et al., 2003; Jones & Inouye, 1994). The SOS response occurs when RecA inactivates LexA and as a result over 31 genes are upregulated. In addition, the elevated amount of active RecA in the cytoplasm can associate them with the membrane (Han & Lee, 2006; Lee & Lee, 2003). RecA is also essential for flagellar-driven swarming behavior in E. coli and Salmonella (Gomez-Gomez, Manfredi, Alonso, & Blazquez, 2007; Mayola et al., 2014; Medina-Ruiz et al., 2010). Mayola et al. (2014) in a series of mutant fusion studies along with microfluidic and chemotaxis capillary assays established a direct link between S. Typhimurium RecA, chemotaxis, and flagellar rotation switching. This led them to suggest that Salmonella RecA is involved in swarming and chemotaxis. Whether Salmonella swarming behavior and flagellar motion would be influenced by changes in RecA production during cold shock is not known, but Shah et al. (2013) did not observe an intense-induction response of the S. Typhimurium CheY protein (flagellar rotational regulator) in response to cold stress. 2.6.6 Trigger Factor The trigger factor (TF) protein in E. coli (peptidyl prolyl isomerase) has been identified as a molecular chaperone to correct protein folding and hydrolyze misfolded polypeptides (Phadtare, 2004). The tig gene is induced by multiple stresses and is involved in ribosome binding. It is induced under cold shock conditions and has a role in improving the cellular viability of E. coli when temperature falls between 4°C and 16°C where the level of TF protein increases significantly (Kandror & Goldberg, 1997). In addition, the protein is involved in cotranslational proteins folding and sustains the exportation of proteins in a structurally efficient state through the support of the colddamaged proteins refolding (Barria et al., 2013; Han & Lee, 2006; Phadtare & Severinov, 2010). Shah et al. (2013) observed considerable induction of the tig gene which encodes TF in S. Typhimurium during cold-stress exposure. However, Di Pasqua, Mauriello, Mamone, and Erclolini (2013) using quantitative reverse transcription—PCR observed reduced expression of tig in S. Thompson and downregulation of the TF protein upon exposure to 15°C leading them to suggest that this cold acclimation protein was not involved in cold-stress adaptation. It is possible that TF is less important for cold-stress adaptation in some Salmonella serovars

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than others given the serovar differences know to occur in genetic responses to other stresses (Andino & Hanning, 2015; Gonza´lez-Gil et al., 2012). There may be a temperature gradient impact as well since Shah et al. (2013) used 5°C cold shock vs 15°C by Di Pasqua et al. (2013). More quantitative comparisons need to be made across serovars to assess whether TF is serovar specific for cold stress responses and examined over a range of incremental cold temperature differences. 2.6.7 RbfA Ribosome-binding factor A is a CSP that is essential for efficient translation (16S rRNA processing and 30S ribosomal subunit) and cell growth at cold temperature (Barria et al., 2013). The RbfA protein initially was characterized as a multicopy suppressor of a cold sensitive 16S rRNA mutation (Dammel & Noller, 1995; Weber & Marahiel, 2003). The rbfA mRNA has a section containing an A/T rich sequence downstream where the start codon is known as a translation-enhancing element. In cold-shock mRNAs, it has been recognized as a translation initiation enhancement factor (Barria et al., 2013; Kaczanowska & Ryd
en-Aulin, 2007; Phadtare & Severinov, 2010; Qing, Xia, & Inouye, 2003; Shajani et al., 2011). 2.6.8 PNPase This enzyme, polynucleotide phosphorylase (PNPase), is encoded by the pnp gene (Phadtare & Severinov, 2010). It is a major E. coli degradosome element with a 30 -to-50 exonuclease mainly involved in RNA metabolism. PNPase activity has been demonstrated to be significantly essential at cold-induced conditions for cell survival and growth (Haddad et al., 2009; Hu, McCormick, Means, & Zhu, 2014; Mathy, Jarrige, Robert-Le Meur, & Portier, 2001). In addition, it is induced at a posttranscriptional stage and is autoregulated with a role in inhibiting translation and stabilizing mRNA. Furthermore, it suppresses the CSPs family production at the end of the acclimation phase (Barria et al., 2013; Kaberdin & Bl€asi, 2013; Phadtare & Severinov, 2010). In addition to cold adaptation, the PNPase protein may have additional functions in Salmonella (Clements et al., 2002; Ygberg et al., 2006). For example, Clements et al. (2002) used mouse studies and microarray analyses to demonstrate that S. Typhimurium PNPase impacted pathogenicity islands 1 and 2 virulence genes, altering acute vs persistent infection and negatively controlling spv virulence gene expression (Ygberg et al., 2006). More recently, it has been shown by Bearson, Bearson, Lee, and Kich (2013) to also be required for S. Typhimurium colonization of swine.

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2.6.9 KsgA The KsgA protein is a dimethyl adenosine transferase (a 16S rRNA adenine methyltransferase in E. coli). The ksgA gene is critical at cold-induced temperatures for cell growth rate and is a regulator of ribosome biogenesis (Kaczanowska & Ryd
en-Aulin, 2007; Shajani et al., 2011; ZhangAkiyama et al., 2009). While KsgA appears to be important in cold adaptation for E. coli, Chiok, Addwebi, Guard, and Shah (2013) did not detect an impact on growth response in a KsgA deficient S. Enteritidis mutant when exposed to suboptimal temperature, and this mutant did not appear to exhibit a cold-sensitive phenotype. However, these authors did observe increased susceptibility to high osmolarity, chloramphenicol, oxidative stress in this mutant and they concluded that KsgA might play a role in intestinal colonization and organ invasion of chickens. Whether similar responses occur in other Salmonella serovars remain to be determined. 2.6.10 SrmB The SrmB protein is a member of the DEAD-box family of the helicases superfamily 2 (Kaberdin & Bl€asi, 2013; Khemici & Linder, 2016). It was first isolated by Nishi and Schnier (1986, 1988). It plays a role in ribosome biogenesis mainly for the assembly of the 50S ribosomal subunit. It has been shown that SrmB is involved at the ribosomal biogenesis level in advance of CsdA. At cold temperatures, it causes a defect in cell growth when deleted and is overexpressed in the wildtype strain of E. coli. In addition, it was proposed that this protein possibly operates as an ATP-independent RNA chaperone (without the energy source of ATP hydrolysis) and interacts with 23S ribosomal RNA subunit (Kaczanowska & Ryd
en-Aulin, 2007; Phadtare & Severinov, 2010; Shajani et al., 2011). In their review, Khemici and Linder (2016) concluded that it needs to be worked out before fully understanding the molecular functioning of these DEAD-box proteins. If and/or how Salmonella utilizes these DEAD-box family of helicase proteins such as SrmB during cold shock remains to be determined. 2.6.11 Initiation Factors (IFs) The initiation factor 2, encoded by the infB gene is involved in the initiation of bacterial translation with GTPase activity (Jones, VanBogelen, & Neidhardt, 1987; Laursen, Sørensen, Mortensen, & Sperling-Petersen, 2005). This protein in concert with two other factors, IF1 and IF3, directs the selection of the 30S subunit of initiator tRNA and mRNA translation initiation region to form the “30S preinitiation complex” and initiates the process (Laursen, Mortensen, Sperling-Petersen, & Hoffman, 2003).

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Laursen et al. (2005) have stated that all three translation initiation factors could be involved in cold shock regulation based on data summarized by Gualerzi et al. (2003) that indicated a doubling of their stoichiometry with respect to the ribosomes during cold shock exposure. Upregulation of IF2 has been reported for cold shocked E. coli and was proposed to result from CspA and the other cold shock-induced Csp protein’s ability to facilitate transcription antitermination (Bae et al., 2000; Laursen et al., 2005). Presumably, Salmonella IFs would behave in the same fashion, but this has not been clearly established. Early work using an immunoblotting approach to compare E. coli with S. Typhimurium suggested that IF2 and IF3 were structurally similar between the two bacteria (Howe & Hershey, 1984). More recently, Pavlov, Zorzet, Andersson, and Ehrenberg (2011) compared IF2 amino acid sequences between S. Typhimurium and E. coli and reported that they were greater than 96% identical and behaved nearly the same in the in vitro initiation translation system they used for their studies. Shah et al. (2013) reported some increase in expression of the S. Typhimurium infC gene product (encodes IF3 protein) under cold shock conditions, particularly late in the incubation period when compared to noncold shock conditions. As is the case with other CIPs, more definitive work will need to be done with other Salmonella serovars in the presence of cold temperatures to elucidate how universal these cold shock response systems are in Salmonella.

3. SALMONELLA–COLD SHOCK INTERACTION WITH OTHER STRESS RESPONSES 3.1 Cross-Protection During food processing, foodborne pathogens are exposed to numerous stresses that possibly have a major influence on microbial global stress systems and at least in some cases lead to adaptation where the organism becomes more virulent and/or resistant to multiple stressors (Archer, 1996). Consequently, depending on the interventions being employed it may become possible for a foodborne pathogen to experience cross-protection when it becomes tolerant/resistant to multiple hurdles and become a challenge for the food industry to control (Ricke et al., 2005). It has been confirmed in a variety of research studies over the years that an improvement in tolerance and resistance of a microorganism can occur when they are exposed to other subsequent stresses (Rangel, 2011).

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The development of cross-protection in Salmonella is known to occur in the presence of cold temperatures. For example, in a study by Xu, Lee, and Ahn (2008), the authors evaluated the cross-protective capacity of acidadapted S. Enteritidis strain to resist cold stress and concluded that acidshocked cells for a period of 2 h were more resistance to cold stress than a longer acid shock for 7 h. In addition, they observed that acid-adapted S. enterica cells can be present in the VBNC state that requires the resuscitation for the transition to the culturable state. This outcome could very well have physiological significance as acids are extensively applied in the food industry both directly as antimicrobial preservatives and generation of organic acids via fermentation of various food products (Ricke, 2003b). Previously, it has been shown that S. Typhimurium upon prior exposure to organic acids can become tolerant to inorganic acid shock as well as nonacid stressors such as hydrogen peroxide and high osmolarity (Kwon, Park, Birkhold, & Ricke, 2000; Kwon & Ricke, 1998). A more recent study by Shah et al. (2013) simulated the conditions by which Salmonella cells are exposed to cold temperatures used in storing foods and subsequently consumed followed by exposure to acidic–gastric conditions. They tested the response of S. Typhimurium LT2 strain for various stresses (peroxide, osmotic, and acid (pH 5.3) for a time period of 30 min (shock) and 5 h (stress)). They noted that only peroxide shock critically decreased cellular survival indicating a potential capacity of this foodborne pathogen to endure harsh environmental stresses for several hours mainly during transit and inside the host. Proteomic profiles indicated that 104 proteins were expressed during exposure to cold stress. They were divided into three categories as information storage and processing, cellular processing, and metabolism.

3.2 Interaction With Virulence Responses In addition to cross-protection to other antimicrobials, exposure to certain environmental stressors associated with the food industry can also lead to enhanced pathogenesis (Archer, 1996). One of the earliest studies conducted in evaluating the pathogenicity of Salmonella after freezing was by Sorrells, Speck, and Warren (1970). They used a S. Gallinarum cell suspension and froze it at 75°C in a bath of dry ice acetone followed by storage at 20°C for 1 day. This treatment yielded three kinds of cells, dead, metabolically injured, and undamaged cells. They compared freezing the cell suspension at 75°C as the sole condition and after storage at 20°C for 1 day.

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They evaluated the pathogenicity of uninjured and frozen sublethally injured cells by injecting a 1 mL cell suspension into the peritoneum (the body cavity) of 6-week-old chicks (180 chicks, 18 groups, 10 chicks in each group). They concluded that the differences between the two treatments were not statistically significant. This demonstrated that metabolically injured cells after preservation by freezing were capable of recovering when conditions were favorable and could potentially cause infections (Sorrells et al., 1970). The process of causing an infection is complicated and involves several steps in bacterial pathogenesis. Critical steps of infection are adherence and invasion to host cells. Two main bacterial adhesions are fimbriae (pili) (type 1, P, and S fimbriae) and afimbrial adhesion. Afimbrial adhesins are proteins that play a role in colonization as adherence factors but differ in not forming a long structure such as fimbrial adhesions (Wilson et al., 2002). Cold stress has been shown to enhance the association between S. Typhimurium and Caco-2 epithelial cells through adhesion and invasion (Shah, Desai, & Weimer, 2014). Cold stress induced the gene expression of numerous genes associated with virulence such as Type III Secretion Systems (T3SS) and their effectors for SPI-1 and SPI-2. Other induced genes belong to cell processes (pathogenesis and DNA transformation), prophage functions, plasmid functions, protein secretion and trafficking, DNA replication, recombination and repair, purine ribonucleotide biosynthesis, and RNA degradation. Virulence effectors can be directly exported into the cytoplasm of the host cell via T3SS (also referred to as the injectisome) in Salmonella as well as various Gram-negative bacteria such as E. coli, Shigella, Vibrio, and Yersinia (Tsai, Burkinshaw, Strynadka, & Tainer, 2015). The SPI-1 and SPI-2 that encode for T3SS are the main factors of Salmonella pathogenesis. Virulence of Salmonella depends on SPI-2 T3SS for translocation of effector proteins to host cell from vacuolar-resident bacteria (Jennings, Thurston, & Holden, 2017). Hapfelmeier et al. (2005) reported attenuated colitis from Salmonella mutants having only an SPI-1 (M556; sseD::aphT) or SPI-2 TTSS (SB161; ΔinvG) (Hapfelmeier et al., 2005). Some genes associated with SPI-2 T3SS are located outside SPI-2 in SPI-5 are necessary for intracellular replication of Salmonella during enteric infection. A set of genes that creates part of the Type IV Secretion System (T4SS) is expressed in response to cold stress. The function of these genes is essential as part of plasmid function and conjugal DNA transformation. Shah et al. (2014) examined the effect of cold exposure 5°C for 48 h on S. Typhimurium pathogenicity by quantifying adhesion and invasion of

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Caco-2 cultured tissue cells. They observed increases in both adhesion and invasion of the Caco cells after exposure to the cold stress conditions. In conjunction with the tissue culture assays, the authors also conducted gene expression profiles and noted induction of several groups of virulence genes as well as metabolic genes in response to cold stress. The virulence genes included T3SS-associated genes located on the Salmonella pathogenicity islands. Assessment of Salmonella gene expression in infected Caco cells revealed induction of intracellular proliferation genes, spvR and spvABC and several stress-related genes including the cold shock genes cspABE. This together with their previous research (Shah et al., 2013) where they reported that cold stress also induced acid resistance, led them to suggest that cold stress could, in fact, increase overall pathogenicity in Salmonella. It is conceivable that such prior exposure might lower the infectious dose for Salmonella and thus enhance risk. This in part would depend on how sustained induction and presence of CSPs would be once Salmonella is removed from the cold environment of the chilled food matrix during consumption and ingestion. Whether this would be a practical consideration to take into account for screening Salmonella physiological status and upshifts of CSPs remains to be determined. Presence and significance of Salmonella in frozen and chilled foods will be discussed in the following section.

4. SALMONELLA RESPONSES TO COLD TEMPERATURES IN FOOD PRODUCTION 4.1 Salmonella Growth, Survival, and Influential Factors Freezing and chilling (refrigeration) are common methods of food preservation by lowering the temperature of food products affecting several functional mechanisms of microorganisms including metabolism (Archer, 2004). As newer food cold temperature preservation technologies have been developed, this will no doubt impact Salmonella growth and survival under these conditions and further complicate attempts to delineate the mechanisms associated with these environmental stressors. Some of these preservation approaches involve combinations that alter the food environment in multiple ways. For example, application of rapid vacuum cooling in food processing involves rapid evaporative decreases in temperature and removal of moisture and has been mostly applied to horticulture products (McDonald & Sun, 2000). Likewise, as suggested by Russell (2002) the combination of chilling with bacterial membrane disrupting technologies

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such as ultrasound, high hydrostatic pressure, or pulsed electric field are potential means to further extend shelf life. Over the past few decades, several fundamental studies of Salmonella survival/injury/growth involving freezing and chilling have been conducted. Most of the early research involved enumerating the recoverable bacterial cell populations after exposure to different cold temperatures and/or different periods of times of exposure to a particular temperature. For example, Sorrells et al. (1970) found that the freezing condition of 75°C resulted in 86% cell death and 29% of S. Gallinarum survivors becoming injured cells, whereas storing the cell suspension at 20°C for 1 day after freezing at 75°C increased the death rate by 2% (total of 88%) and resulted in 13% additional injured cells (total of 42%) of the survivors. In more recent research by M€ uller et al. (2012), they investigated the ability of some Salmonella clones from stationary- and exponential-phases to survive and grow after exposure to freezing stress (mimicking a meat processing chain) for up to 48 weeks in minced pork meat. Salmonella strains were selected using a mathematical model for epidemiological studies and characterizing the selected isolates to be either a successful or nonsuccessful clone. Twenty-six Salmonella isolates were selected with different antimicrobial resistance characteristics belonging to 6 serovars (14 strains S. Typhimurium, 4 strains S. Derby, 2 strains S. Newport, 2 strains S. Infantis, 2 strains S. Saintpaul, and 2 strains S. Virchow) from human and animal sources. The study concluded that up to 1 log reduction of cells at stationary phase of all strains was observed after 1 year of frozen storage, while more than a 1 log decrease of cells occurred during the exponential growth phase for the two strains of S. Typhimurium that exhibited the same reduction in 49 days of freezing stress indicating that exponential phase cells have more sensitivity to the same stress (M€ uller et al., 2012). They evaluated the recovery time needed by observing the growth in lag phase after the freezing stress for stationary and exponential phases of S. Typhimurium strains. The initiation of growth acquired an average of 102 min for stationary phase cells and shorter than that for cells of exponential phase (M€ uller et al., 2012). Phillips, Humphrey, and Lappin-Scott (1998) investigated the effect of chilling on two S. Enteritidis PT4 strains, E and I with strain E being more tolerant and pathogenic. These strains were considered different in heat- and acid-tolerance with the ability to survive on surfaces, and pathogenicity in animal models. For both strains, stationary phase cells were diluted to correspond to 5  105 mL1 and were used for chilling at 4°C for 12 days. The results indicated that strain I was consistent at all time periods and did not

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exhibit any significant reductions, whereas strain E expressed significant reduction at day 12. At the end of the treatment, strain E exhibited a sublethal injury (metabolic and structural injury) of 93%, while 29% occurred in strain I (Phillips et al., 1998). Therefore, even strains from the same species can potentially respond to stresses differently as has been seen in the response of Salmonella to other stresses (Andino & Hanning, 2015). Several microbial factors can influence the subsequent assessment of microbial responses to freezing. As discussed by Archer (2004) such factors include the growth phase of the organism, rate of freezing, and recovery media used for estimating viable microbial survivors. In addition, as Archer (2004) points out the composition of the menstruum which the microorganism is associated with while exposed to cold shock can be a factor, depending on the presence of compounds that exhibit cryobiological properties. It is well known that compositional differences can play a role as protective factors for pathogens when subjected to other stressors such as thermal or acid (Jarvis et al., 2016; Waterman & Small, 1998) and therefore it should be no surprise that similar interactions occur for cold shock as well. For example, Smadi, Sargeant, Shannon, and Raina (2012) using mixed effect meta-analysis, demonstrated a statistically significant difference when a chicken meat matrix was used vs laboratory media to assess Salmonella growth at refrigeration temperatures. Consequently, it may be important to assess quantitative impacts of cooling and freezing in matrices that approximate the actual food product as closely as possible to achieve the best estimates of responses in food processing. However, not all differences in food products are solely due to food composition alone. For example, Aldsworth, Sharman, Dodd, and Stewart (1998) demonstrated that the presence of viable non-Salmonella microbiota protected the underlying S. Typhimurium against freeze injury by changing the oxygen tension through respiration of the competitive microbial population. This protective outcome would suggest that microbial population differences in different foods and, in some cases, the same food source could contribute to differences in Salmonella survival during cold shock. It would be interesting to follow Salmonella survival during extended cold storage as the non-Salmonella population shifts to a more cold-tolerant psychrotrophic microbiota (Dainty & Mackey, 1992). Cold preservation of foods continues to be an important component of the food supply system in the United States. As of early 2018, cold storage supplies of frozen poultry and red meats in the United States were increased from the previous month and poultry was increased 13% from the year

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before (USDA Cold Storage Report, 2018). In this same report, frozen pork supplies were up 16% from the previous month, while frozen fruit and vegetable stocks were decreased compared to the month before. Regardless of the food commodity, storage under cold conditions is a potential risk for long-term carryover of Salmonella if the product has become contaminated at some point during processing of the food. The following sections describe a select set of studies conducted on the various food commodities involving chilling or freezing and Salmonella responses that illustrate some fundamental factors that need to be considered.

4.2 Beef Products A simulation study of commercial freezing was used for beef trimmings and three Salmonella serotypes (S. Brandenberg, S. Dublin, and S. Typhimurium) for exposure to slow (18°C) and rapid (35°C) freezing rates reaching a temperature of between 17°C and 22°C within 24 h incubation (Dykes & Moorhead, 2001). The rate exhibited by rapid freezing was 1.8 times more rapid. Subsequently, all treated beef trimmings were stored at 18°C for 9 months. Monthly samples were collected after thawing and refreezing, plated on selective and nonselective media, and Salmonella strains enumerated. Beef trimmings samples were partially thawed and refrozen at 18°C for 24 h to evaluate the potentially stressful procedure on the Salmonella serotypes. The survival difference of all strains was not significant as expected during the storage time period (Dykes & Moorhead, 2001). Their explanation was that the inoculated strains were rapidly frozen compared to the meat. In addition, no significant sublethal cell injuries were determined after comparing cell counts on selective and nonselective media. Long-term refrigeration studies have been conducted on beef as well. For example, Pittman et al. (2011) examined the potential to combine citrus essential oils with refrigeration on beef subprimal cuts (brisket flats) using a surrogate generic 5 strain biotype I E. coli cocktail that behaved similarly to pathogenic E. coli O157:H7 and Salmonella species when growth and survival responses were compared. Once inoculated with E. coli, brisket samples treated either with no spray, water spray control, 3% oil, or 6% oil were held in 4°C cold storage over a 90-day period and E. coli were enumerated on days 1, 2, 3, and 5, followed by 5-day intervals from day 5 to day 90. The citrus essential oil treatment significantly reduced E. coli on the brisket over the entire refrigeration storage period when compared to the no spray and water spray controls. Based on unpublished work, the authors

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did not observe a difference in minimum inhibitory concentration of essential oils between 4°C and 37°C. The authors suggested that synergism did not occur between temperature and the citrus essential oil but that the essential oil compound retained its antimicrobial activity at the lower temperature.

4.3 Chicken Meat Products Dominguez and Schaffner (2009) conducted a study on Salmonella survival in processed chicken products stored under frozen conditions. A cocktail of Salmonella strains, S. Kentucky and S. Typhimurium, originally isolated from chicken, with and without antibiotic resistance, were inoculated in fully cooked chicken nuggets and uncooked (raw) chicken strips; subsequently, the inoculated products were stored in a laboratory freezer (20°C) for 16 weeks with a weekly sampling collection. Samples were analyzed and plated in minimal, selective, and nonselective media. After incubation for 24 h at 37°C, colonies were enumerated to determine the survival of the bacterial cell population. The results demonstrated that Salmonella strains are capable of surviving freezing food processing for long periods of storage time when using frozen processed chicken products (Dominguez & Schaffner, 2009). Chaves, Han, Dawson, and Northcutt (2011) conducted a study to determine the survival of S. Typhimurium artificially inoculated on the surface of raw poultry products, skinless chicken breasts, and chicken thighs with skin, treated with freezing (85°C for 20 min). Late exponential-phase cultures were cold-shocked at 4°C incubated for 10 days, and noncold shocked cultures were used to inoculate skinless chicken breasts and chicken thighs with skin. For the crust freezing treatment, samples were divided into two groups. One group was crust frozen at 85°C for 20 min and the other group was frozen at 85°C for 60 min. Subsequently, all samples were refrigerated for 20 h and were recovered by rinsing with 50 mL sterile Bacto Peptone water. The collected solution was serially diluted and bacteria populations were enumerated on selective media, tryptic soy agar, and brilliant green agar with nalidixic acid. The results exhibited no significant reduction in any of the treatments with reductions of less than 1 log CFU/mL (Chaves et al., 2011). S. Typhimurium DT104, a multidrug-resistant strain, was used to analyze its growth on chicken meat under cold stress storage since it can be enumerated in the presence of other microorganisms and because it was previously isolated from chicken (Oscar, 2014). Chicken breasts, thighs,

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and skin were inoculated by spotting the surface with S. Typhimurium DT104. Subsequently, they were stored at cold storage from 8°C to 16°C for 0–8 days. Results indicated that when samples were inappropriately refrigerated at 12–16°C, S. Typhimurium DT104 proliferated at the highest level on thighs, followed by the skin and breast meat (Oscar, 2014).

4.4 Other Food Products The relationship between chicken eggs and S. Enteritidis continues to be a concern since the initial outbreaks occurred several decades ago (Galiş et al., 2013; Howard et al., 2012; Ricke, 2003a, 2017). This is due to the ability of S. Enteritidis to either externally penetrate the egg shell and reach the inner part of the egg or being deposited internally by transovarian contamination during formation of the egg after colonization of the reproductive tract (Galiş et al., 2013; Gantois et al., 2009; Ricke, 2017). Once reaching the inner part of the egg, it can, depending upon the internal temperature of the egg, multiply quite rapidly (Galiş et al., 2013; Howard et al., 2012). To restrain S. Enteritidis growth in eggs has been the focus of developing methods to rapidly cool eggs before prolonged storage (Galiş et al., 2013). Theron, Venter, and Lues (2003) reported that a cold shock 4°C for 4–6 h followed by storage and transport at 25°C was the most effective in limiting the growth of microbial populations including both Salmonella and non-Salmonella microorganisms on egg shells and in egg contents. Clearly the time it takes to reduce temperature to refrigeration level is important. For example, Chen, Anantheswaran, and Knabel (2002) inoculated internal shell egg contents with S. Enteritidis at a level of 10 cells and cooled eggs by either rapid cooling from 27°C to 7.2°C in a range of 6–6.5 min depending on the cooling method vs traditional cooling which required 142 h to reach 7.2°C. All eggs after cooling were stored at 7.2°C until sampled for S. Enteritidis. For rapidly cooled eggs, S. Enteritidis growth in the yolk and albumen was inhibited but yolk populations quickly multiplied (up 107 CFU within 3 days) in the slowly cooled eggs even though they did not grow in the albumen probably due to the presence of eggborne antimicrobial defenses as noted by the authors. The preponderance of growth in the yolk supports why transovarian internal contamination that does not come into contact with the albumen could be particularly problematic. Gast, Holt, and Guraya (2006) demonstrated that immediate refrigeration at 7°C also prevented S. Enteritidis already internalized in the egg on the egg yolk membrane from penetrating the membrane and

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contaminating the yolk while storage at higher temperatures before refrigeration led to an invasion of the yolk. Fresh produce and vegetables continue to be identified with foodborne pathogens including Salmonella and the issues associated with processing and control measures have been described extensively elsewhere (Erickson, 2010; Hanning et al., 2009; Lynch et al., 2009) and will not be discussed in the current review. However, refrigerated juices have come under specific scrutiny as a source of Salmonella to the point of a federal regulatory edict to institute treatments that reduce pathogens such as Salmonella by 5 logs in the United States (FDA, 2001; Parrish, Goodrich, & Miller, 2004). The confounding issue is that because juices are a high-acid food product, the potential for acid adaptation and cross-protection does exist. Yuk and Schneider (2006) demonstrated this experimentally when they showed that Salmonella in stored juices exhibited enhanced survival in simulated gastric juice. When acid-adapted (pH 5, 0.25% anhydrous citric acid) Salmonella species were stored at various refrigeration temperatures in either grapefruit or orange concentrate and sampled periodically for survivors, considerable differences were observed by Parrish et al. (2004). For the orange concentrate 2.3–4.8 Salmonella log reductions occurred after 50 days, while the time frame was much shorter for grapefruit concentrate reaching log reductions of 6.0–6.9 after only 11 days. Given the differences in the two juice concentrates, it would be of interest to do a detailed study on the respective concentrations particularly the types and levels of acids. Yuk and Schneider (2006) also noted differences in survival of Salmonella according to juice type as well as differences in serovars.

5. CONCLUSIONS Bacteria can encounter unexpected downshifts of temperature in the environment that will require them to generate cellular physical and biochemical modifications in response to gene expression regulation. This includes maintaining cell membrane fluidity, DNA supercoiling modifications, CSPs, mRNA secondary structure modulation, and other mechanisms depending on the cold shock level and exposure time. Salmonella can express physiological and genetic responses to cold stress; they can survive for long periods of time during cold environment and induce various modifications including cross-protection to other stressors and virulence factors. In some case, cold stress caused an enhancement of Salmonella pathogenicity by increasing adhesion and invasion to epithelial cells, demonstrating exposure

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to cold environments during manufacturing, transporting, and storage could be a considerable problem for food safety. Whether this needs to be considered a risk factor is unclear at this time since it is not known how transient some of the responses are. Other issues such as serovar differences also need to be examined. Therefore, the mechanisms of Salmonella stress response to cold will need to be studied more in-depth not only for individual serovars but across different serovars to achieve better control of Salmonella using cold temperature in the food industries.

ACKNOWLEDGMENTS Author T.M.D. was supported by a scholarship from King Saud University, Riyadh, Saudi Arabia. During his graduate work, he was partially funded by a grant from the Deanship of Scientific Research, King Saud University (Research Group No. RGP-VPP-020). Author S.A.K. was initially supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF2015R1A6A3A03016811).

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