Salmonella Pathogenicity and Host Adaptation in Chicken-Associated Serovars

SUMMARY Enteric pathogens such as Salmonella enterica cause significant morbidity and mortality. S. enterica serovars are a diverse group of pathogens that have evolved to survive in a wide range of environments and across multiple hosts. S. enterica serovars such as S. Typhi, S. Dublin, and S. Gallinarum have a restricted host range, in which they are typically associated with one or a few host species, while S. Enteritidis and S. Typhimurium have broad host ranges. This review examines how S. enterica has evolved through adaptation to different host environments, especially as related to the chicken host, and continues to be an important human pathogen. Several factors impact host range, and these include the acquisition of genes via horizontal gene transfer with plasmids, transposons, and phages, which can potentially expand host range, and the loss of genes or their function, which would reduce the range of hosts that the organism can infect. S. Gallinarum, with a limited host range, has a large number of pseudogenes in its genome compared to broader-host-range serovars. S. enterica serovars such as S. Kentucky and S. Heidelberg also often have plasmids that may help them colonize poultry more efficiently. The ability to colonize different hosts also involves interactions with the host's immune system and commensal organisms that are present. Thus, the factors that impact the ability of Salmonella to colonize a particular host species, such as chickens, are complex and multifactorial, involving the host, the pathogen, and extrinsic pressures. It is the interplay of these factors which leads to the differences in host ranges that we observe today.

[1]  Dipshikha Chakravortty,et al.  Host-specificity of Salmonella enterica serovar Gallinarum: insights from comparative genomics. , 2009, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[2]  R. Gast,et al.  Colonization of Avian Reproductive-Tract Tissues by Variant Subpopulations of Salmonella Enteritidis , 2010, Avian diseases.

[3]  M. Widdowson,et al.  Foodborne Illness Acquired in the United States—Major Pathogens , 2011, Emerging infectious diseases.

[4]  Matthew A. Kayala,et al.  Identification of a common immune signature in murine and human systemic Salmonellosis , 2012, Proceedings of the National Academy of Sciences.

[5]  F. Fang,et al.  Plasmid-mediated virulence genes in non-typhoid Salmonella serovars. , 1994, FEMS microbiology letters.

[6]  H. Danbara,et al.  Molecular analysis of spv virulence genes of the salmonella virulence plasmids , 1993, Molecular microbiology.

[7]  J. Shea,et al.  Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages , 1998, Molecular microbiology.

[8]  M. Hume,et al.  Effect of feed withdrawal on the incidence of Salmonella in the crops and ceca of market age broiler chickens. , 1997, Poultry science.

[9]  E. Boyd,et al.  Bacteriophage-encoded bacterial virulence factors and phage-pathogenicity island interactions. , 2012, Advances in virus research.

[10]  C. Beaumont,et al.  Toward integrative genomics study of genetic resistance to Salmonella and Campylobacter intestinal colonization in fowl , 2012, Front. Gene..

[11]  A. Thompson,et al.  Butyrate Specifically Down-Regulates Salmonella Pathogenicity Island 1 Gene Expression , 2006, Applied and Environmental Microbiology.

[12]  S. Shinoda,et al.  [Iron uptake mechanisms of pathogenic bacteria]. , 1996, Nihon saikingaku zasshi. Japanese journal of bacteriology.

[13]  Wolf-Dietrich Hardt,et al.  Salmonella type III secretion effectors: pulling the host cell's strings. , 2006, Current opinion in microbiology.

[14]  R. H. Bailey,et al.  Survival of Salmonella in the crop contents of market-age broilers during feed withdrawal. , 1999, Avian diseases.

[15]  C. V. Van Nevel,et al.  Influence of substrate and microbial interaction on efficiency of rumen microbial growth. , 1986, Reproduction, nutrition, developpement.

[16]  T. Mignot,et al.  Bacterial motility complexes require the actin‐like protein, MreB and the Ras homologue, MglA , 2010, The EMBO journal.

[17]  R. Curtiss,et al.  The Salmonella Pathogenicity Island (SPI) 1 contributes more than SPI2 to the colonization of the chicken by Salmonella enterica serovar Typhimurium , 2009, BMC Microbiology.

[18]  J. Stephen,et al.  Pathogenesis of infectious diarrhea. , 2001, Canadian journal of gastroenterology = Journal canadien de gastroenterologie.

[19]  Songnian Hu,et al.  Complete nucleotide sequence of pSCV50, the virulence plasmid of Salmonella enterica serovar Choleraesuis SC-B67. , 2006, Plasmid.

[20]  F. Grau,et al.  Effect of some preslaughter treatments on the Salmonella population in the bovine rumen and faeces. , 1968, The Journal of applied bacteriology.

[21]  P. McDermott,et al.  Characterization of Salmonella enterica serovar Heidelberg from Turkey-Associated Sources , 2008, Applied and Environmental Microbiology.

[22]  M. Hensel,et al.  Salmonella Pathogenicity Island 2 , 2000, Molecular microbiology.

[23]  D. Holden,et al.  Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system , 2003, Cellular microbiology.

[24]  Kathleen Marchal,et al.  Integration of omics data: how well does it work for bacteria? , 2006, Molecular microbiology.

[25]  A. Chaussé,et al.  Multiplicity of Salmonella entry mechanisms, a new paradigm for Salmonella pathogenesis , 2012, MicrobiologyOpen.

[26]  P. Grimont,et al.  Restriction Fragment Length Polymorphism Analysis of Some Flagellin Genes of Salmonella enterica , 1998, Journal of Clinical Microbiology.

[27]  T. Johnson,et al.  DNA Sequence of a ColV Plasmid and Prevalence of Selected Plasmid-Encoded Virulence Genes among Avian Escherichia coli Strains , 2006, Journal of bacteriology.

[28]  L. Bossi,et al.  Inducible prophages contribute to Salmonella virulence in mice , 1999, Molecular microbiology.

[29]  P. Nordmann,et al.  Evolution of IncA/C blaCMY-2-Carrying Plasmids by Acquisition of the blaNDM-1 Carbapenemase Gene , 2011, Antimicrobial Agents and Chemotherapy.

[30]  M. Wick,et al.  Immunity to Salmonella from a dendritic point of view , 2004, Cellular microbiology.

[31]  Hans Wolf-Watz,et al.  Protein delivery into eukaryotic cells by type III secretion machines , 2006, Nature.

[32]  S. Ricke,et al.  Salmonella Enteritidis in shell eggs: Current issues and prospects for control , 2012 .

[33]  D. Call,et al.  Salmonella Enteritidis strains from poultry exhibit differential responses to acid stress, oxidative stress, and survival in the egg albumen. , 2012, Foodborne pathogens and disease.

[34]  B. Beutler,et al.  The interface between innate and adaptive immunity , 2004, Nature Immunology.

[35]  M. Rasmussen,et al.  Identification of Salmonella enterica Serovar Typhimurium Genes Important for Survival in the Swine Gastric Environment , 2006, Applied and Environmental Microbiology.

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

[37]  P. Donnelly,et al.  Recombination and Population Structure in Salmonella enterica , 2011, PLoS genetics.

[38]  Julian Parkhill,et al.  Pseudogene accumulation in the evolutionary histories of Salmonella enterica serovars Paratyphi A and Typhi , 2009, BMC Genomics.

[39]  P. Rosenstiel,et al.  ACE2 links amino acid malnutrition to microbial ecology and intestinal inflammation , 2012, Nature.

[40]  C. S. DENATURING GRADIENT GEL ELECTROPHORESIS ( DGGE ) AS A RAPID METHOD FOR ASSESSING GASTROINTESTINAL TRACT MICROFLORA RESPONSES IN LAYING HENS FED SIMILAR ZINC MOLT INDUCTION DIETS , 2006 .

[41]  P. Holt,et al.  Molting and Salmonella enterica serovar enteritidis infection: the problem and some solutions. , 2003, Poultry science.

[42]  A. Kalergis,et al.  Excision of an Unstable Pathogenicity Island in Salmonella enterica Serovar Enteritidis Is Induced during Infection of Phagocytic Cells , 2011, PloS one.

[43]  T. Cebula,et al.  Diagnostic potential ofsefADNA probes toSalmonella enteritidisand certain other O-serogroup D1Salmonellaserovars , 1996 .

[44]  Patrick Jenny,et al.  Hierarchical Effector Protein Transport by the Salmonella Typhimurium SPI-1 Type III Secretion System , 2008, PloS one.

[45]  S. Ricke,et al.  Observations on the history of the development of antimicrobials and their use in poultry feeds. , 2003, Poultry science.

[46]  F. Haesebrouck,et al.  Protection of laying hens against Salmonella Enteritidis by immunization with type 1 fimbriae. , 2005, Veterinary microbiology.

[47]  S. Casjens,et al.  Evolution of mosaically related tailed bacteriophage genomes seen through the lens of phage P22 virion assembly. , 2011, Virology.

[48]  K. Mizobuchi,et al.  Complete genome sequence of the incompatibility group I1 plasmid R64. , 2010, Plasmid.

[49]  D. Call,et al.  In vitro and in vivo pathogenicity of Salmonella enteritidis clinical strains isolated from North America , 2011, Archives of Microbiology.

[50]  P. Nordmann,et al.  Genetic Features of blaNDM-1-Positive Enterobacteriaceae , 2011, Antimicrobial Agents and Chemotherapy.

[51]  S. Rubino,et al.  Host adapted serotypes of Salmonella enterica , 2000, Epidemiology and Infection.

[52]  D. Maskell,et al.  Molecular insights into farm animal and zoonotic Salmonella infections , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[53]  H. Hradecká,et al.  Distribution and function of plasmids in Salmonella enterica. , 2006, Veterinary microbiology.

[54]  T. Taylor,et al.  Chemical Preservatives and Natural Antimicrobial Compounds , 2007 .

[55]  B. Finlay,et al.  Salmonella pathogenicity islands: big virulence in small packages. , 2000, Microbes and infection.

[56]  S. Ricke,et al.  Short-chain volatile fatty acids modulate the expression of the hilA and invF genes of Salmonella typhimurium. , 2000, Journal of food protection.

[57]  G. Olsen,et al.  Comparative genomics of closely related salmonellae. , 2002, Trends in microbiology.

[58]  A. Carattoli,et al.  First report on IncN plasmid-mediated quinolone resistance gene qnrS1 in porcine Escherichia coli in Europe. , 2011, Microbial drug resistance.

[59]  Didier Hocquet,et al.  Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. , 2011, Trends in microbiology.

[60]  J. Garrett Morris,et al.  Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens. , 2012, Journal of food protection.

[61]  A. Carattoli,et al.  Multilocus sequence typing of IncI1 plasmids carrying extended-spectrum beta-lactamases in Escherichia coli and Salmonella of human and animal origin. , 2008, The Journal of antimicrobial chemotherapy.

[62]  Marian M. Cahill Bacterial flora of fishes: A review , 2005, Microbial Ecology.

[63]  Frank T. Jones,et al.  A review of practical Salmonella control measures in animal feed , 2011 .

[64]  Howard Ochman,et al.  The Extinction Dynamics of Bacterial Pseudogenes , 2010, PLoS genetics.

[65]  M. Donnenberg,et al.  Pathogenic strategies of enteric bacteria , 2000, Nature.

[66]  R. Tauxe,et al.  The emergence of grade A eggs as a major source of Salmonella enteritidis infections. New implications for the control of salmonellosis. , 1988, JAMA.

[67]  Christopher M. Bailey,et al.  Type VI secretion: a beginner's guide. , 2008, Current opinion in microbiology.

[68]  P. Nordmann,et al.  Analysis of the Resistome of a Multidrug-Resistant NDM-1-Producing Escherichia coli Strain by High-Throughput Genome Sequencing , 2011, Antimicrobial Agents and Chemotherapy.

[69]  F. Aarestrup,et al.  IS6100-mediated genetic rearrangement within the complex class 1 integron In104 of the Salmonella genomic island 1. , 2010, The Journal of antimicrobial chemotherapy.

[70]  P. Visca,et al.  Class 1 Integron-Borne Multiple-Antibiotic Resistance Carried by IncFI and IncL/M Plasmids in Salmonella enterica Serotype Typhimurium , 1998, Antimicrobial Agents and Chemotherapy.

[71]  P. Fedorka-Cray,et al.  Alternate routes of invasion may affect pathogenesis of Salmonella typhimurium in swine , 1995, Infection and immunity.

[72]  M. Hensel,et al.  Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells , 2006, Cellular microbiology.

[73]  J. Russell,et al.  The effects of fermentation acids on bacterial growth. , 1998, Advances in microbial physiology.

[74]  S. Ricke,et al.  Short-chain fatty acids affect cell-association and invasion of HEp-2 cells by Salmonella typhimurium. , 1999, Journal of environmental science and health. Part. B, Pesticides, food contaminants, and agricultural wastes.

[75]  F. Haesebrouck,et al.  Interactions of Butyric Acid– and Acetic Acid–Treated Salmonella with Chicken Primary Cecal Epithelial Cells In Vitro , 2004, Avian diseases.

[76]  D. Chakravortty,et al.  Visiting the cell biology of Salmonella infection. , 2010, Microbes and infection.

[77]  B. Finlay,et al.  Analysis of the Contribution of Salmonella Pathogenicity Islands 1 and 2 to Enteric Disease Progression Using a Novel Bovine Ileal Loop Model and a Murine Model of Infectious Enterocolitis , 2005, Infection and Immunity.

[78]  Timothy R. Walsh,et al.  Characterization of a New Metallo-β-Lactamase Gene, blaNDM-1, and a Novel Erythromycin Esterase Gene Carried on a Unique Genetic Structure in Klebsiella pneumoniae Sequence Type 14 from India , 2009, Antimicrobial Agents and Chemotherapy.

[79]  A. Smith,et al.  The long view: Salmonella – the last forty years , 2012, Avian pathology : journal of the W.V.P.A.

[80]  A. Carattoli,et al.  Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella. , 2009, The Journal of antimicrobial chemotherapy.

[81]  D. Gibson,et al.  Extracellular Polysaccharides Associated with Thin Aggregative Fimbriae of Salmonella enterica Serovar Enteritidis , 2003, Journal of bacteriology.

[82]  C. Donskey,et al.  Poultry digestive microflora biodiversity as indicated by denaturing gradient gel electrophoresis. , 2003, Poultry science.

[83]  Songnian Hu,et al.  Evolution of genes on the Salmonella Virulence plasmid phylogeny revealed from sequencing of the virulence plasmids of S. enterica serotype Dublin and comparative analysis. , 2008, Genomics.

[84]  D. Korver Overview of the Immune Dynamics of the Digestive System , 2006 .

[85]  A. Horswill,et al.  Salmonella typhimurium LT2 Catabolizes Propionate via the 2-Methylcitric Acid Cycle , 1999, Journal of bacteriology.

[86]  A. Kropinski,et al.  Salmonella phages and prophages--genomics and practical aspects. , 2007, Methods in molecular biology.

[87]  M. Katamay,et al.  Antagonistic effect of fatty acids against Salmonella in meat and bone meal. , 1969, Applied microbiology.

[88]  S. Ricke,et al.  A review on development of novel strategies for controlling Salmonella Enteritidis colonization in laying hens: fiber-based molt diets. , 2013, Poultry science.

[89]  R. Aminov,et al.  Commensal gut bacteria: mechanisms of immune modulation. , 2005, Trends in immunology.

[90]  M. Quail,et al.  Structure, Diversity, and Mobility of the Salmonella Pathogenicity Island 7 Family of Integrative and Conjugative Elements within Enterobacteriaceae , 2012, Journal of bacteriology.

[91]  Sujata A. Sirsat,et al.  Antimicrobials for foodborne pathogen reduction in organic and natural poultry production , 2009 .

[92]  M. Mendoza,et al.  Characterization of pUO-StVR2, a Virulence-Resistance Plasmid Evolved from the pSLT Virulence Plasmid of Salmonella enterica Serovar Typhimurium , 2008, Antimicrobial Agents and Chemotherapy.

[93]  R. Singer,et al.  Comparative Genomics of Multidrug Resistance-Encoding IncA/C Plasmids from Commensal and Pathogenic Escherichia coli from Multiple Animal Sources , 2011, PloS one.

[94]  A. Lynne,et al.  Food animal-associated Salmonella challenges: pathogenicity and antimicrobial resistance. , 2008, Journal of animal science.

[95]  Georgios S. Vernikos,et al.  Comparative genome analysis of Salmonella Enteritidis PT4 and Salmonella Gallinarum 287/91 provides insights into evolutionary and host adaptation pathways. , 2008, Genome research.

[96]  F. Haesebrouck,et al.  The Salmonella Enteritidis Lipopolysaccharide Biosynthesis Gene rfbH is Required for Survival in Egg Albumen , 2009, Zoonoses and public health.

[97]  L. Bossi,et al.  Bacteriophage Crosstalk: Coordination of Prophage Induction by Trans-Acting Antirepressors , 2011, PLoS genetics.

[98]  G. Macfarlane,et al.  Short chain fatty acids in human large intestine, portal, hepatic and venous blood. , 1987, Gut.

[99]  F. Haesebrouck,et al.  Salmonella enterica serovar Enteritidis colonization of the chicken caecum requires the HilA regulatory protein. , 2006, Veterinary microbiology.

[100]  P. McDermott,et al.  Characterization of extended-spectrum cephalosporin-resistant Salmonella enterica serovar Heidelberg isolated from food animals, retail meat, and humans in the United States 2009. , 2012, Foodborne pathogens and disease.

[101]  K. Darwin,et al.  Molecular Basis of the Interaction ofSalmonella with the Intestinal Mucosa , 1999, Clinical Microbiology Reviews.

[102]  G. Tannock CHAPTER 20 – Effect of Dietary and Environmental Stress on the Gastrointestinal Microbiota , 1983 .

[103]  S. Ricke,et al.  Induced moulting issues and alternative dietary strategies for the egg industry in the United States , 2004 .

[104]  W. Demczuk,et al.  Drug resistance, plasmids, biotypes and susceptibility to bacteriophages of Salmonella isolated from poultry in Canada. , 1996, International journal of food microbiology.

[105]  G. Mead Microbes of the avian cecum: types present and substrates utilized. , 1989, The Journal of experimental zoology. Supplement : published under auspices of the American Society of Zoologists and the Division of Comparative Physiology and Biochemistry.

[106]  M. Levine,et al.  Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans , 1988, The Journal of experimental medicine.

[107]  Kathleen Marchal,et al.  A community effort towards a knowledge-base and mathematical model of the human pathogen Salmonella Typhimurium LT2 , 2011, BMC Systems Biology.

[108]  S. Akira,et al.  Differential inductions of TNF‐α and IGTP, IIGP by structurally diverse classic and non‐classic lipopolysaccharides , 2006, Cellular microbiology.

[109]  G. Macfarlane,et al.  Human colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria. , 1997, Scandinavian journal of gastroenterology. Supplement.

[110]  R. Eckroade,et al.  Invasion of chicken reproductive tissues and forming eggs is not unique to Salmonella enteritidis. , 1997, Avian diseases.

[111]  B. Ahmer,et al.  The Virulence Plasmid of Salmonella typhimurium Is Self-Transmissible , 1999, Journal of bacteriology.

[112]  C. Chiu,et al.  EMERGENCE OF FLUOROQUINOLONE RESISTANCE IN SALMONELLA ENTERICA SEROTYPE CHOLERAESUIS THE EMERGENCE IN TAIWAN OF FLUOROQUINOLONE RESISTANCE IN SALMONELLA ENTERICA SEROTYPE CHOLERAESUIS , 2002 .

[113]  B. Finlay,et al.  Salmonella Phage ST64B Encodes a Member of the SseK/NleB Effector Family , 2011, PloS one.

[114]  Joshua Xu,et al.  DNA Sequence Analysis of Plasmids from Multidrug Resistant Salmonella enterica Serotype Heidelberg Isolates , 2012, PloS one.

[115]  B. Hurley,et al.  Translating tissue culture results into animal models: the case of Salmonella typhimurium. , 2003, Trends in microbiology.

[116]  Yunsong Yu,et al.  Emergence of NDM-1-producing Acinetobacter baumannii in China. , 2011, The Journal of antimicrobial chemotherapy.

[117]  L. H. Cheng,et al.  Egg consumption is the principal risk factor for sporadic Salmonella serotype Heidelberg infections: a case-control study in FoodNet sites. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[118]  T. Whittam,et al.  Evolutionary origin and radiation of the avian-adapted non-motile salmonellae. , 1993, Journal of medical microbiology.

[119]  D. Vugia,et al.  Invasive Salmonella infections in the United States, FoodNet, 1996-1999: incidence, serotype distribution, and outcome. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[120]  F. Haesebrouck,et al.  Salmonella Enteritidis universal stress protein (usp) gene expression is stimulated by egg white and supports oviduct colonization and egg contamination in laying hens. , 2011, Veterinary microbiology.

[121]  P. Weimer Cellulose Degradation by Ruminal Microorganisms , 1992 .

[122]  JAMES L. Smith,et al.  The role of gastric acid in preventing foodborne disease and how bacteria overcome acid conditions. , 2003, Journal of food protection.

[123]  B. Appel,et al.  Antimicrobial Resistance and Virulence Determinants in European Salmonella Genomic Island 1-Positive Salmonella enterica Isolates from Different Origins , 2011, Applied and Environmental Microbiology.

[124]  S. Ricke,et al.  Molting in Salmonella Enteritidis-challenged laying hens fed alfalfa crumbles. II. Fermentation and microbial ecology response. , 2007, Poultry science.

[125]  J. Folster,et al.  Characterization of bla(CMY)-encoding plasmids among Salmonella isolated in the United States in 2007. , 2011, Foodborne pathogens and disease.

[126]  S. Ricke,et al.  Induction of resistance of Salmonella typhimurium to environmental stresses by exposure to short-chain fatty acids , 2000 .

[127]  S. Ricke,et al.  The gastrointestinal tract ecology of Salmonella enteritidis colonization in molting hens. , 2003, Poultry science.

[128]  E. Groisman,et al.  At Least Four Percent of the Salmonella typhimurium Genome Is Required for Fatal Infection of Mice , 1998, Infection and Immunity.

[129]  B. McCormick,et al.  Salmonella Interaction with and Passage through the Intestinal Mucosa: Through the Lens of the Organism , 2011, Front. Microbio..

[130]  S. Ricke,et al.  Molting in Salmonella enteritidis-challenged laying hens fed alfalfa crumbles. I. Salmonella enteritidis colonization and virulence gene hilA response. , 2007, Poultry science.

[131]  F. Haesebrouck,et al.  Invasion of Salmonella enteritidis in avian intestinal epithelial cells in vitro is influenced by short-chain fatty acids. , 2003, International journal of food microbiology.

[132]  James M. Slauch,et al.  Identification of GtgE, a Novel Virulence Factor Encoded on the Gifsy-2 Bacteriophage of Salmonella enterica Serovar Typhimurium , 2002, Journal of bacteriology.

[133]  M. Spector The starvation-stress response (SSR) of Salmonella. , 1998, Advances in microbial physiology.

[134]  J. Foster,et al.  The acid tolerance response of Salmonella typhimurium provides protection against organic acids. , 1996, Microbiology.

[135]  F. Haesebrouck,et al.  Mechanisms of egg contamination by Salmonella Enteritidis. , 2009, FEMS microbiology reviews.

[136]  R. Karpíšková,et al.  Low-Molecular-Weight Plasmid of Salmonella enterica Serovar Enteritidis Codes for Retron Reverse Transcriptase and Influences Phage Resistance , 2001, Journal of bacteriology.

[137]  K. Kniel,et al.  Comparison of genetic and physiological properties of Salmonella enterica isolates from chickens reveals one major difference between serovar Kentucky and other serovars: response to acid. , 2009, Foodborne pathogens and disease.

[138]  S. Farr,et al.  Oxidative stress responses in Escherichia coli and Salmonella typhimurium. , 1991, Microbiological reviews.

[139]  Amy K. Cain,et al.  Evolution of a multiple antibiotic resistance region in IncHI1 plasmids: reshaping resistance regions in situ. , 2012, The Journal of antimicrobial chemotherapy.

[140]  B. Finlay,et al.  Type III effector-mediated processes in Salmonella infection. , 2012, Future microbiology.

[141]  W. Hardt,et al.  The Salmonella enterica Serotype Typhimurium Effector Proteins SipA, SopA, SopB, SopD, and SopE2 Act in Concert To Induce Diarrhea in Calves , 2002, Infection and Immunity.

[142]  Shuping Zhang,et al.  Molecular Pathogenesis of Salmonella enterica Serotype Typhimurium-Induced Diarrhea , 2003, Infection and Immunity.

[143]  G. Macfarlane,et al.  The control and consequences of bacterial fermentation in the human colon. , 1991, The Journal of applied bacteriology.

[144]  M. Friedrich,et al.  Nucleotide sequence of a 13.9 kb segment of the 90 kb virulence plasmid of Salmonella typhimurium: the presence of fimbriai biosynthetic genes , 1993, Molecular microbiology.

[145]  D. Kamra Rumen microbial ecosystem , 2005 .

[146]  F. Boyen,et al.  The fibronectin binding protein ShdA is not a prerequisite for long term faecal shedding of Salmonella typhimurium in pigs. , 2006, Veterinary microbiology.

[147]  P. Weimer,et al.  Lessons from the cow: what the ruminant animal can teach us about consolidated bioprocessing of cellulosic biomass. , 2009, Bioresource technology.

[148]  L. Peixe,et al.  First description of qnrS1-IncN plasmid in a ST11 Salmonella Enteritidis clinical isolate from Portugal. , 2011, Diagnostic microbiology and infectious disease.

[149]  J. Garrett Morris,et al.  Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. , 2012, Journal of food protection.

[150]  S. Winter,et al.  The Salmonella enterica serotype Typhi regulator TviA reduces interleukin‐8 production in intestinal epithelial cells by repressing flagellin secretion , 2007, Cellular microbiology.

[151]  B. Guerra,et al.  IncA/C plasmids mediate antimicrobial resistance linked to virulence genes in the Spanish clone of the emerging Salmonella enterica serotype 4,[5],12:i:-. , 2011, The Journal of antimicrobial chemotherapy.

[152]  J. Alverdy,et al.  Effect of immunonutrition on virulence strategies in bacteria. , 1998, Nutrition.

[153]  S. Pillai,et al.  Incidence, sources, and control of food-borne Salmonella spp. in poultry feeds , 2004 .

[154]  D. David,et al.  Comparison of Salmonella enterica Serovar Heidelberg Isolates from Human Patients with Those from Animal and Food Sources , 2010, Journal of Clinical Microbiology.

[155]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[156]  D. David,et al.  Characterization of antimicrobial resistance in Salmonella enterica serotype Heidelberg isolated from food animals. , 2009, Foodborne pathogens and disease.

[157]  T. Mignot,et al.  A Bacterial Ras-Like Small GTP-Binding Protein and Its Cognate GAP Establish a Dynamic Spatial Polarity Axis to Control Directed Motility , 2010, PLoS biology.

[158]  D. E. Bradley,et al.  Bacteriophage X-2: a filamentous phage lysing IncX-plasmid-harbouring bacterial strains. , 1988, Journal of general microbiology.

[159]  Lisa H. Orfe,et al.  Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system. , 2011, Microbiology.

[160]  W. Kay,et al.  Unique fimbriae‐like structures encoded by sefD of the SEF14 fimbrial gene cluster of Salmonella enteritidis , 1994, Molecular microbiology.

[161]  F. Haesebrouck,et al.  Adhesion of Salmonella enterica serotype Enteritidis isolates to chicken isthmal glandular secretions. , 2003, Veterinary microbiology.

[162]  M. Lotze,et al.  PAMPs and DAMPs: signal 0s that spur autophagy and immunity , 2012, Immunological reviews.

[163]  J. Galán,et al.  Salmonella interactions with host cells: type III secretion at work. , 2001, Annual review of cell and developmental biology.

[164]  Pietro Liò,et al.  Analysis of plasmid genes by phylogenetic profiling and visualization of homology relationships using Blast2Network , 2008, BMC Bioinformatics.

[165]  Steven C. Ricke,et al.  Cell yields and fermentation responses of a Salmonella Typhimurium poultry isolate at different dilution rates in an anaerobic steady state continuous culture , 2009, Antonie van Leeuwenhoek.

[166]  M. E. Potter,et al.  Salmonella enterica serovar enteritidis in humans and animals : epidemiology, pathogenesis, and control , 1999 .

[167]  D. Call,et al.  Transposon Mutagenesis of Salmonella enterica Serovar Enteritidis Identifies Genes That Contribute to Invasiveness in Human and Chicken Cells and Survival in Egg Albumen , 2012, Infection and Immunity.

[168]  J. Casadesús,et al.  The virulence plasmids of Salmonella. , 1999, International microbiology : the official journal of the Spanish Society for Microbiology.

[169]  Robert A. Kingsley,et al.  The shdA Gene Is Restricted to Serotypes ofSalmonella enterica Subspecies I and Contributes to Efficient and Prolonged Fecal Shedding , 2000, Infection and Immunity.

[170]  Ferric C. Fang,et al.  Taming the Elephant: Salmonella Biology, Pathogenesis, and Prevention , 2010, Infection and Immunity.

[171]  C. Chiu,et al.  Salmonella enterica Serotype Choleraesuis: Epidemiology, Pathogenesis, Clinical Disease, and Treatment , 2004, Clinical Microbiology Reviews.

[172]  J. E. Olsen,et al.  Differences in the carriage and the ability to utilize the serotype associated virulence plasmid in strains of Salmonella enterica serotype Typhimurium investigated by use of a self-transferable virulence plasmid, pOG669. , 2004, Microbial pathogenesis.

[173]  P. Barrow,et al.  Identification of Salmonella typhimuriumGenes Required for Colonization of the Chicken Alimentary Tract and for Virulence in Newly Hatched Chicks , 1998, Infection and Immunity.

[174]  A. Fluit Towards more virulent and antibiotic-resistant Salmonella? , 2005, FEMS immunology and medical microbiology.

[175]  M. Bohnhoff,et al.  A Study of Experimental Salmonella Infection in the Mouse , 1962 .

[176]  A. Fruth,et al.  Salmonella enterotoxin (stn) gene is prevalent among strains of Salmonella enterica, but not among Salmonella bongori and other Enterobacteriaceae. , 1995, FEMS immunology and medical microbiology.

[177]  T. Eklund The antimicrobial effect of dissociated and undissociated sorbic acid at different pH levels. , 1983, The Journal of applied bacteriology.

[178]  John Painter,et al.  Attributing Illness to Food , 2005, Emerging infectious diseases.

[179]  S. Ricke,et al.  Immediate Reduction of Salmonella enterica Serotype Typhimurium Viability via Membrane Destabilization following Exposure to Multiple-Hurdle Treatments with Heated, Acidified Organic Acid Salt Solutions , 2011, Applied and Environmental Microbiology.

[180]  D. Sherratt,et al.  Small Plasmids Harboring qnrB19: a Model for Plasmid Evolution Mediated by Site-Specific Recombination at oriT and Xer Sites , 2012, Antimicrobial Agents and Chemotherapy.

[181]  V. Sintchenko,et al.  Genetic Relationships of Phage Types and Single Nucleotide Polymorphism Typing of Salmonella enterica Serovar Typhimurium , 2011, Journal of Clinical Microbiology.

[182]  A. V. Asten,et al.  Distribution of “classic” virulence factors among Salmonella spp. , 2005 .

[183]  R. H. Bailey,et al.  Presence of Salmonella in the crop and ceca of broiler chickens before and after preslaughter feed withdrawal. , 1999, Poultry science.

[184]  V. Vaillant,et al.  Outbreak of Salmonella enterica serotype Montevideo infections in France linked to consumption of cheese made from raw milk. , 2009, Foodborne pathogens and disease.

[185]  R. B. Hespell Efficiency of growth by ruminal bacteria. , 1979, Federation proceedings.

[186]  R. Elson,et al.  Salmonella and raw shell eggs: results of a cross-sectional study of contamination rates and egg safety practices in the United Kingdom catering sector in 2003. , 2005, Journal of food protection.

[187]  J. V. van Dijk,et al.  Distribution of "classic" virulence factors among Salmonella spp. , 2005, FEMS immunology and medical microbiology.

[188]  C. Thorns,et al.  Studies into the role of the SEF14 fimbrial antigen in the pathogenesis of Salmonella enteritidis. , 1996, Microbial pathogenesis.

[189]  D. Maskell,et al.  Genomic Comparison of the Closely Related Salmonella enterica Serovars Enteritidis and Dublin , 2012, The open microbiology journal.

[190]  H. Ochman,et al.  How Salmonella became a pathogen. , 1997, Trends in microbiology.

[191]  J. Wain,et al.  A clinical, microbiological, and pathological study of intestinal perforation associated with typhoid fever. , 2004, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[192]  K. Seo,et al.  Comparison of Salmonella Enteritidis infection in hens molted via long-term feed withdrawal versus full-fed wheat middling. , 2001, Journal of food protection.

[193]  C. Wray,et al.  A survey of antimicrobial resistance in Salmonellae isolated from animals in England and Wales during 1984-1987. , 1991, The British veterinary journal.

[194]  D. Holden,et al.  Trafficking of the Salmonella Vacuole in Macrophages , 2002, Traffic.

[195]  F. Weill,et al.  Comparative Analysis of IncHI2 Plasmids Carrying blaCTX-M-2 or blaCTX-M-9 from Escherichia coli and Salmonella enterica Strains Isolated from Poultry and Humans , 2007, Antimicrobial Agents and Chemotherapy.

[196]  J. Wain,et al.  International spread of an epidemic population of Salmonella enterica serotype Kentucky ST198 resistant to ciprofloxacin. , 2011, The Journal of infectious diseases.

[197]  J. Foster,et al.  How Salmonella survive against the odds. , 1995, Annual review of microbiology.

[198]  Steven C. Ricke,et al.  Population Dynamics of Salmonella enterica Serotypes in Commercial Egg and Poultry Production , 2011, Applied and Environmental Microbiology.

[199]  T. Humphrey,et al.  Influence of feeding patterns on the artificial infection of laying hens with Salmonella enteritidis phage type 4 , 1993, Veterinary Record.

[200]  R. E. Hungate,et al.  The Rumen and Its Microbes , 2013 .

[201]  T. Bannerman,et al.  A multistate outbreak of Salmonella enterica serotype typhimurium infection linked to raw milk consumption--Ohio, 2003. , 2004, Journal of food protection.

[202]  J. Escalante‐Semerena,et al.  In Salmonella enterica, 2-Methylcitrate Blocks Gluconeogenesis , 2009, Journal of bacteriology.

[203]  T. Wallis,et al.  The Early Dynamic Response of the Calf Ileal Epithelium to Salmonella typhimurium , 1997, Veterinary pathology.

[204]  M. Woodward,et al.  Cloning, DNA nucleotide sequence and distribution of the gene encoding the SEF14 fimbrial antigen of Salmonella enteritidis. , 1993, Journal of general microbiology.

[205]  R. Isaacson,et al.  Type 1 Fimbriae of Salmonella enterica Serovar Typhimurium Bind to Enterocytes and Contribute to Colonization of Swine In Vivo , 2003, Infection and Immunity.

[206]  B. Rowe,et al.  Acquisition of a drug resistance plasmid converts Salmonella enteritidis phage type 4 to phage type 24 , 1989, Epidemiology and Infection.

[207]  E. Siebor,et al.  The new variant of Salmonella genomic island 1 (SGI1-V) from a Proteus mirabilis French clinical isolate harbours blaVEB-6 and qnrA1 in the multiple antibiotic resistance region. , 2011, The Journal of antimicrobial chemotherapy.

[208]  J. Galán,et al.  Campylobacter jejuni Survives within Epithelial Cells by Avoiding Delivery to Lysosomes , 2008, PLoS pathogens.

[209]  W. Rabsch,et al.  [Characterization and epidemiology of a Salmonella typhimurium epidemic strain]. , 1982, Zeitschrift fur arztliche Fortbildung.

[210]  K. Carroll,et al.  First NDM-Positive Salmonella sp. Strain Identified in the United States , 2011, Antimicrobial Agents and Chemotherapy.

[211]  L. Emödy,et al.  Shigella dysenteriae 1-like cytotoxic enterotoxins produced by Salmonella strains. , 1979, Acta microbiologica Academiae Scientiarum Hungaricae.

[212]  Laura E. Williams,et al.  Large plasmids of Escherichia coli and Salmonella encode highly diverse arrays of accessory genes on common replicon families. , 2013, Plasmid.

[213]  L. L. Nesse,et al.  Control of Salmonella in food related environments by chemical disinfection , 2012 .

[214]  A. Smith,et al.  Age at primary infection with Salmonella enterica serovar Typhimurium in the chicken influences persistence of infection and subsequent immunity to re-challenge. , 2004, Veterinary immunology and immunopathology.

[215]  B. Ahmer,et al.  Interaction of Salmonella spp. with the Intestinal Microbiota , 2011, Front. Microbio..

[216]  D. David,et al.  Genetic characterization of antimicrobial resistance in Salmonella enterica serovars isolated from dairy cattle in Wisconsin , 2012 .

[217]  Arin L. Zirnheld,et al.  Gut Microbiota, Immunity, and Disease: A Complex Relationship , 2011, Front. Microbio..

[218]  R. W. Moore,et al.  Colonization of Specific Regions of the Reproductive Tract and Deposition at Different Locations Inside Eggs Laid by Hens Infected with Salmonella Enteritidis or Salmonella Heidelberg , 2007, Avian diseases.

[219]  S. Ricke,et al.  Induction of Acid Resistance of Salmonella typhimurium by Exposure to Short-Chain Fatty Acids , 1998, Applied and Environmental Microbiology.

[220]  D. David,et al.  Characterisation of antibiotic resistance in host-adapted Salmonella enterica. , 2009, International journal of antimicrobial agents.

[221]  A. Bäumler,et al.  How To Become a Top Model: Impact of Animal Experimentation on Human Salmonella Disease Research , 2011, Infection and Immunity.

[222]  G. Karnam,et al.  Differentially Evolved Genes of Salmonella Pathogenicity Islands: Insights into the Mechanism of Host Specificity in Salmonella , 2008, PloS one.

[223]  J. Russell,et al.  Microbial rumen fermentation. , 1981, Journal of dairy science.

[224]  L. Bossi,et al.  Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella , 2001, Molecular microbiology.

[225]  S. Ricke,et al.  Ecology, metabolism, and genetics of ruminal selenomonads. , 1996, Critical reviews in microbiology.

[226]  H. de Jong,et al.  Salmonellosis in calves--the effect of dose rate and other factors on transmission. , 1965, New Zealand veterinary journal.

[227]  M. Huggins,et al.  Host specificity of Salmonella infection in chickens and mice is expressed in vivo primarily at the level of the reticuloendothelial system , 1994, Infection and immunity.

[228]  S. Ricke,et al.  LATE LOGARITHMIC SALMONELLA TYPHIMURIUM HEp‐2 CELL ASSOCIATION AND INVASION RESPONSE TO SHORT‐CHAIN FATTY ACID ADDITION , 2000 .

[229]  J. Prescott,et al.  Salmonella enterica serovar enteritidis in humans and animals : epidemiology, pathogenesis, and control , 1999 .

[230]  K. Leung,et al.  Type VI secretion regulation: crosstalk and intracellular communication. , 2011, Current opinion in microbiology.

[231]  S. Ricke,et al.  In vitro fermentation response of laying hen cecal bacteria to combinations of fructooligosaccharide prebiotics with alfalfa or a layer ration. , 2008, Poultry science.

[232]  S. Ricke,et al.  Short chain fatty acids alter HEp-2 cell association and invasion by stationary growth phase Salmonella typhimurium , 2000 .

[233]  D. Monack,et al.  Salmonella's long-term relationship with its host. , 2012, FEMS microbiology reviews.

[234]  A. Kalergis,et al.  Mechanisms used by virulent Salmonella to impair dendritic cell function and evade adaptive immunity , 2012, Immunology.

[235]  A. Bäumler,et al.  From bench to bedside: stealth of enteroinvasive pathogens , 2008, Nature Reviews Microbiology.

[236]  A. Berndt,et al.  Exploitation of Intestinal Colonization‐Inhibition Between Salmonella Organisms for Live Vaccines in Poultry – Potential and Limitations , 2011, Zoonoses and public health.

[237]  A. Bhunia,et al.  Effect of sublethal heat stress on Salmonella Typhimurium virulence , 2011, Journal of applied microbiology.

[238]  Sang J. Shin,et al.  Salmonella enterica Serotype Dublin Infection: an Emerging Infectious Disease for the Northeastern United States , 1999, Journal of Clinical Microbiology.

[239]  J. Burnside,et al.  Differential cytokine expression in avian cells in response to invasion by Salmonella typhimurium, Salmonella enteritidis and Salmonella gallinarum. , 2000, Microbiology.

[240]  P. Roy,et al.  Results of Salmonella Isolation from Poultry Products, Poultry, Poultry Environment, and Other Characteristics , 2002, Avian diseases.

[241]  C. Chiu,et al.  Pseudogene recoding revealed from proteomic analysis of salmonella serovars. , 2012, Journal of proteome research.

[242]  R. L. La Ragione,et al.  Differences in Salmonella enterica serovar Typhimurium strain invasiveness are associated with heterogeneity in SPI-1 gene expression , 2011, Microbiology.

[243]  S. Ricke,et al.  Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. , 2003, Poultry science.

[244]  D. Holden,et al.  Bacterial interactions with the eukaryotic secretory pathway. , 2005, Current opinion in microbiology.

[245]  J. Wain,et al.  Unlocking the genome of the human typhoid bacillus. , 2002, The Lancet. Infectious diseases.

[246]  S. Sørensen,et al.  Investigation of diversity of plasmids carrying the blaTEM-52 gene. , 2011, The Journal of antimicrobial chemotherapy.

[247]  M. P. Bryant,et al.  Efficiency of rumen microbial growth: influence of some theoretical and experimental factors of YATP. , 1979, Journal of animal science.

[248]  L. Herman,et al.  Limited Genetic Diversity and Gene Expression Differences between Egg‐ and Non‐Egg‐Related Salmonella Enteritidis Strains , 2009, Zoonoses and public health.

[249]  L R Ward,et al.  Spread of multiresistant strains of Salmonella typhimurium phage types 204 and 193 in Britain. , 1978, British medical journal.

[250]  F. Heffron,et al.  Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella typhimurium , 1995, Journal of bacteriology.

[251]  R. Wiegert,et al.  A simulation of microbial competition in the human colonic ecosystem , 1996, Applied and environmental microbiology.

[252]  A. Tiérrez,et al.  New concepts in Salmonella virulence: the importance of reducing the intracellular growth rate in the host , 2005, Cellular microbiology.

[253]  Russell Maurer,et al.  Intestinal short‐chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA , 2002, Molecular microbiology.

[254]  John-hwa Lee,et al.  Antimicrobial resistance of Salmonella isolated from food animals: A review , 2012 .

[255]  T. Cebula,et al.  Comparative Genomics of 28 Salmonella enterica Isolates: Evidence for CRISPR-Mediated Adaptive Sublineage Evolution , 2011, Journal of bacteriology.

[256]  E. Shotts,et al.  Effect of short-chain fatty acids on the growth of Salmonella typhimurium in an in vitro system. , 1993, Avian diseases.

[257]  O. Reva,et al.  Distribution of horizontally transferred heavy metal resistance operons in recent outbreak bacteria , 2012, Mobile genetic elements.

[258]  P. Gulig,et al.  Regulation of the spvR gene of the Salmonella typhimurium virulence plasmid during exponential-phase growth in intracellular salts medium and at stationary phase in L broth. , 1998, Microbiology.

[259]  A. Kalergis,et al.  Deletion of a prophage-like element causes attenuation of Salmonella enterica serovar Enteritidis and promotes protective immunity. , 2010, Vaccine.

[260]  B. Doublet,et al.  The Salmonella Genomic Island 1 Is Specifically Mobilized In Trans by the IncA/C Multidrug Resistance Plasmid Family , 2010, PloS one.

[261]  C. Schmerk,et al.  The Francisella Pathogenicity Island , 2007, Annals of the New York Academy of Sciences.

[262]  C. Chiu,et al.  Lack of Evidence of an Association between the Carriage of Virulence Plasmid and the Bacteremia of Salmonella typhimurium in Humans , 2000, Microbiology and immunology.

[263]  E. J. Threlfall,et al.  pSGI15, a small ColE-like qnrB19 plasmid of a Salmonella enterica serovar Typhimurium strain carrying Salmonella genomic island 1 (SGI1). , 2010, The Journal of antimicrobial chemotherapy.

[264]  A. Carattoli,et al.  Comparative genomics and phylogeny of the IncI1 plasmids: a common plasmid type among porcine enterotoxigenic Escherichia coli. , 2011, Plasmid.

[265]  L. Ursell,et al.  Gut Microbiomes of Malawian Twin Pairs Discordant for Kwashiorkor , 2013, Science.

[266]  T. Marlovits,et al.  Structural Insights into the Assembly of the Type III Secretion Needle Complex , 2004, Science.

[267]  Salmonella typhimurium infection associated with raw milk and cheese consumption--Pennsylvania, 2007. , 2007, MMWR. Morbidity and mortality weekly report.

[268]  N. Thomson,et al.  Analysis of the role of 13 major fimbrial subunits in colonisation of the chicken intestines by Salmonella enterica serovar Enteritidis reveals a role for a novel locus , 2008, BMC Microbiology.

[269]  L. Knodler,et al.  Taking Possession: Biogenesis of the Salmonella‐Containing Vacuole , 2003, Traffic.

[270]  F. Haesebrouck,et al.  The use of organic acids to combat Salmonella in poultry: a mechanistic explanation of the efficacy , 2006, Avian pathology : journal of the W.V.P.A.

[271]  M. Gilmour,et al.  The complete nucleotide sequence of the resistance plasmid R478: defining the backbone components of incompatibility group H conjugative plasmids through comparative genomics. , 2004, Plasmid.

[272]  J. Celli,et al.  Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia , 2010, Proceedings of the National Academy of Sciences.

[273]  I. Hanning,et al.  Salmonella enterica isolates from pasture‐raised poultry exhibit antimicrobial resistance and class I integrons , 2010, Journal of applied microbiology.

[274]  C W Hedberg,et al.  A national outbreak of Salmonella enteritidis infections from ice cream. The Investigation Team. , 1996 .

[275]  T. Cebula,et al.  Diagnostic potential of sefA DNA probes to Salmonella enteritidis and certain other O-serogroup D1 Salmonella serovars. , 1996, Molecular and cellular probes.

[276]  J. Stanley,et al.  Salmonella plasmids of the pre-antibiotic era. , 1992, Journal of general microbiology.

[277]  Alison G Lee,et al.  Genomic rearrangements at rrn operons in Salmonella. , 2003, Genetics.

[278]  F. Grau,et al.  Effect of food intake on growth and survival of salmonellas and Escherichia coli in the bovine rumen. , 1967, Journal of general microbiology.

[279]  Steven C Ricke,et al.  Ecology and characteristics of methanogenic archaea in animals and humans , 2014, Critical reviews in microbiology.

[280]  R. Guerrant,et al.  Principles and Syndromes of Enteric Infection , 2010 .

[281]  J. E. Olsen,et al.  Phage type conversion in Salmonella enterica serotype Enteritidis caused by the introduction of a resistance plasmid of incompatibility group X (IncX) , 1999, Epidemiology and Infection.

[282]  S. Ricke,et al.  Feed Deprivation Affects Crop Environment and Modulates Salmonella enteritidis Colonization and Invasion of Leghorn Hens , 1999, Applied and Environmental Microbiology.

[283]  I. Chopra,et al.  Organic acids: chemistry, antibacterial activity and practical applications. , 1991, Advances in microbial physiology.

[284]  J. Volf,et al.  Virulence potential of five major pathogenicity islands (SPI-1 to SPI-5) of Salmonella enterica serovar Enteritidis for chickens , 2009, BMC Microbiology.

[285]  J. Casadesús,et al.  Conjugal Transfer of the Salmonella enterica Virulence Plasmid in the Mouse Intestine , 2008, Journal of bacteriology.

[286]  S. Ricke,et al.  Growth and genetic responses of Salmonella Typhimurium to pH-shifts in an anaerobic continuous culture. , 2008, Anaerobe.

[287]  J. Dewulf,et al.  Salmonella Enteritidis is superior in egg white survival compared with other Salmonella serotypes. , 2013, Poultry science.

[288]  A. Wanger,et al.  Quantitative analysis and partial characterization of cytotoxin production by Salmonella strains , 1988, Infection and immunity.

[289]  T. Ficht,et al.  Evolution of Host Adaptation inSalmonella enterica , 1998, Infection and Immunity.

[290]  J. Guard-Petter The chicken, the egg and Salmonella enteritidis. , 2001, Environmental microbiology.

[291]  A. Potter,et al.  Salmonella enterica Serovar Enteritidis Pathogenicity Island 1 Is Not Essential for but Facilitates Rapid Systemic Spread in Chickens , 2009, Infection and Immunity.

[292]  D. Józefiak,et al.  Carbohydrate fermentation in the avian ceca: a review , 2004 .

[293]  J. Goepfert,et al.  Effect of volatile fatty acids on Salmonella typhimurium , 1969, Journal of bacteriology.

[294]  F. Haesebrouck,et al.  Salmonella enterica Serovar Enteritidis Genes Induced during Oviduct Colonization and Egg Contamination in Laying Hens , 2008, Applied and Environmental Microbiology.

[295]  S. Altekruse,et al.  A comparison of Salmonella enteritidis phage types from egg-associated outbreaks and implicated laying flocks , 1993, Epidemiology and Infection.

[296]  G. Leyer,et al.  Acid adaptation promotes survival of Salmonella spp. in cheese , 1992, Applied and environmental microbiology.

[297]  Mark P Stevens,et al.  Identification of host‐specific colonization factors of Salmonella enterica serovar Typhimurium , 2004, Molecular microbiology.

[298]  S. Ricke,et al.  Comparison of in vitro fermentation and molecular microbial profiles of high-fiber feed substrates incubated with chicken cecal inocula. , 2007, Poultry science.

[299]  T S Wallis,et al.  Molecular basis of Salmonella‐induced enteritis , 2000, Molecular microbiology.

[300]  J. Casadesús,et al.  Virulence plasmid interchange between strains ATCC 14028, LT2, and SL1344 of Salmonella enterica serovar Typhimurium. , 2011, Plasmid.

[301]  B. Kuehn Salmonella cases traced to egg producers: findings trigger recall of more than 500 million eggs. , 2010, JAMA.

[302]  C. O’Byrne,et al.  Weak Organic Acids: A Panoply of Effects on Bacteria , 2003, Science progress.

[303]  S. Ricke,et al.  Effects of nitro compounds and feedstuffs on in vitro methane production in chicken cecal contents and rumen fluid. , 2006, Anaerobe.

[304]  T. Johnson,et al.  DNA Sequence and Comparative Genomics of pAPEC-O2-R, an Avian Pathogenic Escherichia coli Transmissible R Plasmid , 2005, Antimicrobial Agents and Chemotherapy.

[305]  W. Rabsch,et al.  Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[306]  N. Moran,et al.  Genes Lost and Genes Found: Evolution of Bacterial Pathogenesis and Symbiosis , 2001, Science.

[307]  M. R. Evans,et al.  Analysis of the ArcA regulon in anaerobically grown Salmonella enterica sv. Typhimurium , 2011, BMC Microbiology.

[308]  R. Mackie Mutualistic Fermentative Digestion in the Gastrointestinal Tract: Diversity and Evolution1 , 2002, Integrative and comparative biology.

[309]  Michael McClelland,et al.  The Fur regulon in anaerobically grown Salmonella enterica sv. Typhimurium: identification of new Fur targets , 2011, BMC Microbiology.

[310]  P. Majerus,et al.  SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[311]  W. F. Fricke,et al.  Horizontal Gene Transfer of a ColV Plasmid Has Resulted in a Dominant Avian Clonal Type of Salmonella enterica Serovar Kentucky , 2010, PloS one.

[312]  I. Uchida,et al.  Characterization of Salmonella enterica Serovar Typhimurium Isolates Harboring a Chromosomally Encoded CMY-2 β-Lactamase Gene Located on a Multidrug Resistance Genomic Island , 2011, Antimicrobial Agents and Chemotherapy.

[313]  S. Ricke,et al.  Microbial ecology of the gastrointestinal tract of fish and the potential application of prebiotics and probiotics in finfish aquaculture , 2005 .

[314]  L. Florea,et al.  Characterization of Salmonella enterica Subspecies I Genovars by Use of Microarrays , 2004, Journal of bacteriology.

[315]  R. Eckroade,et al.  Salmonella enteritidis colonization of the reproductive tract and forming and freshly laid eggs of chickens , 1995, Infection and immunity.

[316]  Rene S. Hendriksen,et al.  The Salmonella enterica Pan-genome , 2011, Microbial Ecology.

[317]  S. Ricke,et al.  Synergistic reduction of Salmonella in a model raw chicken media using a combined thermal and acidified organic acid salt intervention treatment. , 2010, Journal of food science.

[318]  K. Hopkins,et al.  Potential International Spread of Multidrug-Resistant Invasive Salmonella enterica Serovar Enteritidis , 2012, Emerging infectious diseases.

[319]  Catherine A. Lee,et al.  Invasion Genes Are Not Required for Salmonella enterica Serovar Typhimurium To Breach the Intestinal Epithelium: Evidence That Salmonella Pathogenicity Island 1 Has Alternative Functions during Infection , 2000, Infection and Immunity.

[320]  A. Carattoli,et al.  Integrons and Transposons on the Salmonellaenterica Serovar Typhimurium Virulence Plasmid , 2005, Antimicrobial Agents and Chemotherapy.

[321]  J. Russell,et al.  Another explanation for the toxicity of fermentation acids at low pH: anion accumulation versus uncoupling , 1992 .

[322]  G. Węgrzyn,et al.  Plasmids derived from Gifsy-1/Gifsy-2, lambdoid prophages contributing to the virulence of Salmonella enterica serovar Typhimurium: implications for the evolution of replication initiation proteins of lambdoid phages and enterobacteria. , 2007, Microbiology.

[323]  B. Finlay,et al.  Host–microbe interactions , 2007, Nature.

[324]  J. Clemente,et al.  Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans , 2011, Science.

[325]  S. Ricke,et al.  Expression of the hilA Salmonella typhimurium gene in a poultry Salm. enteritidis isolate in response to lactate and nutrients , 2000, Journal of applied microbiology.

[326]  B. Finlay,et al.  Enteropathogenic E. coli, Salmonella, and Shigella: masters of host cell cytoskeletal exploitation. , 1999, Emerging infectious diseases.

[327]  Herbert Schmidt,et al.  Pathogenicity Islands in Bacterial Pathogenesis , 2004, Clinical Microbiology Reviews.

[328]  H. Ochman,et al.  Short-Term Signatures of Evolutionary Change in the Salmonella enterica Serovar Typhimurium 14028 Genome , 2009, Journal of bacteriology.

[329]  Xiao-lian Zhang,et al.  Salmonella enterica Serovar Typhi Uses Type IVB Pili To Enter Human Intestinal Epithelial Cells , 2000, Infection and Immunity.

[330]  Hespell Rb Efficiency of growth by ruminal bacteria. , 1979 .

[331]  L. Florea,et al.  Differences in Gene Content between Salmonella enterica Serovar Enteritidis Isolates and Comparison to Closely Related Serovars Gallinarum and Dublin , 2005, Journal of bacteriology.

[332]  F. Haesebrouck,et al.  Long-term colonisation-inhibition studies to protect broilers against colonisation with Salmonella Enteritidis, using Salmonella Pathogenicity Island 1 and 2 mutants. , 2007, Vaccine.

[333]  W. Goebel,et al.  A cytolysin encoded by Salmonella is required for survival within macrophages. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[334]  C. Lostroh,et al.  The Salmonella pathogenicity island-1 type III secretion system. , 2001, Microbes and infection.

[335]  R. Kingsley,et al.  Fibronectin Binding to the Salmonella enterica Serotype Typhimurium ShdA Autotransporter Protein Is Inhibited by a Monoclonal Antibody Recognizing the A3 Repeat , 2004, Journal of bacteriology.

[336]  J. B. Turpin,et al.  Gene expression analysis of Salmonella enterica Enteritidis Nal(R) and Salmonella enterica Kentucky 3795 exposed to HCl and acetic acid in rich medium. , 2012, Foodborne pathogens and disease.

[337]  Cheng-Hsun Chiu,et al.  Salmonella: clinical importance and evolution of nomenclature. , 2007, Chang Gung medical journal.

[338]  T. Brocklehurst,et al.  The Lactic Acid-Induced Acid Tolerance Response in Salmonella enterica Serovar Typhimurium Induces Sensitivity to Hydrogen Peroxide , 2006, Applied and Environmental Microbiology.

[339]  S. Porwollik,et al.  Infection of Mice by Salmonella enterica Serovar Enteritidis Involves Additional Genes That Are Absent in the Genome of Serovar Typhimurium , 2011, Infection and Immunity.

[340]  A. Lynne,et al.  Salmonella challenges: prevalence in swine and poultry and potential pathogenicity of such isolates. , 2008, Journal of animal science.

[341]  Neal J. Golden,et al.  Review of induced molting by feed removal and contamination of eggs with Salmonella enterica serovar Enteritidis. , 2008, Veterinary microbiology.

[342]  J. E. Peters,et al.  Identification and Characterization of Novel Salmonella Mobile Elements Involved in the Dissemination of Genes Linked to Virulence and Transmission , 2012, PloS one.

[343]  R. Gast,et al.  Isolation of Salmonella enteritidis from internal organs of experimentally infected hens. , 1990, Avian diseases.

[344]  S. Ricke,et al.  Reduction of Salmonella enterica serovar enteritidis colonization and invasion by an alfalfa diet during molt in Leghorn hens. , 2005, Poultry science.

[345]  P. Markham,et al.  Variation between Pathogenic Serovars within Salmonella Pathogenicity Islands , 2003, Journal of bacteriology.

[346]  R. Kingsley,et al.  Salmonella enterica serotype Typhimurium ShdA is an outer membrane fibronectin‐binding protein that is expressed in the intestine , 2002, Molecular microbiology.

[347]  A. Aderem,et al.  Evasion of Toll-like receptor 5 by flagellated bacteria. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[348]  A. Maurelli Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. , 2007, FEMS microbiology letters.

[349]  J. Dewulf,et al.  The effect of oral administration of a homologous hilA mutant strain on the long-term colonization and transmission of Salmonella Enteritidis in broiler chickens. , 2008, Vaccine.

[350]  C. D. Garner,et al.  Formate Acts as a Diffusible Signal To Induce Salmonella Invasion , 2008, Journal of bacteriology.

[351]  H. Kiyono,et al.  Epithelial cell microRNAs in gut immunity , 2011, Nature Immunology.

[352]  M. Hensel,et al.  Cooperation of Salmonella pathogenicity islands 1 and 4 is required to breach epithelial barriers , 2008, Cellular microbiology.

[353]  J. E. Olsen,et al.  Genomic lineage of Salmonella enterica serotype Gallinarum. , 1996, Journal of medical microbiology.

[354]  T. Brocklehurst,et al.  The Acetic Acid Tolerance Response induces cross-protection to salt stress in Salmonella typhimurium. , 2006, International journal of food microbiology.

[355]  S. Ricke,et al.  Fermented Meat, Poultry, and Fish Products , 2007 .

[356]  J. Foster,et al.  A Low pH-Inducible, PhoPQ-Dependent Acid Tolerance Response Protects Salmonella typhimurium against Inorganic Acid Stress , 1998, Journal of bacteriology.

[357]  Zhongming Zhao,et al.  The current Salmonella‐host interactome , 2012, Proteomics. Clinical applications.

[358]  P. Kaiser Advances in avian immunology—prospects for disease control: a review , 2010, Avian pathology : journal of the W.V.P.A.

[359]  Nan Zhang,et al.  Expression of hilA in response to mild acid stress in Salmonella enterica is serovar and strain dependent. , 2012, Journal of food science.

[360]  S. Ricke,et al.  Environmental Dissemination of Foodborne Salmonella in Preharvest Poultry Production: Reservoirs, Critical Factors, and Research Strategies , 2008 .

[361]  Amita Sharma,et al.  Vi polysaccharide of Salmonella typhi targets the prohibitin family of molecules in intestinal epithelial cells and suppresses early inflammatory responses. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[362]  J. Leong,et al.  The Tir‐binding region of enterohaemorrhagic Escherichia coli intimin is sufficient to trigger actin condensation after bacterial‐induced host cell signalling , 1999, Molecular microbiology.

[363]  Nicola C. Reading,et al.  The Starting Lineup: Key Microbial Players in Intestinal Immunity and Homeostasis , 2011, Front. Microbio..

[364]  D. Paterson,et al.  Novel Integron Gene Cassette Arrays Identified in a Global Collection of Multi-Drug Resistant Non-Typhoidal Salmonellaenterica , 2010, Current Microbiology.

[365]  Sandra Hoffmann,et al.  Ranking the Risks: The 10 PaThogen-Food CombinaTions WiTh The greaTesT burden on PubliC healTh , 2011 .

[366]  T. Johnson,et al.  Complete DNA Sequence of a ColBM Plasmid from Avian Pathogenic Escherichia coli Suggests that It Evolved from Closely Related ColV Virulence Plasmids , 2006, Journal of bacteriology.

[367]  R. Kenworthy,et al.  Volatile fatty acids in the digestive tract of the fowl , 1968, British Journal of Nutrition.

[368]  K. Hopkins,et al.  Frequency and polymorphism of sopE in isolates of Salmonella enterica belonging to the ten most prevalent serotypes in England and Wales. , 2004, Journal of medical microbiology.

[369]  K. Sanderson,et al.  The location of four fimbrin-encoding genes, agfA, fimA, sefA and sefD, on the Salmonella enteritidis and/or S. typhimurium XbaI-BlnI genomic restriction maps. , 1996, Gene.

[370]  B. Hargis,et al.  Provision of lactose to molting hens enhances resistance to Salmonella enteritidis colonization. , 1997, Journal of Food Protection.

[371]  D. Chakravortty,et al.  Salmonella enterica serovars Typhimurium and Typhi as model organisms , 2012, Virulence.

[372]  S. Lok,et al.  Complete Sequencing of pNDM-HK Encoding NDM-1 Carbapenemase from a Multidrug-Resistant Escherichia coli Strain Isolated in Hong Kong , 2011, PloS one.

[373]  D. Kelly,et al.  Microbiome and immunological interactions. , 2012, Nutrition reviews.

[374]  F. L. Hart,et al.  Eggs and Egg Products , 1971 .

[375]  J. Karns,et al.  Prevalence of Salmonella enterica, Listeria monocytogenes, and Escherichia coli virulence factors in bulk tank milk and in-line filters from U.S. dairies. , 2011, Journal of food protection.

[376]  J. Foster Salmonella acid shock proteins are required for the adaptive acid tolerance response , 1991, Journal of bacteriology.

[377]  Y. M. Kwon,et al.  The effect of long‐term propionate adaptation on the stress resistance of Salmonella Enteritidis , 2010, Journal of applied microbiology.

[378]  Wolin Mj,et al.  Interactions of microbial populations in cellulose fermentation. , 1983 .

[379]  Jacques Ravel,et al.  Comparative Genomics of the IncA/C Multidrug Resistance Plasmid Family , 2009, Journal of bacteriology.

[380]  D. Maskell,et al.  Role in virulence and protective efficacy in pigs of Salmonella enterica serovar Typhimurium secreted components identified by signature-tagged mutagenesis. , 2007, Microbiology.

[381]  M. Kogut,et al.  A comparative study on invasion, survival, modulation of oxidative burst, and nitric oxide responses of macrophages (HD11), and systemic infection in chickens by prevalent poultry Salmonella serovars. , 2012, Foodborne pathogens and disease.

[382]  F. W. Brenner,et al.  Salmonella Nomenclature , 2000, Journal of Clinical Microbiology.

[383]  D. Bell Historical and current molting practices in the U.S. table egg industry. , 2003, Poultry science.

[384]  G. Richarme,et al.  The MglA component of the binding protein-dependent galactose transport system of Salmonella typhimurium is a galactose-stimulated ATPase. , 1993, The Journal of biological chemistry.

[385]  A. Potter,et al.  Protection of epithelial cells from Salmonella enterica serovar Enteritidis invasion by antibodies against the SPI-1 type III secretion system. , 2010, Canadian journal of microbiology.

[386]  M. G. Smith,et al.  Effects of food intake on numbers of salmonellae and Escherichia coli in rumen and faeces of sheep. , 1969, The Journal of applied bacteriology.

[387]  J. Kiss,et al.  Stability, Entrapment and Variant Formation of Salmonella Genomic Island 1 , 2012, PloS one.

[388]  A. Horswill,et al.  Studies of Propionate Toxicity in Salmonella enterica Identify 2-Methylcitrate as a Potent Inhibitor of Cell Growth* , 2001, The Journal of Biological Chemistry.

[389]  T. Cebula,et al.  Multiple Antimicrobial Resistance in Plague: An Emerging Public Health Risk , 2007, PloS one.

[390]  Derrick E. Fouts,et al.  Comparative ICE Genomics: Insights into the Evolution of the SXT/R391 Family of ICEs , 2009, PLoS genetics.

[391]  J. Hughes,et al.  Analysis of Host Cells Associated with the Spv-Mediated Increased Intracellular Growth Rate of Salmonella typhimurium in Mice , 1998, Infection and Immunity.

[392]  R. Edwards,et al.  Chromosomal Rearrangements Formed by rrn Recombination Do Not Improve Replichore Balance in Host-Specific Salmonella enterica Serovars , 2010, PloS one.

[393]  L. Hurst The Ka/Ks ratio: diagnosing the form of sequence evolution. , 2002, Trends in genetics : TIG.