The Role of the Salmonella spvB IncF Plasmid and Its Resident Entry Exclusion Gene traS on Plasmid Exclusion

Salmonella enterica cause significant illnesses worldwide. There has been a marked increase in resistance to fluoroquinolones and β-lactams/cephalosporins, antibiotics commonly used to treat salmonellosis. However, S. enterica serovars vary in their resistance to these and other antibiotics. The sys...

Full description

Bibliographic Details
Main Authors: Mopelola Oluwadare, Margie D. Lee, Christopher J. Grim, Erin K. Lipp, Ying Cheng, John J. Maurer
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2020.00949/full
id doaj-551f11c4b55b46a98a3a684dd598d805
record_format Article
spelling doaj-551f11c4b55b46a98a3a684dd598d8052020-11-25T03:12:31ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-05-011110.3389/fmicb.2020.00949538647The Role of the Salmonella spvB IncF Plasmid and Its Resident Entry Exclusion Gene traS on Plasmid ExclusionMopelola Oluwadare0Margie D. Lee1Margie D. Lee2Christopher J. Grim3Erin K. Lipp4Ying Cheng5John J. Maurer6John J. Maurer7Department of Population Health, University of Georgia, Athens, GA, United StatesDepartment of Population Health, University of Georgia, Athens, GA, United StatesDepartment of Biomedical Sciences and Pathobiology, Virginia Polytechnic Institute and State University, Blacksburg, VA, United StatesCenter for Food Safety and Applied Nutrition, U.S. Food and Drug Administration, Laurel, MD, United StatesDepartment of Environmental Health Science, University of Georgia, Athens, GA, United StatesDepartment of Population Health, University of Georgia, Athens, GA, United StatesDepartment of Population Health, University of Georgia, Athens, GA, United StatesDepartment of Animal and Poultry Sciences, Virginia Polytechnic Institute and State University, Blacksburg, VA, United StatesSalmonella enterica cause significant illnesses worldwide. There has been a marked increase in resistance to fluoroquinolones and β-lactams/cephalosporins, antibiotics commonly used to treat salmonellosis. However, S. enterica serovars vary in their resistance to these and other antibiotics. The systemic virulence of some Salmonella serovars is due to a low copy number, IncF plasmid (65–100 kb) that contains the ADP-ribosylating toxin, SpvB. This virulence plasmid is present in only nine Salmonella serovars. It is possible that the spvB-virulence plasmid excludes other plasmids and may explain why antibiotic resistance is slow to develop in certain Salmonella serovars such as S. Enteritidis. The distribution of plasmid entry exclusion genes traS/traT and traY/excA are variable in Salmonella IncF and IncI plasmids, respectively and may account for differences in emergent antimicrobial resistance for some Salmonella serovars. The goal of this study is to determine the contribution of the Salmonella spvB-virulence plasmid in F-plasmid exclusion. From conjugation experiments, S. Typhimurium exhibited lower conjugation frequency with incFI and incFII plasmids when the spvB-virulence plasmid is present. Furthermore, introduction of cloned incFI traS into a “plasmidless” S. Typhimurium LT2 strain and Escherichia coli DH5α excluded incFI plasmid. However, deletion of the virulence plasmid traS did not affect plasmid exclusion significantly compared to a spvB control deletion. In addition, differences in F plasmid conjugation in natural Salmonella isolates did not correlate with IncF or SpvB-virulence plasmid genotype. There appear to be other plasmid or chromosomal genes at play in plasmid exclusion that may be responsible for the slow development of antibiotic resistance in certain serovars.https://www.frontiersin.org/article/10.3389/fmicb.2020.00949/fullSalmonellavirulence plasmidantibiotic resistanceentry exclusionconjugation
collection DOAJ
language English
format Article
sources DOAJ
author Mopelola Oluwadare
Margie D. Lee
Margie D. Lee
Christopher J. Grim
Erin K. Lipp
Ying Cheng
John J. Maurer
John J. Maurer
spellingShingle Mopelola Oluwadare
Margie D. Lee
Margie D. Lee
Christopher J. Grim
Erin K. Lipp
Ying Cheng
John J. Maurer
John J. Maurer
The Role of the Salmonella spvB IncF Plasmid and Its Resident Entry Exclusion Gene traS on Plasmid Exclusion
Frontiers in Microbiology
Salmonella
virulence plasmid
antibiotic resistance
entry exclusion
conjugation
author_facet Mopelola Oluwadare
Margie D. Lee
Margie D. Lee
Christopher J. Grim
Erin K. Lipp
Ying Cheng
John J. Maurer
John J. Maurer
author_sort Mopelola Oluwadare
title The Role of the Salmonella spvB IncF Plasmid and Its Resident Entry Exclusion Gene traS on Plasmid Exclusion
title_short The Role of the Salmonella spvB IncF Plasmid and Its Resident Entry Exclusion Gene traS on Plasmid Exclusion
title_full The Role of the Salmonella spvB IncF Plasmid and Its Resident Entry Exclusion Gene traS on Plasmid Exclusion
title_fullStr The Role of the Salmonella spvB IncF Plasmid and Its Resident Entry Exclusion Gene traS on Plasmid Exclusion
title_full_unstemmed The Role of the Salmonella spvB IncF Plasmid and Its Resident Entry Exclusion Gene traS on Plasmid Exclusion
title_sort role of the salmonella spvb incf plasmid and its resident entry exclusion gene tras on plasmid exclusion
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2020-05-01
description Salmonella enterica cause significant illnesses worldwide. There has been a marked increase in resistance to fluoroquinolones and β-lactams/cephalosporins, antibiotics commonly used to treat salmonellosis. However, S. enterica serovars vary in their resistance to these and other antibiotics. The systemic virulence of some Salmonella serovars is due to a low copy number, IncF plasmid (65–100 kb) that contains the ADP-ribosylating toxin, SpvB. This virulence plasmid is present in only nine Salmonella serovars. It is possible that the spvB-virulence plasmid excludes other plasmids and may explain why antibiotic resistance is slow to develop in certain Salmonella serovars such as S. Enteritidis. The distribution of plasmid entry exclusion genes traS/traT and traY/excA are variable in Salmonella IncF and IncI plasmids, respectively and may account for differences in emergent antimicrobial resistance for some Salmonella serovars. The goal of this study is to determine the contribution of the Salmonella spvB-virulence plasmid in F-plasmid exclusion. From conjugation experiments, S. Typhimurium exhibited lower conjugation frequency with incFI and incFII plasmids when the spvB-virulence plasmid is present. Furthermore, introduction of cloned incFI traS into a “plasmidless” S. Typhimurium LT2 strain and Escherichia coli DH5α excluded incFI plasmid. However, deletion of the virulence plasmid traS did not affect plasmid exclusion significantly compared to a spvB control deletion. In addition, differences in F plasmid conjugation in natural Salmonella isolates did not correlate with IncF or SpvB-virulence plasmid genotype. There appear to be other plasmid or chromosomal genes at play in plasmid exclusion that may be responsible for the slow development of antibiotic resistance in certain serovars.
topic Salmonella
virulence plasmid
antibiotic resistance
entry exclusion
conjugation
url https://www.frontiersin.org/article/10.3389/fmicb.2020.00949/full
work_keys_str_mv AT mopelolaoluwadare theroleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT margiedlee theroleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT margiedlee theroleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT christopherjgrim theroleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT erinklipp theroleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT yingcheng theroleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT johnjmaurer theroleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT johnjmaurer theroleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT mopelolaoluwadare roleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT margiedlee roleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT margiedlee roleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT christopherjgrim roleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT erinklipp roleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT yingcheng roleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT johnjmaurer roleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
AT johnjmaurer roleofthesalmonellaspvbincfplasmidanditsresidententryexclusiongenetrasonplasmidexclusion
_version_ 1724650002772393984