The RNA-binding chaperone Hfq is an important global regulator of gene expression in Pasteurella multocida and plays a crucial role in production of a number of virulence factors including hyaluronic acid capsule

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Abstract

The Gram-negative bacterium Pasteurella multocida is the causative agent of a number of economically important animal diseases, including avian fowl cholera. Numerous P. multocida virulence factors have been identified, including capsule, lipopolysaccharide (LPS) and filamentous hemagglutinin, but little is known about how the expression of these virulence factors is regulated. Hfq is an RNA-binding protein that facilitates riboregulation via interaction with small noncoding RNA molecules (sRNAs) and their mRNA targets. Here, we show that a P. multocida hfq mutant produces significantly less hyaluronic acid capsule during all growth phases and displays reduced in vivo fitness. Transcriptional and proteomic analyses of the hfq mutant during mid-exponential growth revealed altered transcript levels for 128 genes and altered protein levels for 78 proteins. Further proteomic analyses of the hfq mutant during early-exponential growth phase identified 106 proteins that were produced at altered levels. Both the transcript and protein levels for genes/proteins involved in capsule biosynthesis were reduced in the hfq mutant as were the levels of the filamentous hemagglutinin protein PfhB2 and its secretion partner LspB2. In contrast, there was increased expression of three LPS biosynthesis genes, encoding proteins involved in phosphocholine and phosphoethanolamine addition to LPS, suggesting that these genes are negatively regulated by Hfq-dependent mechanisms. Taken together, these data provide the first evidence that Hfq plays a crucial role in regulating the global expression of P. multocida genes, including the regulation of key P. multocida virulence factors, capsule, LPS, and filamentous hemagglutinin.
Original languageEnglish
Pages (from-to)1361 - 1370
Number of pages10
JournalInfection and Immunity
Volume84
Issue number5
DOIs
Publication statusPublished - 2016

Cite this

@article{159ea24ce07147ecac3679d81fc54520,
title = "The RNA-binding chaperone Hfq is an important global regulator of gene expression in Pasteurella multocida and plays a crucial role in production of a number of virulence factors including hyaluronic acid capsule",
abstract = "The Gram-negative bacterium Pasteurella multocida is the causative agent of a number of economically important animal diseases, including avian fowl cholera. Numerous P. multocida virulence factors have been identified, including capsule, lipopolysaccharide (LPS) and filamentous hemagglutinin, but little is known about how the expression of these virulence factors is regulated. Hfq is an RNA-binding protein that facilitates riboregulation via interaction with small noncoding RNA molecules (sRNAs) and their mRNA targets. Here, we show that a P. multocida hfq mutant produces significantly less hyaluronic acid capsule during all growth phases and displays reduced in vivo fitness. Transcriptional and proteomic analyses of the hfq mutant during mid-exponential growth revealed altered transcript levels for 128 genes and altered protein levels for 78 proteins. Further proteomic analyses of the hfq mutant during early-exponential growth phase identified 106 proteins that were produced at altered levels. Both the transcript and protein levels for genes/proteins involved in capsule biosynthesis were reduced in the hfq mutant as were the levels of the filamentous hemagglutinin protein PfhB2 and its secretion partner LspB2. In contrast, there was increased expression of three LPS biosynthesis genes, encoding proteins involved in phosphocholine and phosphoethanolamine addition to LPS, suggesting that these genes are negatively regulated by Hfq-dependent mechanisms. Taken together, these data provide the first evidence that Hfq plays a crucial role in regulating the global expression of P. multocida genes, including the regulation of key P. multocida virulence factors, capsule, LPS, and filamentous hemagglutinin.",
author = "Marianne Megroz and Oded Kleifeld and Wright, {A Amy} and Powell, {David R} and Paul Harrison and Ben Adler and Marina Harper and Boyce, {John D}",
year = "2016",
doi = "10.1128/IAI.00122-16",
language = "English",
volume = "84",
pages = "1361 -- 1370",
journal = "Infection and Immunity",
issn = "0019-9567",
publisher = "American Society for Microbiology",
number = "5",

}

TY - JOUR

T1 - The RNA-binding chaperone Hfq is an important global regulator of gene expression in Pasteurella multocida and plays a crucial role in production of a number of virulence factors including hyaluronic acid capsule

AU - Megroz, Marianne

AU - Kleifeld, Oded

AU - Wright, A Amy

AU - Powell, David R

AU - Harrison, Paul

AU - Adler, Ben

AU - Harper, Marina

AU - Boyce, John D

PY - 2016

Y1 - 2016

N2 - The Gram-negative bacterium Pasteurella multocida is the causative agent of a number of economically important animal diseases, including avian fowl cholera. Numerous P. multocida virulence factors have been identified, including capsule, lipopolysaccharide (LPS) and filamentous hemagglutinin, but little is known about how the expression of these virulence factors is regulated. Hfq is an RNA-binding protein that facilitates riboregulation via interaction with small noncoding RNA molecules (sRNAs) and their mRNA targets. Here, we show that a P. multocida hfq mutant produces significantly less hyaluronic acid capsule during all growth phases and displays reduced in vivo fitness. Transcriptional and proteomic analyses of the hfq mutant during mid-exponential growth revealed altered transcript levels for 128 genes and altered protein levels for 78 proteins. Further proteomic analyses of the hfq mutant during early-exponential growth phase identified 106 proteins that were produced at altered levels. Both the transcript and protein levels for genes/proteins involved in capsule biosynthesis were reduced in the hfq mutant as were the levels of the filamentous hemagglutinin protein PfhB2 and its secretion partner LspB2. In contrast, there was increased expression of three LPS biosynthesis genes, encoding proteins involved in phosphocholine and phosphoethanolamine addition to LPS, suggesting that these genes are negatively regulated by Hfq-dependent mechanisms. Taken together, these data provide the first evidence that Hfq plays a crucial role in regulating the global expression of P. multocida genes, including the regulation of key P. multocida virulence factors, capsule, LPS, and filamentous hemagglutinin.

AB - The Gram-negative bacterium Pasteurella multocida is the causative agent of a number of economically important animal diseases, including avian fowl cholera. Numerous P. multocida virulence factors have been identified, including capsule, lipopolysaccharide (LPS) and filamentous hemagglutinin, but little is known about how the expression of these virulence factors is regulated. Hfq is an RNA-binding protein that facilitates riboregulation via interaction with small noncoding RNA molecules (sRNAs) and their mRNA targets. Here, we show that a P. multocida hfq mutant produces significantly less hyaluronic acid capsule during all growth phases and displays reduced in vivo fitness. Transcriptional and proteomic analyses of the hfq mutant during mid-exponential growth revealed altered transcript levels for 128 genes and altered protein levels for 78 proteins. Further proteomic analyses of the hfq mutant during early-exponential growth phase identified 106 proteins that were produced at altered levels. Both the transcript and protein levels for genes/proteins involved in capsule biosynthesis were reduced in the hfq mutant as were the levels of the filamentous hemagglutinin protein PfhB2 and its secretion partner LspB2. In contrast, there was increased expression of three LPS biosynthesis genes, encoding proteins involved in phosphocholine and phosphoethanolamine addition to LPS, suggesting that these genes are negatively regulated by Hfq-dependent mechanisms. Taken together, these data provide the first evidence that Hfq plays a crucial role in regulating the global expression of P. multocida genes, including the regulation of key P. multocida virulence factors, capsule, LPS, and filamentous hemagglutinin.

UR - http://www.ncbi.nlm.nih.gov/pubmed/26883595

U2 - 10.1128/IAI.00122-16

DO - 10.1128/IAI.00122-16

M3 - Article

VL - 84

SP - 1361

EP - 1370

JO - Infection and Immunity

JF - Infection and Immunity

SN - 0019-9567

IS - 5

ER -