In vivo transcriptomes of Streptococcus suis reveal genes required for niche-specific adaptation and pathogenesis

Jesús Arenas, Ruth Bossers-de Vries, José Harders-Westerveen, Herma Buys, Lisette M.F. Ruuls-van Stalle, Norbert Stockhofe-Zurwieden, Edoardo Zaccaria, Jan Tommassen, Jerry M. Wells, Hilde E. Smith, Astrid de Greeff

Research output: Contribution to journalArticleAcademicpeer-review

2 Citations (Scopus)

Abstract

Streptococcus suis is a Gram-positive bacterium and a zoonotic pathogen residing in the nasopharynx or the gastrointestinal tract of pigs with a potential of causing life-threatening invasive disease. It is endemic in the porcine production industry worldwide, and it is also an emerging human pathogen. After invasion, the pathogen adapts to cause bacteremia and disseminates to different organs including the brain. To gain insights in this process, we infected piglets with a highly virulent strain of S. suis, and bacterial transcriptomes were obtained from blood and different organs (brain, joints, and heart) when animals had severe clinical symptoms of infection. Microarrays were used to determine the genome-wide transcriptional profile at different infection sites and during growth in standard growth medium in vitro. We observed differential expression of around 30% of the Open Reading Frames (ORFs) and infection-site specific patterns of gene expression. Genes with major changes in expression were involved in transcriptional regulation, metabolism, nutrient acquisition, stress defenses, and virulence, amongst others, and results were confirmed for a subset of selected genes using RT-qPCR. Mutants were generated in two selected genes, and the encoded proteins, i.e., NADH oxidase and MetQ, were shown to be important virulence factors in coinfection experiments and in vitro assays. The knowledge derived from this study regarding S. suis gene expression in vivo and identification of virulence factors is important for the development of novel diagnostic and therapeutic strategies to control S. suis disease.

LanguageEnglish
Pages334-351
JournalVirulence
Volume10
Issue number1
DOIs
Publication statusPublished - 7 Apr 2019

Fingerprint

Streptococcus suis
Transcriptome
Virulence Factors
Genes
Swine
Infection
Gene Expression
Nasopharynx
Zoonoses
Brain
Gram-Positive Bacteria
Growth
Bacteremia
Coinfection
Open Reading Frames
Virulence
Gastrointestinal Tract
Industry
Joints
Genome

Keywords

  • infection
  • infectomics
  • pathogenesis
  • transcriptomics
  • zoonotic pathogen

Cite this

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title = "In vivo transcriptomes of Streptococcus suis reveal genes required for niche-specific adaptation and pathogenesis",
abstract = "Streptococcus suis is a Gram-positive bacterium and a zoonotic pathogen residing in the nasopharynx or the gastrointestinal tract of pigs with a potential of causing life-threatening invasive disease. It is endemic in the porcine production industry worldwide, and it is also an emerging human pathogen. After invasion, the pathogen adapts to cause bacteremia and disseminates to different organs including the brain. To gain insights in this process, we infected piglets with a highly virulent strain of S. suis, and bacterial transcriptomes were obtained from blood and different organs (brain, joints, and heart) when animals had severe clinical symptoms of infection. Microarrays were used to determine the genome-wide transcriptional profile at different infection sites and during growth in standard growth medium in vitro. We observed differential expression of around 30{\%} of the Open Reading Frames (ORFs) and infection-site specific patterns of gene expression. Genes with major changes in expression were involved in transcriptional regulation, metabolism, nutrient acquisition, stress defenses, and virulence, amongst others, and results were confirmed for a subset of selected genes using RT-qPCR. Mutants were generated in two selected genes, and the encoded proteins, i.e., NADH oxidase and MetQ, were shown to be important virulence factors in coinfection experiments and in vitro assays. The knowledge derived from this study regarding S. suis gene expression in vivo and identification of virulence factors is important for the development of novel diagnostic and therapeutic strategies to control S. suis disease.",
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author = "Jes{\'u}s Arenas and {Bossers-de Vries}, Ruth and Jos{\'e} Harders-Westerveen and Herma Buys and {Ruuls-van Stalle}, {Lisette M.F.} and Norbert Stockhofe-Zurwieden and Edoardo Zaccaria and Jan Tommassen and Wells, {Jerry M.} and Smith, {Hilde E.} and {de Greeff}, Astrid",
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In vivo transcriptomes of Streptococcus suis reveal genes required for niche-specific adaptation and pathogenesis. / Arenas, Jesús; Bossers-de Vries, Ruth; Harders-Westerveen, José; Buys, Herma; Ruuls-van Stalle, Lisette M.F.; Stockhofe-Zurwieden, Norbert; Zaccaria, Edoardo; Tommassen, Jan; Wells, Jerry M.; Smith, Hilde E.; de Greeff, Astrid.

In: Virulence, Vol. 10, No. 1, 07.04.2019, p. 334-351.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Arenas, Jesús

AU - Bossers-de Vries, Ruth

AU - Harders-Westerveen, José

AU - Buys, Herma

AU - Ruuls-van Stalle, Lisette M.F.

AU - Stockhofe-Zurwieden, Norbert

AU - Zaccaria, Edoardo

AU - Tommassen, Jan

AU - Wells, Jerry M.

AU - Smith, Hilde E.

AU - de Greeff, Astrid

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N2 - Streptococcus suis is a Gram-positive bacterium and a zoonotic pathogen residing in the nasopharynx or the gastrointestinal tract of pigs with a potential of causing life-threatening invasive disease. It is endemic in the porcine production industry worldwide, and it is also an emerging human pathogen. After invasion, the pathogen adapts to cause bacteremia and disseminates to different organs including the brain. To gain insights in this process, we infected piglets with a highly virulent strain of S. suis, and bacterial transcriptomes were obtained from blood and different organs (brain, joints, and heart) when animals had severe clinical symptoms of infection. Microarrays were used to determine the genome-wide transcriptional profile at different infection sites and during growth in standard growth medium in vitro. We observed differential expression of around 30% of the Open Reading Frames (ORFs) and infection-site specific patterns of gene expression. Genes with major changes in expression were involved in transcriptional regulation, metabolism, nutrient acquisition, stress defenses, and virulence, amongst others, and results were confirmed for a subset of selected genes using RT-qPCR. Mutants were generated in two selected genes, and the encoded proteins, i.e., NADH oxidase and MetQ, were shown to be important virulence factors in coinfection experiments and in vitro assays. The knowledge derived from this study regarding S. suis gene expression in vivo and identification of virulence factors is important for the development of novel diagnostic and therapeutic strategies to control S. suis disease.

AB - Streptococcus suis is a Gram-positive bacterium and a zoonotic pathogen residing in the nasopharynx or the gastrointestinal tract of pigs with a potential of causing life-threatening invasive disease. It is endemic in the porcine production industry worldwide, and it is also an emerging human pathogen. After invasion, the pathogen adapts to cause bacteremia and disseminates to different organs including the brain. To gain insights in this process, we infected piglets with a highly virulent strain of S. suis, and bacterial transcriptomes were obtained from blood and different organs (brain, joints, and heart) when animals had severe clinical symptoms of infection. Microarrays were used to determine the genome-wide transcriptional profile at different infection sites and during growth in standard growth medium in vitro. We observed differential expression of around 30% of the Open Reading Frames (ORFs) and infection-site specific patterns of gene expression. Genes with major changes in expression were involved in transcriptional regulation, metabolism, nutrient acquisition, stress defenses, and virulence, amongst others, and results were confirmed for a subset of selected genes using RT-qPCR. Mutants were generated in two selected genes, and the encoded proteins, i.e., NADH oxidase and MetQ, were shown to be important virulence factors in coinfection experiments and in vitro assays. The knowledge derived from this study regarding S. suis gene expression in vivo and identification of virulence factors is important for the development of novel diagnostic and therapeutic strategies to control S. suis disease.

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KW - infectomics

KW - pathogenesis

KW - transcriptomics

KW - zoonotic pathogen

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VL - 10

SP - 334

EP - 351

JO - Virulence

T2 - Virulence

JF - Virulence

SN - 2150-5594

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