Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic Escherichia coli
Escherichia coli are major bacterial pathogens causing bovine mastitis, a disease of great economic impact on dairy production worldwide. This work aimed to study the virulence determinants of mammary pathogenic E. coli (MPEC). By whole-genome sequencing analysis of 40 MPEC and 22 environmental (“da...
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2018-04-01
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doaj-905260750c36453aa3929b5e4746f68f2021-07-02T09:23:31ZengAmerican Society for MicrobiologymBio2150-75112018-04-0192e00423-1810.1128/mBio.00423-18Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic Escherichia coliShlomo E. BlumRobert J. GoldstoneJames P. R. ConnollyMaryline Répéérant-FerterPierre GermonNeil F. InglisOleg KrifucksShubham MathurErin MansonKevin McleanPascal RainardAndrew J. RoeGabriel LeitnerDavid G. E. SmithRino RappuoliEscherichia coli are major bacterial pathogens causing bovine mastitis, a disease of great economic impact on dairy production worldwide. This work aimed to study the virulence determinants of mammary pathogenic E. coli (MPEC). By whole-genome sequencing analysis of 40 MPEC and 22 environmental (“dairy-farm” E. coli [DFEC]) strains, we found that only the fec locus (fecIRABCDE) for ferric dicitrate uptake was present in the core genome of MPEC and that it was absent in DFEC genomes (P < 0.05). Expression of the FecA receptor in the outer membrane was shown to be citrate dependent by mass spectrometry. FecA was overexpressed when bacteria were grown in milk. Transcription of the fecA gene and of the inner membrane transport component fecB gene was upregulated in bacteria recovered from experimental intramammary infection. The presence of the fec system was shown to affect the ability of E. coli to grow in milk. While the rate of growth in milk of fec-positive (fec+) DFEC was similar to that of MPEC, it was significantly lower in DFEC lacking fec. Furthermore, deletion of fec reduced the rate of growth in milk of MPEC strain P4, whereas fec-transformed non-mammary gland-pathogenic DFEC strain K71 gained the phenotype of the level of growth in milk observed in MPEC. The role of fec in E. coli intramammary pathogenicity was investigated in vivo in cows, with results showing that an MPEC P4 mutant lacking fec lost its ability to induce mastitis, whereas the fec+ DFEC K71 mutant was able to trigger intramammary inflammation. For the first time, a single molecular locus was shown to be crucial in MPEC pathogenicity.http://mbio.asm.org/cgi/content/full/9/2/e00423-18 |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Shlomo E. Blum Robert J. Goldstone James P. R. Connolly Maryline Répéérant-Ferter Pierre Germon Neil F. Inglis Oleg Krifucks Shubham Mathur Erin Manson Kevin Mclean Pascal Rainard Andrew J. Roe Gabriel Leitner David G. E. Smith Rino Rappuoli |
spellingShingle |
Shlomo E. Blum Robert J. Goldstone James P. R. Connolly Maryline Répéérant-Ferter Pierre Germon Neil F. Inglis Oleg Krifucks Shubham Mathur Erin Manson Kevin Mclean Pascal Rainard Andrew J. Roe Gabriel Leitner David G. E. Smith Rino Rappuoli Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic Escherichia coli mBio |
author_facet |
Shlomo E. Blum Robert J. Goldstone James P. R. Connolly Maryline Répéérant-Ferter Pierre Germon Neil F. Inglis Oleg Krifucks Shubham Mathur Erin Manson Kevin Mclean Pascal Rainard Andrew J. Roe Gabriel Leitner David G. E. Smith Rino Rappuoli |
author_sort |
Shlomo E. Blum |
title |
Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic Escherichia coli |
title_short |
Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic Escherichia coli |
title_full |
Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic Escherichia coli |
title_fullStr |
Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic Escherichia coli |
title_full_unstemmed |
Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic Escherichia coli |
title_sort |
postgenomics characterization of an essential genetic determinant of mammary pathogenic escherichia coli |
publisher |
American Society for Microbiology |
series |
mBio |
issn |
2150-7511 |
publishDate |
2018-04-01 |
description |
Escherichia coli are major bacterial pathogens causing bovine mastitis, a disease of great economic impact on dairy production worldwide. This work aimed to study the virulence determinants of mammary pathogenic E. coli (MPEC). By whole-genome sequencing analysis of 40 MPEC and 22 environmental (“dairy-farm” E. coli [DFEC]) strains, we found that only the fec locus (fecIRABCDE) for ferric dicitrate uptake was present in the core genome of MPEC and that it was absent in DFEC genomes (P < 0.05). Expression of the FecA receptor in the outer membrane was shown to be citrate dependent by mass spectrometry. FecA was overexpressed when bacteria were grown in milk. Transcription of the fecA gene and of the inner membrane transport component fecB gene was upregulated in bacteria recovered from experimental intramammary infection. The presence of the fec system was shown to affect the ability of E. coli to grow in milk. While the rate of growth in milk of fec-positive (fec+) DFEC was similar to that of MPEC, it was significantly lower in DFEC lacking fec. Furthermore, deletion of fec reduced the rate of growth in milk of MPEC strain P4, whereas fec-transformed non-mammary gland-pathogenic DFEC strain K71 gained the phenotype of the level of growth in milk observed in MPEC. The role of fec in E. coli intramammary pathogenicity was investigated in vivo in cows, with results showing that an MPEC P4 mutant lacking fec lost its ability to induce mastitis, whereas the fec+ DFEC K71 mutant was able to trigger intramammary inflammation. For the first time, a single molecular locus was shown to be crucial in MPEC pathogenicity. |
url |
http://mbio.asm.org/cgi/content/full/9/2/e00423-18 |
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