Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic <italic toggle="yes">Escherichia coli</italic>

ABSTRACT 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 environme...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Shlomo E. Blum, Robert J. Goldstone, James P. R. Connolly, Maryline Répérant-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
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Escherichia coli bovine ferric citrate mammary gland mastitis milk Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/adf8534cbb094e8e93aeaeafbec91e0a
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:adf8534cbb094e8e93aeaeafbec91e0a
record_format	dspace
spelling	oai:doaj.org-article:adf8534cbb094e8e93aeaeafbec91e0a2021-11-15T15:53:27ZPostgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic <italic toggle="yes">Escherichia coli</italic>10.1128/mBio.00423-182150-7511https://doaj.org/article/adf8534cbb094e8e93aeaeafbec91e0a2018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00423-18https://doaj.org/toc/2150-7511ABSTRACT 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. IMPORTANCE Bovine mastitis is the major infectious disease in dairy cows and the leading cause of economic loss to the global dairy industry, directly contributing to the price of dairy products on supermarket shelves and the financial hardships suffered by dairy farmers. Mastitis is also the leading reason for the use of antibiotics in dairy farms. Good farm management practices in many countries have dramatically reduced the incidence of contagious mastitis; however, the problems associated with the incidence of environmental mastitis caused by bacteria such as Escherichia coli have proven intractable. E. coli bacteria cause acute mastitis, which affects the health and welfare of cows and in extreme cases may be fatal. Here we show for the first time that the pathogenicity of E. coli causing mastitis in cows is highly dependent on the fecIRABCDE ferric citrate uptake system that allows the bacterium to capture iron from citrate. The Fec system is highly expressed during infection in the bovine udder and is ubiquitous in and necessary for the E. coli bacteria that cause mammary infections in cattle. These results have far-reaching implications, raising the possibility that mastitis may be controllable by targeting this system.Shlomo E. BlumRobert J. GoldstoneJames P. R. ConnollyMaryline Répérant-FerterPierre GermonNeil F. InglisOleg KrifucksShubham MathurErin MansonKevin McleanPascal RainardAndrew J. RoeGabriel LeitnerDavid G. E. SmithAmerican Society for MicrobiologyarticleEscherichia colibovineferric citratemammary glandmastitismilkMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Escherichia coli bovine ferric citrate mammary gland mastitis milk Microbiology QR1-502
spellingShingle	Escherichia coli bovine ferric citrate mammary gland mastitis milk Microbiology QR1-502 Shlomo E. Blum Robert J. Goldstone James P. R. Connolly Maryline Répérant-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 Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic <italic toggle="yes">Escherichia coli</italic>
description	ABSTRACT 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. IMPORTANCE Bovine mastitis is the major infectious disease in dairy cows and the leading cause of economic loss to the global dairy industry, directly contributing to the price of dairy products on supermarket shelves and the financial hardships suffered by dairy farmers. Mastitis is also the leading reason for the use of antibiotics in dairy farms. Good farm management practices in many countries have dramatically reduced the incidence of contagious mastitis; however, the problems associated with the incidence of environmental mastitis caused by bacteria such as Escherichia coli have proven intractable. E. coli bacteria cause acute mastitis, which affects the health and welfare of cows and in extreme cases may be fatal. Here we show for the first time that the pathogenicity of E. coli causing mastitis in cows is highly dependent on the fecIRABCDE ferric citrate uptake system that allows the bacterium to capture iron from citrate. The Fec system is highly expressed during infection in the bovine udder and is ubiquitous in and necessary for the E. coli bacteria that cause mammary infections in cattle. These results have far-reaching implications, raising the possibility that mastitis may be controllable by targeting this system.
format	article
author	Shlomo E. Blum Robert J. Goldstone James P. R. Connolly Maryline Répérant-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
author_facet	Shlomo E. Blum Robert J. Goldstone James P. R. Connolly Maryline Répérant-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
author_sort	Shlomo E. Blum
title	Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic <italic toggle="yes">Escherichia coli</italic>
title_short	Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic <italic toggle="yes">Escherichia coli</italic>
title_full	Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic <italic toggle="yes">Escherichia coli</italic>
title_fullStr	Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic <italic toggle="yes">Escherichia coli</italic>
title_full_unstemmed	Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic <italic toggle="yes">Escherichia coli</italic>
title_sort	postgenomics characterization of an essential genetic determinant of mammary pathogenic <italic toggle="yes">escherichia coli</italic>
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/adf8534cbb094e8e93aeaeafbec91e0a
work_keys_str_mv	AT shlomoeblum postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT robertjgoldstone postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT jamesprconnolly postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT marylinereperantferter postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT pierregermon postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT neilfinglis postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT olegkrifucks postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT shubhammathur postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT erinmanson postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT kevinmclean postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT pascalrainard postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT andrewjroe postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT gabrielleitner postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic AT davidgesmith postgenomicscharacterizationofanessentialgeneticdeterminantofmammarypathogenicitalictoggleyesescherichiacoliitalic
_version_	1718427237245517824

Postgenomics Characterization of an Essential Genetic Determinant of Mammary Pathogenic <italic toggle="yes">Escherichia coli</italic>

Ejemplares similares