Variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of Escherichia coli.
Iron is essential for Escherichia coli growth and survival in the host and the external environment, but its availability is generally low due to the poor solubility of its ferric form in aqueous environments and the presence of iron-withholding proteins in the host. Most E. coli can increase access...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2015-01-01
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| Series: | PLoS ONE |
| Online Access: | http://europepmc.org/articles/PMC4355413?pdf=render |
| _version_ | 1811319691661017088 |
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| author | Laura J Searle Guillaume Méric Ida Porcelli Samuel K Sheppard Sacha Lucchini |
| author_facet | Laura J Searle Guillaume Méric Ida Porcelli Samuel K Sheppard Sacha Lucchini |
| author_sort | Laura J Searle |
| collection | DOAJ |
| description | Iron is essential for Escherichia coli growth and survival in the host and the external environment, but its availability is generally low due to the poor solubility of its ferric form in aqueous environments and the presence of iron-withholding proteins in the host. Most E. coli can increase access to iron by excreting siderophores such as enterobactin, which have a very strong affinity for Fe3+. A smaller proportion of isolates can generate up to 3 additional siderophores linked with pathogenesis; aerobactin, salmochelin, and yersiniabactin. However, non-pathogenic E. coli are also able to synthesise these virulence-associated siderophores. This raises questions about their role in the ecology of E. coli, beyond virulence, and whether specific siderophores might be linked with persistence in the external environment. Under the assumption that selection favours phenotypes that confer a fitness advantage, we compared siderophore production and gene distribution in E. coli isolated either from agricultural plants or the faeces of healthy mammals. This population-level comparison has revealed that under iron limiting growth conditions plant-associated isolates produced lower amounts of siderophores than faecal isolates. Additionally, multiplex PCR showed that environmental isolates were less likely to contain loci associated with aerobactin and yersiniabactin synthesis. Although aerobactin was linked with strong siderophore excretion, a significant difference in production was still observed between plant and faecal isolates when the analysis was restricted to strains only able to synthesise enterobactin. This finding suggests that the regulatory response to iron limitation may be an important trait associated with adaptation to the non-host environment. Our findings are consistent with the hypothesis that the ability to produce multiple siderophores facilitates E. coli gut colonisation and plays an important role in E. coli commensalism. |
| first_indexed | 2024-04-13T12:47:06Z |
| format | Article |
| id | doaj.art-2da6370f0a3143e0954ed7b2edef6a17 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-04-13T12:47:06Z |
| publishDate | 2015-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-2da6370f0a3143e0954ed7b2edef6a172022-12-22T02:46:20ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-01103e011790610.1371/journal.pone.0117906Variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of Escherichia coli.Laura J SearleGuillaume MéricIda PorcelliSamuel K SheppardSacha LucchiniIron is essential for Escherichia coli growth and survival in the host and the external environment, but its availability is generally low due to the poor solubility of its ferric form in aqueous environments and the presence of iron-withholding proteins in the host. Most E. coli can increase access to iron by excreting siderophores such as enterobactin, which have a very strong affinity for Fe3+. A smaller proportion of isolates can generate up to 3 additional siderophores linked with pathogenesis; aerobactin, salmochelin, and yersiniabactin. However, non-pathogenic E. coli are also able to synthesise these virulence-associated siderophores. This raises questions about their role in the ecology of E. coli, beyond virulence, and whether specific siderophores might be linked with persistence in the external environment. Under the assumption that selection favours phenotypes that confer a fitness advantage, we compared siderophore production and gene distribution in E. coli isolated either from agricultural plants or the faeces of healthy mammals. This population-level comparison has revealed that under iron limiting growth conditions plant-associated isolates produced lower amounts of siderophores than faecal isolates. Additionally, multiplex PCR showed that environmental isolates were less likely to contain loci associated with aerobactin and yersiniabactin synthesis. Although aerobactin was linked with strong siderophore excretion, a significant difference in production was still observed between plant and faecal isolates when the analysis was restricted to strains only able to synthesise enterobactin. This finding suggests that the regulatory response to iron limitation may be an important trait associated with adaptation to the non-host environment. Our findings are consistent with the hypothesis that the ability to produce multiple siderophores facilitates E. coli gut colonisation and plays an important role in E. coli commensalism.http://europepmc.org/articles/PMC4355413?pdf=render |
| spellingShingle | Laura J Searle Guillaume Méric Ida Porcelli Samuel K Sheppard Sacha Lucchini Variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of Escherichia coli. PLoS ONE |
| title | Variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of Escherichia coli. |
| title_full | Variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of Escherichia coli. |
| title_fullStr | Variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of Escherichia coli. |
| title_full_unstemmed | Variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of Escherichia coli. |
| title_short | Variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of Escherichia coli. |
| title_sort | variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of escherichia coli |
| url | http://europepmc.org/articles/PMC4355413?pdf=render |
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