Comparative Genomic Analysis and Characterization of Two Salmonella enterica Serovar Enteritidis Isolates From Poultry With Notably Different Survival Abilities in Egg Whites

Salmonellaenterica serovar Enteritidis (Salmonella Enteritidis) is a globally important foodborne pathogen, and the contaminated chicken eggs are the major source of salmonellosis in humans. Salmonella Enteritidis strains are differentially susceptible to the hostile environment of egg whites. Strai...

Full description

Bibliographic Details
Main Authors: Yanyan Wang, Ben Jia, Xuebin Xu, Lida Zhang, Chaochun Wei, Hongyu Ou, Yan Cui, Chunlei Shi, Xianming Shi
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-09-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2018.02111/full
id doaj-d820a4678eba40eeabc453fcf7098c1a
record_format Article
spelling doaj-d820a4678eba40eeabc453fcf7098c1a2020-11-24T21:06:08ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-09-01910.3389/fmicb.2018.02111387012Comparative Genomic Analysis and Characterization of Two Salmonella enterica Serovar Enteritidis Isolates From Poultry With Notably Different Survival Abilities in Egg WhitesYanyan Wang0Ben Jia1Xuebin Xu2Lida Zhang3Chaochun Wei4Hongyu Ou5Yan Cui6Chunlei Shi7Xianming Shi8MOST-USDA Joint Research Center for Food Safety, School of Agriculture and Biology and State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai, ChinaSchool of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaDepartment of Microbiology, Shanghai Center for Disease Control and Prevention, Shanghai, ChinaMOST-USDA Joint Research Center for Food Safety, School of Agriculture and Biology and State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai, ChinaSchool of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaSchool of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, ChinaMOST-USDA Joint Research Center for Food Safety, School of Agriculture and Biology and State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai, ChinaMOST-USDA Joint Research Center for Food Safety, School of Agriculture and Biology and State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai, ChinaMOST-USDA Joint Research Center for Food Safety, School of Agriculture and Biology and State Key Laboratory of Microbial Metabolism, Shanghai Jiao Tong University, Shanghai, ChinaSalmonellaenterica serovar Enteritidis (Salmonella Enteritidis) is a globally important foodborne pathogen, and the contaminated chicken eggs are the major source of salmonellosis in humans. Salmonella Enteritidis strains are differentially susceptible to the hostile environment of egg whites. Strains with superior survival ability in egg whites are more likely to contaminate eggs and consequently infect humans. However, the genetic basis for this phenotype is unclear. We characterized two Salmonella Enteritidis strains isolated from chicken meat that had similar genetic backgrounds but large differences in survival ability in egg whites. Although genome comparisons indicated that the gene content and genomic synteny were highly conserved, variations including six insertions or deletions (INDELs) and 70 single nucleotide polymorphisms (SNPs) were observed between the two genomes. Of these, 38 variations including four INDELs and 34 non-synonymous SNPs (nsSNP) were annotated to result in amino acid substitutions or INDELs in coding proteins. These variations were located in 38 genes involved in lysozyme inhibition, vitamin biosynthesis, cell division and DNA damage response, osmotic and oxidative protection, iron-related functions, cell envelope maintenance, amino acid and carbohydrate metabolism, antimicrobial resistance, and type III secretion system. We carried out allelic replacements for two nsSNPs in bioC (biotin synthesis) and pliC (lysozyme inhibition), and two INDELs in ftsK and yqiJ (DNA damage response) by homologous recombination, and these replacements did not alter the bacterial survival ability in egg whites. However, the bacterial survival ability in egg whites was reduced when deletion mutation of the genes bioC and pliC occurred. This study provides initial correlations between observed genotypes and phenotypes and serves as an important caveat for further functional studies.https://www.frontiersin.org/article/10.3389/fmicb.2018.02111/fullSalmonella Enteritidisegg whitegenome sequencinggenome comparisonsurvival
collection DOAJ
language English
format Article
sources DOAJ
author Yanyan Wang
Ben Jia
Xuebin Xu
Lida Zhang
Chaochun Wei
Hongyu Ou
Yan Cui
Chunlei Shi
Xianming Shi
spellingShingle Yanyan Wang
Ben Jia
Xuebin Xu
Lida Zhang
Chaochun Wei
Hongyu Ou
Yan Cui
Chunlei Shi
Xianming Shi
Comparative Genomic Analysis and Characterization of Two Salmonella enterica Serovar Enteritidis Isolates From Poultry With Notably Different Survival Abilities in Egg Whites
Frontiers in Microbiology
Salmonella Enteritidis
egg white
genome sequencing
genome comparison
survival
author_facet Yanyan Wang
Ben Jia
Xuebin Xu
Lida Zhang
Chaochun Wei
Hongyu Ou
Yan Cui
Chunlei Shi
Xianming Shi
author_sort Yanyan Wang
title Comparative Genomic Analysis and Characterization of Two Salmonella enterica Serovar Enteritidis Isolates From Poultry With Notably Different Survival Abilities in Egg Whites
title_short Comparative Genomic Analysis and Characterization of Two Salmonella enterica Serovar Enteritidis Isolates From Poultry With Notably Different Survival Abilities in Egg Whites
title_full Comparative Genomic Analysis and Characterization of Two Salmonella enterica Serovar Enteritidis Isolates From Poultry With Notably Different Survival Abilities in Egg Whites
title_fullStr Comparative Genomic Analysis and Characterization of Two Salmonella enterica Serovar Enteritidis Isolates From Poultry With Notably Different Survival Abilities in Egg Whites
title_full_unstemmed Comparative Genomic Analysis and Characterization of Two Salmonella enterica Serovar Enteritidis Isolates From Poultry With Notably Different Survival Abilities in Egg Whites
title_sort comparative genomic analysis and characterization of two salmonella enterica serovar enteritidis isolates from poultry with notably different survival abilities in egg whites
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2018-09-01
description Salmonellaenterica serovar Enteritidis (Salmonella Enteritidis) is a globally important foodborne pathogen, and the contaminated chicken eggs are the major source of salmonellosis in humans. Salmonella Enteritidis strains are differentially susceptible to the hostile environment of egg whites. Strains with superior survival ability in egg whites are more likely to contaminate eggs and consequently infect humans. However, the genetic basis for this phenotype is unclear. We characterized two Salmonella Enteritidis strains isolated from chicken meat that had similar genetic backgrounds but large differences in survival ability in egg whites. Although genome comparisons indicated that the gene content and genomic synteny were highly conserved, variations including six insertions or deletions (INDELs) and 70 single nucleotide polymorphisms (SNPs) were observed between the two genomes. Of these, 38 variations including four INDELs and 34 non-synonymous SNPs (nsSNP) were annotated to result in amino acid substitutions or INDELs in coding proteins. These variations were located in 38 genes involved in lysozyme inhibition, vitamin biosynthesis, cell division and DNA damage response, osmotic and oxidative protection, iron-related functions, cell envelope maintenance, amino acid and carbohydrate metabolism, antimicrobial resistance, and type III secretion system. We carried out allelic replacements for two nsSNPs in bioC (biotin synthesis) and pliC (lysozyme inhibition), and two INDELs in ftsK and yqiJ (DNA damage response) by homologous recombination, and these replacements did not alter the bacterial survival ability in egg whites. However, the bacterial survival ability in egg whites was reduced when deletion mutation of the genes bioC and pliC occurred. This study provides initial correlations between observed genotypes and phenotypes and serves as an important caveat for further functional studies.
topic Salmonella Enteritidis
egg white
genome sequencing
genome comparison
survival
url https://www.frontiersin.org/article/10.3389/fmicb.2018.02111/full
work_keys_str_mv AT yanyanwang comparativegenomicanalysisandcharacterizationoftwosalmonellaentericaserovarenteritidisisolatesfrompoultrywithnotablydifferentsurvivalabilitiesineggwhites
AT benjia comparativegenomicanalysisandcharacterizationoftwosalmonellaentericaserovarenteritidisisolatesfrompoultrywithnotablydifferentsurvivalabilitiesineggwhites
AT xuebinxu comparativegenomicanalysisandcharacterizationoftwosalmonellaentericaserovarenteritidisisolatesfrompoultrywithnotablydifferentsurvivalabilitiesineggwhites
AT lidazhang comparativegenomicanalysisandcharacterizationoftwosalmonellaentericaserovarenteritidisisolatesfrompoultrywithnotablydifferentsurvivalabilitiesineggwhites
AT chaochunwei comparativegenomicanalysisandcharacterizationoftwosalmonellaentericaserovarenteritidisisolatesfrompoultrywithnotablydifferentsurvivalabilitiesineggwhites
AT hongyuou comparativegenomicanalysisandcharacterizationoftwosalmonellaentericaserovarenteritidisisolatesfrompoultrywithnotablydifferentsurvivalabilitiesineggwhites
AT yancui comparativegenomicanalysisandcharacterizationoftwosalmonellaentericaserovarenteritidisisolatesfrompoultrywithnotablydifferentsurvivalabilitiesineggwhites
AT chunleishi comparativegenomicanalysisandcharacterizationoftwosalmonellaentericaserovarenteritidisisolatesfrompoultrywithnotablydifferentsurvivalabilitiesineggwhites
AT xianmingshi comparativegenomicanalysisandcharacterizationoftwosalmonellaentericaserovarenteritidisisolatesfrompoultrywithnotablydifferentsurvivalabilitiesineggwhites
_version_ 1716766651553153024