CmeR functions as a pleiotropic regulator and is required for optimal colonization of Campylobacter jejuni in vivo

Baoqing Guo, Ying Wang, Feng Shi, Yi Wen Barton, Paul Plummer, Donald Reynolds, Dan Nettleton, Tara Grinnage-Pulley, Jun Lin, Qijing Zhang

Research output: Contribution to journalArticle

51 Citations (Scopus)

Abstract

CmeR functions as a transcriptional repressor modulating the expression of the multidrug efflux pump CmeABC in Campylobacter jejuni. To determine if CmeR also regulates other genes in C. jejuni, we compared the transcriptome of the cmeR mutant with that of the wild-type strain using a DNA microarray. This comparison identified 28 genes that showed a ≥2-fold change in expression in the cmeR mutant. Independent real-time quantitative reverse transcription-PCR experiments confirmed 27 of the 28 differentially expressed genes. The CmeR-regulated genes encode membrane transporters, proteins involved in C 4 -dicarboxylate transport and utilization, enzymes for biosynthesis of capsular polysaccharide, and hypothetical proteins with unknown functions. Among the genes whose expression was upregulated in the cmeR mutant, Cj0561c (encoding a putative periplasmic protein) showed the greatest increase in expression. Subsequent experiments demonstrated that this gene is strongly repressed by CmeR. The presence of the known CmeR-binding site, an inverted repeat of TGTAAT, in the promoter region of Cj0561c suggests that CmeR directly inhibits the transcription of Cj0561c. Similar to expression of cmeABC, transcription of Cj0561c is strongly induced by bile compounds, which are normally present in the intestinal tracts of animals. Inactivation of Cj0561c did not affect the susceptibility of C. jejuni to antimicrobial compounds in vitro but reduced the fitness of C. jejuni in chickens. Loss-of-function mutation of cmeR severely reduced the ability of C. jejuni to colonize chickens. Together, these findings indicate that CmeR governs the expression of multiple genes with diverse functions and is required for Campylobacter adaptation in the chicken host.

Original languageEnglish (US)
Pages (from-to)1879-1890
Number of pages12
JournalJournal of bacteriology
Volume190
Issue number6
DOIs
StatePublished - Mar 1 2008

Fingerprint

Campylobacter jejuni
Chickens
Genes
Periplasmic Proteins
Gene Expression
Campylobacter
Membrane Transport Proteins
Oligonucleotide Array Sequence Analysis
Transcriptome
Genetic Promoter Regions
Bile
Reverse Transcription
Polysaccharides
Membrane Proteins
Binding Sites
Polymerase Chain Reaction
Mutation
Enzymes
Proteins

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

Cite this

CmeR functions as a pleiotropic regulator and is required for optimal colonization of Campylobacter jejuni in vivo. / Guo, Baoqing; Wang, Ying; Shi, Feng; Barton, Yi Wen; Plummer, Paul; Reynolds, Donald; Nettleton, Dan; Grinnage-Pulley, Tara; Lin, Jun; Zhang, Qijing.

In: Journal of bacteriology, Vol. 190, No. 6, 01.03.2008, p. 1879-1890.

Research output: Contribution to journalArticle

Guo, B, Wang, Y, Shi, F, Barton, YW, Plummer, P, Reynolds, D, Nettleton, D, Grinnage-Pulley, T, Lin, J & Zhang, Q 2008, 'CmeR functions as a pleiotropic regulator and is required for optimal colonization of Campylobacter jejuni in vivo', Journal of bacteriology, vol. 190, no. 6, pp. 1879-1890. https://doi.org/10.1128/JB.01796-07
Guo, Baoqing ; Wang, Ying ; Shi, Feng ; Barton, Yi Wen ; Plummer, Paul ; Reynolds, Donald ; Nettleton, Dan ; Grinnage-Pulley, Tara ; Lin, Jun ; Zhang, Qijing. / CmeR functions as a pleiotropic regulator and is required for optimal colonization of Campylobacter jejuni in vivo. In: Journal of bacteriology. 2008 ; Vol. 190, No. 6. pp. 1879-1890.
@article{24f3e860eb34488f971b1c4454d49df5,
title = "CmeR functions as a pleiotropic regulator and is required for optimal colonization of Campylobacter jejuni in vivo",
abstract = "CmeR functions as a transcriptional repressor modulating the expression of the multidrug efflux pump CmeABC in Campylobacter jejuni. To determine if CmeR also regulates other genes in C. jejuni, we compared the transcriptome of the cmeR mutant with that of the wild-type strain using a DNA microarray. This comparison identified 28 genes that showed a ≥2-fold change in expression in the cmeR mutant. Independent real-time quantitative reverse transcription-PCR experiments confirmed 27 of the 28 differentially expressed genes. The CmeR-regulated genes encode membrane transporters, proteins involved in C 4 -dicarboxylate transport and utilization, enzymes for biosynthesis of capsular polysaccharide, and hypothetical proteins with unknown functions. Among the genes whose expression was upregulated in the cmeR mutant, Cj0561c (encoding a putative periplasmic protein) showed the greatest increase in expression. Subsequent experiments demonstrated that this gene is strongly repressed by CmeR. The presence of the known CmeR-binding site, an inverted repeat of TGTAAT, in the promoter region of Cj0561c suggests that CmeR directly inhibits the transcription of Cj0561c. Similar to expression of cmeABC, transcription of Cj0561c is strongly induced by bile compounds, which are normally present in the intestinal tracts of animals. Inactivation of Cj0561c did not affect the susceptibility of C. jejuni to antimicrobial compounds in vitro but reduced the fitness of C. jejuni in chickens. Loss-of-function mutation of cmeR severely reduced the ability of C. jejuni to colonize chickens. Together, these findings indicate that CmeR governs the expression of multiple genes with diverse functions and is required for Campylobacter adaptation in the chicken host.",
author = "Baoqing Guo and Ying Wang and Feng Shi and Barton, {Yi Wen} and Paul Plummer and Donald Reynolds and Dan Nettleton and Tara Grinnage-Pulley and Jun Lin and Qijing Zhang",
year = "2008",
month = "3",
day = "1",
doi = "10.1128/JB.01796-07",
language = "English (US)",
volume = "190",
pages = "1879--1890",
journal = "Journal of Bacteriology",
issn = "0021-9193",
publisher = "American Society for Microbiology",
number = "6",

}

TY - JOUR

T1 - CmeR functions as a pleiotropic regulator and is required for optimal colonization of Campylobacter jejuni in vivo

AU - Guo, Baoqing

AU - Wang, Ying

AU - Shi, Feng

AU - Barton, Yi Wen

AU - Plummer, Paul

AU - Reynolds, Donald

AU - Nettleton, Dan

AU - Grinnage-Pulley, Tara

AU - Lin, Jun

AU - Zhang, Qijing

PY - 2008/3/1

Y1 - 2008/3/1

N2 - CmeR functions as a transcriptional repressor modulating the expression of the multidrug efflux pump CmeABC in Campylobacter jejuni. To determine if CmeR also regulates other genes in C. jejuni, we compared the transcriptome of the cmeR mutant with that of the wild-type strain using a DNA microarray. This comparison identified 28 genes that showed a ≥2-fold change in expression in the cmeR mutant. Independent real-time quantitative reverse transcription-PCR experiments confirmed 27 of the 28 differentially expressed genes. The CmeR-regulated genes encode membrane transporters, proteins involved in C 4 -dicarboxylate transport and utilization, enzymes for biosynthesis of capsular polysaccharide, and hypothetical proteins with unknown functions. Among the genes whose expression was upregulated in the cmeR mutant, Cj0561c (encoding a putative periplasmic protein) showed the greatest increase in expression. Subsequent experiments demonstrated that this gene is strongly repressed by CmeR. The presence of the known CmeR-binding site, an inverted repeat of TGTAAT, in the promoter region of Cj0561c suggests that CmeR directly inhibits the transcription of Cj0561c. Similar to expression of cmeABC, transcription of Cj0561c is strongly induced by bile compounds, which are normally present in the intestinal tracts of animals. Inactivation of Cj0561c did not affect the susceptibility of C. jejuni to antimicrobial compounds in vitro but reduced the fitness of C. jejuni in chickens. Loss-of-function mutation of cmeR severely reduced the ability of C. jejuni to colonize chickens. Together, these findings indicate that CmeR governs the expression of multiple genes with diverse functions and is required for Campylobacter adaptation in the chicken host.

AB - CmeR functions as a transcriptional repressor modulating the expression of the multidrug efflux pump CmeABC in Campylobacter jejuni. To determine if CmeR also regulates other genes in C. jejuni, we compared the transcriptome of the cmeR mutant with that of the wild-type strain using a DNA microarray. This comparison identified 28 genes that showed a ≥2-fold change in expression in the cmeR mutant. Independent real-time quantitative reverse transcription-PCR experiments confirmed 27 of the 28 differentially expressed genes. The CmeR-regulated genes encode membrane transporters, proteins involved in C 4 -dicarboxylate transport and utilization, enzymes for biosynthesis of capsular polysaccharide, and hypothetical proteins with unknown functions. Among the genes whose expression was upregulated in the cmeR mutant, Cj0561c (encoding a putative periplasmic protein) showed the greatest increase in expression. Subsequent experiments demonstrated that this gene is strongly repressed by CmeR. The presence of the known CmeR-binding site, an inverted repeat of TGTAAT, in the promoter region of Cj0561c suggests that CmeR directly inhibits the transcription of Cj0561c. Similar to expression of cmeABC, transcription of Cj0561c is strongly induced by bile compounds, which are normally present in the intestinal tracts of animals. Inactivation of Cj0561c did not affect the susceptibility of C. jejuni to antimicrobial compounds in vitro but reduced the fitness of C. jejuni in chickens. Loss-of-function mutation of cmeR severely reduced the ability of C. jejuni to colonize chickens. Together, these findings indicate that CmeR governs the expression of multiple genes with diverse functions and is required for Campylobacter adaptation in the chicken host.

UR - http://www.scopus.com/inward/record.url?scp=40449083654&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=40449083654&partnerID=8YFLogxK

U2 - 10.1128/JB.01796-07

DO - 10.1128/JB.01796-07

M3 - Article

VL - 190

SP - 1879

EP - 1890

JO - Journal of Bacteriology

JF - Journal of Bacteriology

SN - 0021-9193

IS - 6

ER -