ShiF acts as an auxiliary factor of aerobactin secretion in meningitis Escherichia coli strain S88
Abstract Background The neonatal meningitis E. coli (NMEC) strain S88 carries a ColV plasmid named pS88 which is involved in meningeal virulence. Transcriptional analysis of pS88 in human serum revealed a strong upregulation of an ORF of unknown function: shiF, which is adjacent to the operon encodi...
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| Format: | Article |
| Language: | English |
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BMC
2019-12-01
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| Series: | BMC Microbiology |
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| Online Access: | https://doi.org/10.1186/s12866-019-1677-2 |
| _version_ | 1818380700421718016 |
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| author | Mathieu Genuini Philippe Bidet Jean-François Benoist Dimitri Schlemmer Chloé Lemaitre André Birgy Stéphane Bonacorsi |
| author_facet | Mathieu Genuini Philippe Bidet Jean-François Benoist Dimitri Schlemmer Chloé Lemaitre André Birgy Stéphane Bonacorsi |
| author_sort | Mathieu Genuini |
| collection | DOAJ |
| description | Abstract Background The neonatal meningitis E. coli (NMEC) strain S88 carries a ColV plasmid named pS88 which is involved in meningeal virulence. Transcriptional analysis of pS88 in human serum revealed a strong upregulation of an ORF of unknown function: shiF, which is adjacent to the operon encoding the siderophore aerobactin. The aim of this work is to investigate the role of shiF in aerobactin production in strain S88. Results Study of the prevalence of shiF and aerobactin operon in a collection of 100 extra-intestinal pathogenic E. coli strains (ExPEC) and 50 whole genome-sequenced E. coli strains revealed the colocalization of these two genes for 98% of the aerobactin positive strains. We used Datsenko and Wanner’s method to delete shiF in two S88 mutants. A cross-feeding assay showed that these mutants were able to excrete aerobactin meaning that shiF is dispensable for aerobactin excretion. Our growth assays revealed that the shiF-deleted mutants grew significantly slower than the wild-type strain S88 in iron-depleted medium with a decrease of maximum growth rates of 23 and 28% (p < 0.05). Using Liquid Chromatography-Mass Spectrometry, we identified and quantified siderophores in the supernatants of S88 and its shiF deleted mutants after growth in iron-depleted medium and found that these mutants secreted significantly less aerobactin than S88 (− 52% and - 49%, p < 0.001). Conclusions ShiF is physically and functionally linked to aerobactin. It provides an advantage to E. coli S88 under iron-limiting conditions by increasing aerobactin secretion and may thus act as an auxiliary virulence factor. |
| first_indexed | 2024-12-14T02:22:51Z |
| format | Article |
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| institution | Directory Open Access Journal |
| issn | 1471-2180 |
| language | English |
| last_indexed | 2024-12-14T02:22:51Z |
| publishDate | 2019-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Microbiology |
| spelling | doaj.art-cccc7fa8cd9f4d38a5b7bb703b794ae42022-12-21T23:20:28ZengBMCBMC Microbiology1471-21802019-12-011911810.1186/s12866-019-1677-2ShiF acts as an auxiliary factor of aerobactin secretion in meningitis Escherichia coli strain S88Mathieu Genuini0Philippe Bidet1Jean-François Benoist2Dimitri Schlemmer3Chloé Lemaitre4André Birgy5Stéphane Bonacorsi6University Paris Diderot, Sorbonne Paris Cité, IAMEUniversity Paris Diderot, Sorbonne Paris Cité, IAMEService de Biochimie-Hormonologie, AP-HP Hôpital Robert DebréService de Biochimie-Hormonologie, AP-HP Hôpital Robert DebréUniversity Paris Diderot, Sorbonne Paris Cité, IAMEUniversity Paris Diderot, Sorbonne Paris Cité, IAMEUniversity Paris Diderot, Sorbonne Paris Cité, IAMEAbstract Background The neonatal meningitis E. coli (NMEC) strain S88 carries a ColV plasmid named pS88 which is involved in meningeal virulence. Transcriptional analysis of pS88 in human serum revealed a strong upregulation of an ORF of unknown function: shiF, which is adjacent to the operon encoding the siderophore aerobactin. The aim of this work is to investigate the role of shiF in aerobactin production in strain S88. Results Study of the prevalence of shiF and aerobactin operon in a collection of 100 extra-intestinal pathogenic E. coli strains (ExPEC) and 50 whole genome-sequenced E. coli strains revealed the colocalization of these two genes for 98% of the aerobactin positive strains. We used Datsenko and Wanner’s method to delete shiF in two S88 mutants. A cross-feeding assay showed that these mutants were able to excrete aerobactin meaning that shiF is dispensable for aerobactin excretion. Our growth assays revealed that the shiF-deleted mutants grew significantly slower than the wild-type strain S88 in iron-depleted medium with a decrease of maximum growth rates of 23 and 28% (p < 0.05). Using Liquid Chromatography-Mass Spectrometry, we identified and quantified siderophores in the supernatants of S88 and its shiF deleted mutants after growth in iron-depleted medium and found that these mutants secreted significantly less aerobactin than S88 (− 52% and - 49%, p < 0.001). Conclusions ShiF is physically and functionally linked to aerobactin. It provides an advantage to E. coli S88 under iron-limiting conditions by increasing aerobactin secretion and may thus act as an auxiliary virulence factor.https://doi.org/10.1186/s12866-019-1677-2Escherichia coliSiderophoreAerobactinShiF |
| spellingShingle | Mathieu Genuini Philippe Bidet Jean-François Benoist Dimitri Schlemmer Chloé Lemaitre André Birgy Stéphane Bonacorsi ShiF acts as an auxiliary factor of aerobactin secretion in meningitis Escherichia coli strain S88 BMC Microbiology Escherichia coli Siderophore Aerobactin ShiF |
| title | ShiF acts as an auxiliary factor of aerobactin secretion in meningitis Escherichia coli strain S88 |
| title_full | ShiF acts as an auxiliary factor of aerobactin secretion in meningitis Escherichia coli strain S88 |
| title_fullStr | ShiF acts as an auxiliary factor of aerobactin secretion in meningitis Escherichia coli strain S88 |
| title_full_unstemmed | ShiF acts as an auxiliary factor of aerobactin secretion in meningitis Escherichia coli strain S88 |
| title_short | ShiF acts as an auxiliary factor of aerobactin secretion in meningitis Escherichia coli strain S88 |
| title_sort | shif acts as an auxiliary factor of aerobactin secretion in meningitis escherichia coli strain s88 |
| topic | Escherichia coli Siderophore Aerobactin ShiF |
| url | https://doi.org/10.1186/s12866-019-1677-2 |
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