Genomic Epidemiology of Salmonella enterica Serotype Enteritidis based on Population Structure of Prevalent Lineages

Xiangyu Deng; Prerak T. Desai; Henk C. den Bakker; Matthew Mikoleit; Beth Tolar; Eija Trees; Rene S. Hendriksen; Jonathan G. Frye; Steffen Porwollik; Bart C. Weimer; Martin Wiedmann; George M. Weinstock; Patricia I. Fields; Michael McClelland

doi:10.3201/eid2009.131095

Genomic Epidemiology of Salmonella enterica Serotype Enteritidis based on Population Structure of Prevalent Lineages

Xiangyu Deng
, Prerak T. Desai
, Henk C. den Bakker
, Matthew Mikoleit
, Beth Tolar
, Eija Trees
, Rene S. Hendriksen
, Jonathan G. Frye
, Steffen Porwollik
, Bart C. Weimer
, Martin Wiedmann
, George M. Weinstock
, Patricia I. Fields
, Michael McClelland

National Food Institute

University of Georgia
University of California at Irvine
Cornell University
Centers for Disease Control and Prevention
United States Department of Agriculture
University of California at Davis
Washington University School of Medicine

Research output: Contribution to journal › Journal article › Research › peer-review

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Abstract

Salmonella enterica serotype Enteritidis is one of the most commonly reported causes of human salmonellosis. Its low genetic diversity, measured by fingerprinting methods, has made subtyping a challenge. We used whole-genome sequencing to characterize 125 S. enterica Enteritidis and 3 S. enterica serotype Nitra strains. Single-nucleotide polymorphisms were filtered to identify 4,887 reliable loci that distinguished all isolates from each other. Our whole-genome single-nucleotide polymorphism typing approach was robust for S. enterica Enteritidis subtyping with combined data for different strains from 2 different sequencing platforms. Five major genetic lineages were recognized, which revealed possible patterns of geographic and epidemiologic distribution. Analyses on the population dynamics and evolutionary history estimated that major lineages emerged during the 17th-18th centuries and diversified during the 1920s and 1950s.

Original language	English
Journal	Emerging Infectious Diseases
Volume	20
Issue number	9
Pages (from-to)	1481-1489
Number of pages	9
ISSN	1080-6040
DOIs	https://doi.org/10.3201/eid2009.131095
Publication status	Published - 2014

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Keywords

genetic diversity
salmonellosis bacterial disease pathology, epidemiology
Facultatively Anaerobic Gram-Negative Rods Eubacteria Bacteria Microorganisms (Bacteria, Eubacteria, Microorganisms) - Enterobacteriaceae [06702] Salmonella enterica species pathogen serotype Enteritidis, strain-Nitra
Primates Mammalia Vertebrata Chordata Animalia (Animals, Chordates, Humans, Mammals, Primates, Vertebrates) - Hominidae [86215] human common host
03508, Genetics - Human
03509, Genetics - Population genetics
12502, Pathology - General
31000, Physiology and biochemistry of bacteria
36002, Medical and clinical microbiology - Bacteriology
37052, Public health: epidemiology - Communicable diseases
37056, Public health: epidemiology - Miscellaneous
Medical Sciences
Population Studies
fingerprinting analysis laboratory techniques, genetic techniques
sequencing laboratory techniques, genetic techniques
single-nucleotide polymorphism typing laboratory techniques, genetic techniques
Epidemiology
Human Medicine
Infection
Population Genetics
IMMUNOLOGY
INFECTIOUS
TANDEM REPEAT ANALYSIS
UNITED-STATES
EVOLUTIONARY
RECOMBINATION
PHYLOGENETICS
TRANSMISSION
PATHOGENS
OUTBREAKS
SELECTION
ORIGINS
FOOD SAFETY
GENETICS
GENOMICS
GENOTYPE
POLYMORPHISM
SALMONELLA
SALMONELLA ENTERITIDIS
Hygiene and toxicology
Microbiological aspects

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10.3201/eid2009.131095

13 1095Final published version, 629 KB

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Deng, X., Desai, P. T., den Bakker, H. C., Mikoleit, M., Tolar, B., Trees, E., Hendriksen, R. S., Frye, J. G., Porwollik, S., Weimer, B. C., Wiedmann, M., Weinstock, G. M., Fields, P. I., & McClelland, M. (2014). Genomic Epidemiology of Salmonella enterica Serotype Enteritidis based on Population Structure of Prevalent Lineages. Emerging Infectious Diseases, 20(9), 1481-1489. https://doi.org/10.3201/eid2009.131095

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title = "Genomic Epidemiology of Salmonella enterica Serotype Enteritidis based on Population Structure of Prevalent Lineages",

abstract = "Salmonella enterica serotype Enteritidis is one of the most commonly reported causes of human salmonellosis. Its low genetic diversity, measured by fingerprinting methods, has made subtyping a challenge. We used whole-genome sequencing to characterize 125 S. enterica Enteritidis and 3 S. enterica serotype Nitra strains. Single-nucleotide polymorphisms were filtered to identify 4,887 reliable loci that distinguished all isolates from each other. Our whole-genome single-nucleotide polymorphism typing approach was robust for S. enterica Enteritidis subtyping with combined data for different strains from 2 different sequencing platforms. Five major genetic lineages were recognized, which revealed possible patterns of geographic and epidemiologic distribution. Analyses on the population dynamics and evolutionary history estimated that major lineages emerged during the 17th-18th centuries and diversified during the 1920s and 1950s.",

keywords = "genetic diversity, salmonellosis bacterial disease pathology, epidemiology, Facultatively Anaerobic Gram-Negative Rods Eubacteria Bacteria Microorganisms (Bacteria, Eubacteria, Microorganisms) - Enterobacteriaceae [06702] Salmonella enterica species pathogen serotype Enteritidis, strain-Nitra, Primates Mammalia Vertebrata Chordata Animalia (Animals, Chordates, Humans, Mammals, Primates, Vertebrates) - Hominidae [86215] human common host, 03508, Genetics - Human, 03509, Genetics - Population genetics, 12502, Pathology - General, 31000, Physiology and biochemistry of bacteria, 36002, Medical and clinical microbiology - Bacteriology, 37052, Public health: epidemiology - Communicable diseases, 37056, Public health: epidemiology - Miscellaneous, Medical Sciences, Population Studies, fingerprinting analysis laboratory techniques, genetic techniques, sequencing laboratory techniques, genetic techniques, single-nucleotide polymorphism typing laboratory techniques, genetic techniques, Epidemiology, Human Medicine, Infection, Population Genetics, IMMUNOLOGY, INFECTIOUS, TANDEM REPEAT ANALYSIS, UNITED-STATES, EVOLUTIONARY, RECOMBINATION, PHYLOGENETICS, TRANSMISSION, PATHOGENS, OUTBREAKS, SELECTION, ORIGINS, FOOD SAFETY, GENETICS, GENOMICS, GENOTYPE, POLYMORPHISM, SALMONELLA, SALMONELLA ENTERITIDIS, Hygiene and toxicology, Microbiological aspects",

author = "Xiangyu Deng and Desai, \{Prerak T.\} and \{den Bakker\}, \{Henk C.\} and Matthew Mikoleit and Beth Tolar and Eija Trees and Hendriksen, \{Rene S.\} and Frye, \{Jonathan G.\} and Steffen Porwollik and Weimer, \{Bart C.\} and Martin Wiedmann and Weinstock, \{George M.\} and Fields, \{Patricia I.\} and Michael McClelland",

year = "2014",

doi = "10.3201/eid2009.131095",

language = "English",

volume = "20",

pages = "1481--1489",

journal = "Emerging Infectious Diseases",

issn = "1080-6040",

publisher = "Centers for Disease Control and Prevention (CDC)",

number = "9",

}

Deng, X, Desai, PT, den Bakker, HC, Mikoleit, M, Tolar, B, Trees, E, Hendriksen, RS, Frye, JG, Porwollik, S, Weimer, BC, Wiedmann, M, Weinstock, GM, Fields, PI & McClelland, M 2014, 'Genomic Epidemiology of Salmonella enterica Serotype Enteritidis based on Population Structure of Prevalent Lineages', Emerging Infectious Diseases, vol. 20, no. 9, pp. 1481-1489. https://doi.org/10.3201/eid2009.131095

TY - JOUR

T1 - Genomic Epidemiology of Salmonella enterica Serotype Enteritidis based on Population Structure of Prevalent Lineages

AU - Deng, Xiangyu

AU - Desai, Prerak T.

AU - den Bakker, Henk C.

AU - Mikoleit, Matthew

AU - Tolar, Beth

AU - Trees, Eija

AU - Hendriksen, Rene S.

AU - Frye, Jonathan G.

AU - Porwollik, Steffen

AU - Weimer, Bart C.

AU - Wiedmann, Martin

AU - Weinstock, George M.

AU - Fields, Patricia I.

AU - McClelland, Michael

PY - 2014

Y1 - 2014

N2 - Salmonella enterica serotype Enteritidis is one of the most commonly reported causes of human salmonellosis. Its low genetic diversity, measured by fingerprinting methods, has made subtyping a challenge. We used whole-genome sequencing to characterize 125 S. enterica Enteritidis and 3 S. enterica serotype Nitra strains. Single-nucleotide polymorphisms were filtered to identify 4,887 reliable loci that distinguished all isolates from each other. Our whole-genome single-nucleotide polymorphism typing approach was robust for S. enterica Enteritidis subtyping with combined data for different strains from 2 different sequencing platforms. Five major genetic lineages were recognized, which revealed possible patterns of geographic and epidemiologic distribution. Analyses on the population dynamics and evolutionary history estimated that major lineages emerged during the 17th-18th centuries and diversified during the 1920s and 1950s.

AB - Salmonella enterica serotype Enteritidis is one of the most commonly reported causes of human salmonellosis. Its low genetic diversity, measured by fingerprinting methods, has made subtyping a challenge. We used whole-genome sequencing to characterize 125 S. enterica Enteritidis and 3 S. enterica serotype Nitra strains. Single-nucleotide polymorphisms were filtered to identify 4,887 reliable loci that distinguished all isolates from each other. Our whole-genome single-nucleotide polymorphism typing approach was robust for S. enterica Enteritidis subtyping with combined data for different strains from 2 different sequencing platforms. Five major genetic lineages were recognized, which revealed possible patterns of geographic and epidemiologic distribution. Analyses on the population dynamics and evolutionary history estimated that major lineages emerged during the 17th-18th centuries and diversified during the 1920s and 1950s.

KW - genetic diversity

KW - salmonellosis bacterial disease pathology, epidemiology

KW - Facultatively Anaerobic Gram-Negative Rods Eubacteria Bacteria Microorganisms (Bacteria, Eubacteria, Microorganisms) - Enterobacteriaceae [06702] Salmonella enterica species pathogen serotype Enteritidis, strain-Nitra

KW - Primates Mammalia Vertebrata Chordata Animalia (Animals, Chordates, Humans, Mammals, Primates, Vertebrates) - Hominidae [86215] human common host

KW - 03508, Genetics - Human

KW - 03509, Genetics - Population genetics

KW - 12502, Pathology - General

KW - 31000, Physiology and biochemistry of bacteria

KW - 36002, Medical and clinical microbiology - Bacteriology

KW - 37052, Public health: epidemiology - Communicable diseases

KW - 37056, Public health: epidemiology - Miscellaneous

KW - Medical Sciences

KW - Population Studies

KW - fingerprinting analysis laboratory techniques, genetic techniques

KW - sequencing laboratory techniques, genetic techniques

KW - single-nucleotide polymorphism typing laboratory techniques, genetic techniques

KW - Epidemiology

KW - Human Medicine

KW - Infection

KW - Population Genetics

KW - IMMUNOLOGY

KW - INFECTIOUS

KW - TANDEM REPEAT ANALYSIS

KW - UNITED-STATES

KW - EVOLUTIONARY

KW - RECOMBINATION

KW - PHYLOGENETICS

KW - TRANSMISSION

KW - PATHOGENS

KW - OUTBREAKS

KW - SELECTION

KW - ORIGINS

KW - FOOD SAFETY

KW - GENETICS

KW - GENOMICS

KW - GENOTYPE

KW - POLYMORPHISM

KW - SALMONELLA

KW - SALMONELLA ENTERITIDIS

KW - Hygiene and toxicology

KW - Microbiological aspects

U2 - 10.3201/eid2009.131095

DO - 10.3201/eid2009.131095

M3 - Journal article

C2 - 25147968

SN - 1080-6040

VL - 20

SP - 1481

EP - 1489

JO - Emerging Infectious Diseases

JF - Emerging Infectious Diseases

IS - 9

ER -

Genomic Epidemiology of Salmonella enterica Serotype Enteritidis based on Population Structure of Prevalent Lineages

Abstract

UN SDGs

Keywords

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