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Review in Advance first posted online on February 4, 2015. (Changes may still occur before final publication online and in print.)
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28 January 2015
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Annu. Rev. Food Sci. Technol. 2015.6. Downloaded from www.annualreviews.org Access provided by University of New Hampshire on 02/16/15. For personal use only.
Stress Adaptation in Foodborne Pathogens M´aire Begley1 and Colin Hill2 1
Department of Biological Sciences, Cork Institute of Technology, Bishopstown, Cork, Ireland; email: [email protected]
2
School of Microbiology and Alimentary Pharmabiotic Centre, University College Cork, Cork, Ireland; email: [email protected]
Annu. Rev. Food Sci. Technol. 2015. 6:9.1–9.20
Keywords
The Annual Review of Food Science and Technology is online at food.annualreviews.org
food pathogen, food safety, stress adaptation, stress proteins, virulence
This article’s doi: 10.1146/annurev-food-030713-092350
Abstract
c 2015 by Annual Reviews. Copyright All rights reserved
Foodborne bacterial pathogens encounter many environmental insults or stresses during food production, processing, storage, distribution, and preparation. However, these pathogens can sense changes in their surroundings and can respond by altering gene expression. A protective response may follow that increases tolerance to one or more stresses. This phenomenon is referred to as stress adaptation and has been shown to aid in the survival of pathogens in food products and in the food processing environment. Furthermore, stress adaptation may alter the virulence properties of pathogens and can contribute to survival in vivo during infection. Elucidating the molecular mechanisms underlying stress adaptation in bacterial food pathogens is essential for the development and implementation of more effective control measures and will permit the design of optimal processing regimes that combine maximum safety with consumer demands for more fresh-like, minimally processed foods.
9.1
Changes may still occur before final publication online and in print
FO06CH09-Begley
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1. INTRODUCTION
Annu. Rev. Food Sci. Technol. 2015.6. Downloaded from www.annualreviews.org Access provided by University of New Hampshire on 02/16/15. For personal use only.
In recent years, significant efforts have been directed toward reducing the burden of foodborne diseases, and a farm-to-fork approach has been adopted to improve food safety. Despite major efforts from scientists, governments, and industry, foodborne diseases continue to be a major problem in modern society. For example, the US Centers for Disease Control and Prevention estimate that there are 48 million cases of foodborne illnesses annually in the United States, which result in 128,000 hospitalizations and 3,000 deaths (Scallan et al. 2011). If these figures are extrapolated to a global scale, an estimated 1 billion or more cases of foodborne disease occur annually; this has been referred to as a largely silent raging epidemic (Choffnes et al. 2012). The recent, well-publicized outbreaks of foodborne illnesses and deaths that were linked to Listeria monocytogenes in cantaloupe, Salmonella spp. in chicken eggs and ground turkey, and Escherichia coli in fenugreek seeds serve to illustrate the threat of foodborne disease to public health, trade, and economies (Choffnes et al. 2012). Multiple factors contribute to or influence the prevalence of foodborne disease. These include demographic factors such as rapid population growth, a shift toward an aging population, higher numbers of immunologically compromised individuals, an increasingly transient human population, changing eating habits, as well as consumer demand for fresh-like, minimally processed foods (Newell et al. 2010). In addition to these host-related factors, microbial factors are also important. It is well established that foodborne bacterial pathogens can adapt in response to environmental challenges or stresses and, in doing so, may display increased virulence properties. Herein we provide an overview of foodborne bacterial pathogen stress adaptation. It is not possible to include all of the available literature in this broad field, so we have selected specific studies to present what we consider to be the most important take-home messages.
2. STRESS ADAPTATION 2.1. Bacterial Stress Responses: What Doesn’t Kill You Makes You Stronger Stress refers to any deleterious factor or condition that adversely affects microbial growth and survival (Yousef & Courtney 2003). Foodborne bacterial pathogens encounter many stresses throughout their life cycle, particularly during food production, processing, storage, and cooking. These stresses include physical treatments such as heat, pressure, or osmotic shock, chemical treatments such as acids or detergents, and biological stresses such as bacteriocins (Table 1). The modern trend toward minimally processed foods is driving food processors to use a combination of mild food preservation strategies (often referred to as hurdle technology) rather than a single extreme stress (Hill et al. 2002, Leistner 2000). Foodborne pathogens may therefore have to overcome many stressful conditions in succession or in parallel. Foodborne pathogens also encounter stresses during infection of the host. Several of these in vivo stresses are similar to stresses encountered in food, such as the low pH encountered in the stomach and macrophages, the elevated osmolarity of the intestine, and relatively high body temperature. However, certain stresses may be unique to the host, such as exposure to bile salts in the intestine. Exposure to stress may result in bacterial cell injury and damage to various cellular structures, including the cell wall, cell membrane, proteins, RNA, and DNA (Wesche et al. 2009). The degree and type of damage obviously depends on the nature and severity of the stress. In this regard, researchers have shown that foodborne pathogens can sense their surroundings and respond to changed environmental conditions by expressing genes that reprogram the cell and assist in 9.2
Begley
·
Hill
Changes may still occur before final publication online and in print
FO06CH09-Begley
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Table 1 Environmental conditions that may induce stress responses in foodborne pathogens at various stages of their life cycle, including food production, processing, storage, distribution, consumption, and finally passage through the human gastrointestinal tract
Annu. Rev. Food Sci. Technol. 2015.6. Downloaded from www.annualreviews.org Access provided by University of New Hampshire on 02/16/15. For personal use only.
Environmental condition
Stage in the food production chain
Low temperature
Refrigeration, freezing
High temperature
Food processing, temperature control failure during storage and distribution, cooking of food, fever in the host
Low pH
Low pH foods (e.g., fermented foods, acidic additives), stomach, macrophage
Osmolarity
Additives during food preparation (e.g., NaCl), intestine
Starvation
Low nutrients in the environment or in vivo
Oxidative stress
Exposure to air or oxidative sanitizers during food processing, storage, and distribution; oxidative stress in the macrophage
Drying
Food processing (air-, vacuum-, and freeze-drying)
High hydrostatic pressure
Food processing
Radiation
Food processing (gamma, UV, and X-rays)
Chemical sanitizers (e.g., chlorine, quaternary ammonium compounds)
Food processing
Preservatives (e.g., bacteriocins, sorbate, nitrate)
Food processing
a
Adapted from Yousef & Courtney (2003) and Wesche et al. (2009).
survival. These stress responses may result in the production of proteins that repair damage, maintain cell homeostasis, or facilitate the removal of the stress agent. The basis of the adaptive or protective response is that preexposure to mild (sublethal) levels of a given stress protects the organism during subsequent exposure to harsh (normally lethal) levels of the same type of stress. This phenomenon of induced tolerance is referred to as stress adaptation or stress hardening (Yousef & Courtney 2003). Preexposure to one stress (e.g., low pH) may also confer protection against a different type of stress (e.g., heat), a phenomenon that is referred to as stress cross-adaptation.
2.2. Examples of Bacterial Stress Adaptation and Cross-Adaptation The best-studied bacterial stress responses are probably the heat shock and acid tolerance responses. In many species, exposure of bacteria to mild temperature shocks can result in acquired thermotolerance, whereas exposure to mildly acidic pH can induce an acid tolerance response (ATR) that protects cells against subsequent exposure to low pH. These responses have been reported in numerous foodborne pathogens, including L. monocytogenes, E. coli, and Salmonella ´ (reviewed by Abee & Wouters 1999, Alvarez-Ord o´ nez ˜ et al. 2012, Ryan et al. 2008, Sleator & Hill 2002, Soni et al. 2011, and Storz & Hengge-Aronis 2000). Adaptation to numerous other stress conditions has also been observed, including osmotic, oxidative, and cold stresses. There are also numerous reports in the literature of cross-adaptation between stresses. For example, thermotolerance can be induced in L. monocytogenes, E. coli, and Salmonella by both starvation and acid adaptation (Leenanon & Drake 2001, Leyer & Johnson 1993, Lou & Yousef 1996, Rowe & Kirk 2000). Exposing Salmonella to mild acid protects against salt stress (Leyer & Johnson www.annualreviews.org • Stress Adaptation in Foodborne Pathogens
Changes may still occur before final publication online and in print
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1993), and acid-adapted L. monocytogenes shows increased tolerance against the bacteriocins nisin and lacticin 3147 (Van Schaik et al. 1999). Preexposure to stresses encountered in the food environment may also induce cross-protection against stresses encountered solely in vivo. For example, experiments performed in our laboratory demonstrated that exposure of L. monocytogenes cells to mild insult with acid, heat, salt, or sodium dodecyl sulfate significantly enhanced the ability of the pathogen to tolerate unconjugated bile salts (Begley et al. 2002). A study by McMahon et al. (2007) demonstrated that exposing E. coli, Salmonella enterica serovar Typhimurium, or Staphylococcus aureus to some sublethal stresses (>4.5% salt,
ARI
V I E W
13:15
Review in Advance first posted online on February 4, 2015. (Changes may still occur before final publication online and in print.)
A
N
I N
C E
S
R
E
28 January 2015
D V A
Annu. Rev. Food Sci. Technol. 2015.6. Downloaded from www.annualreviews.org Access provided by University of New Hampshire on 02/16/15. For personal use only.
Stress Adaptation in Foodborne Pathogens M´aire Begley1 and Colin Hill2 1
Department of Biological Sciences, Cork Institute of Technology, Bishopstown, Cork, Ireland; email: [email protected]
2
School of Microbiology and Alimentary Pharmabiotic Centre, University College Cork, Cork, Ireland; email: [email protected]
Annu. Rev. Food Sci. Technol. 2015. 6:9.1–9.20
Keywords
The Annual Review of Food Science and Technology is online at food.annualreviews.org
food pathogen, food safety, stress adaptation, stress proteins, virulence
This article’s doi: 10.1146/annurev-food-030713-092350
Abstract
c 2015 by Annual Reviews. Copyright All rights reserved
Foodborne bacterial pathogens encounter many environmental insults or stresses during food production, processing, storage, distribution, and preparation. However, these pathogens can sense changes in their surroundings and can respond by altering gene expression. A protective response may follow that increases tolerance to one or more stresses. This phenomenon is referred to as stress adaptation and has been shown to aid in the survival of pathogens in food products and in the food processing environment. Furthermore, stress adaptation may alter the virulence properties of pathogens and can contribute to survival in vivo during infection. Elucidating the molecular mechanisms underlying stress adaptation in bacterial food pathogens is essential for the development and implementation of more effective control measures and will permit the design of optimal processing regimes that combine maximum safety with consumer demands for more fresh-like, minimally processed foods.
9.1
Changes may still occur before final publication online and in print
FO06CH09-Begley
ARI
28 January 2015
13:15
1. INTRODUCTION
Annu. Rev. Food Sci. Technol. 2015.6. Downloaded from www.annualreviews.org Access provided by University of New Hampshire on 02/16/15. For personal use only.
In recent years, significant efforts have been directed toward reducing the burden of foodborne diseases, and a farm-to-fork approach has been adopted to improve food safety. Despite major efforts from scientists, governments, and industry, foodborne diseases continue to be a major problem in modern society. For example, the US Centers for Disease Control and Prevention estimate that there are 48 million cases of foodborne illnesses annually in the United States, which result in 128,000 hospitalizations and 3,000 deaths (Scallan et al. 2011). If these figures are extrapolated to a global scale, an estimated 1 billion or more cases of foodborne disease occur annually; this has been referred to as a largely silent raging epidemic (Choffnes et al. 2012). The recent, well-publicized outbreaks of foodborne illnesses and deaths that were linked to Listeria monocytogenes in cantaloupe, Salmonella spp. in chicken eggs and ground turkey, and Escherichia coli in fenugreek seeds serve to illustrate the threat of foodborne disease to public health, trade, and economies (Choffnes et al. 2012). Multiple factors contribute to or influence the prevalence of foodborne disease. These include demographic factors such as rapid population growth, a shift toward an aging population, higher numbers of immunologically compromised individuals, an increasingly transient human population, changing eating habits, as well as consumer demand for fresh-like, minimally processed foods (Newell et al. 2010). In addition to these host-related factors, microbial factors are also important. It is well established that foodborne bacterial pathogens can adapt in response to environmental challenges or stresses and, in doing so, may display increased virulence properties. Herein we provide an overview of foodborne bacterial pathogen stress adaptation. It is not possible to include all of the available literature in this broad field, so we have selected specific studies to present what we consider to be the most important take-home messages.
2. STRESS ADAPTATION 2.1. Bacterial Stress Responses: What Doesn’t Kill You Makes You Stronger Stress refers to any deleterious factor or condition that adversely affects microbial growth and survival (Yousef & Courtney 2003). Foodborne bacterial pathogens encounter many stresses throughout their life cycle, particularly during food production, processing, storage, and cooking. These stresses include physical treatments such as heat, pressure, or osmotic shock, chemical treatments such as acids or detergents, and biological stresses such as bacteriocins (Table 1). The modern trend toward minimally processed foods is driving food processors to use a combination of mild food preservation strategies (often referred to as hurdle technology) rather than a single extreme stress (Hill et al. 2002, Leistner 2000). Foodborne pathogens may therefore have to overcome many stressful conditions in succession or in parallel. Foodborne pathogens also encounter stresses during infection of the host. Several of these in vivo stresses are similar to stresses encountered in food, such as the low pH encountered in the stomach and macrophages, the elevated osmolarity of the intestine, and relatively high body temperature. However, certain stresses may be unique to the host, such as exposure to bile salts in the intestine. Exposure to stress may result in bacterial cell injury and damage to various cellular structures, including the cell wall, cell membrane, proteins, RNA, and DNA (Wesche et al. 2009). The degree and type of damage obviously depends on the nature and severity of the stress. In this regard, researchers have shown that foodborne pathogens can sense their surroundings and respond to changed environmental conditions by expressing genes that reprogram the cell and assist in 9.2
Begley
·
Hill
Changes may still occur before final publication online and in print
FO06CH09-Begley
ARI
28 January 2015
13:15
Table 1 Environmental conditions that may induce stress responses in foodborne pathogens at various stages of their life cycle, including food production, processing, storage, distribution, consumption, and finally passage through the human gastrointestinal tract
Annu. Rev. Food Sci. Technol. 2015.6. Downloaded from www.annualreviews.org Access provided by University of New Hampshire on 02/16/15. For personal use only.
Environmental condition
Stage in the food production chain
Low temperature
Refrigeration, freezing
High temperature
Food processing, temperature control failure during storage and distribution, cooking of food, fever in the host
Low pH
Low pH foods (e.g., fermented foods, acidic additives), stomach, macrophage
Osmolarity
Additives during food preparation (e.g., NaCl), intestine
Starvation
Low nutrients in the environment or in vivo
Oxidative stress
Exposure to air or oxidative sanitizers during food processing, storage, and distribution; oxidative stress in the macrophage
Drying
Food processing (air-, vacuum-, and freeze-drying)
High hydrostatic pressure
Food processing
Radiation
Food processing (gamma, UV, and X-rays)
Chemical sanitizers (e.g., chlorine, quaternary ammonium compounds)
Food processing
Preservatives (e.g., bacteriocins, sorbate, nitrate)
Food processing
a
Adapted from Yousef & Courtney (2003) and Wesche et al. (2009).
survival. These stress responses may result in the production of proteins that repair damage, maintain cell homeostasis, or facilitate the removal of the stress agent. The basis of the adaptive or protective response is that preexposure to mild (sublethal) levels of a given stress protects the organism during subsequent exposure to harsh (normally lethal) levels of the same type of stress. This phenomenon of induced tolerance is referred to as stress adaptation or stress hardening (Yousef & Courtney 2003). Preexposure to one stress (e.g., low pH) may also confer protection against a different type of stress (e.g., heat), a phenomenon that is referred to as stress cross-adaptation.
2.2. Examples of Bacterial Stress Adaptation and Cross-Adaptation The best-studied bacterial stress responses are probably the heat shock and acid tolerance responses. In many species, exposure of bacteria to mild temperature shocks can result in acquired thermotolerance, whereas exposure to mildly acidic pH can induce an acid tolerance response (ATR) that protects cells against subsequent exposure to low pH. These responses have been reported in numerous foodborne pathogens, including L. monocytogenes, E. coli, and Salmonella ´ (reviewed by Abee & Wouters 1999, Alvarez-Ord o´ nez ˜ et al. 2012, Ryan et al. 2008, Sleator & Hill 2002, Soni et al. 2011, and Storz & Hengge-Aronis 2000). Adaptation to numerous other stress conditions has also been observed, including osmotic, oxidative, and cold stresses. There are also numerous reports in the literature of cross-adaptation between stresses. For example, thermotolerance can be induced in L. monocytogenes, E. coli, and Salmonella by both starvation and acid adaptation (Leenanon & Drake 2001, Leyer & Johnson 1993, Lou & Yousef 1996, Rowe & Kirk 2000). Exposing Salmonella to mild acid protects against salt stress (Leyer & Johnson www.annualreviews.org • Stress Adaptation in Foodborne Pathogens
Changes may still occur before final publication online and in print
9.3
ARI
28 January 2015
13:15
1993), and acid-adapted L. monocytogenes shows increased tolerance against the bacteriocins nisin and lacticin 3147 (Van Schaik et al. 1999). Preexposure to stresses encountered in the food environment may also induce cross-protection against stresses encountered solely in vivo. For example, experiments performed in our laboratory demonstrated that exposure of L. monocytogenes cells to mild insult with acid, heat, salt, or sodium dodecyl sulfate significantly enhanced the ability of the pathogen to tolerate unconjugated bile salts (Begley et al. 2002). A study by McMahon et al. (2007) demonstrated that exposing E. coli, Salmonella enterica serovar Typhimurium, or Staphylococcus aureus to some sublethal stresses (>4.5% salt,
