title: Variation in siderophore biosynthetic gene distribution and production across environmental and faecal populations of Escherichia coli.
abstract: 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.
authors.affiliation: Gut Health and Food Safety, Institute of Food Research, Norwich, United Kingdom.
authors.forename: Laura J
authors.initials: LJ
authors.lastname: Searle
authors.affiliation: Gut Health and Food Safety, Institute of Food Research, Norwich, United Kingdom; Institute of Life Science, College of Medicine, Swansea University, Swansea, United Kingdom.
authors.forename: Guillaume
authors.initials: G
authors.lastname: Méric
authors.affiliation: Gut Health and Food Safety, Institute of Food Research, Norwich, United Kingdom.
authors.forename: Ida
authors.initials: I
authors.lastname: Porcelli
authors.affiliation: Institute of Life Science, College of Medicine, Swansea University, Swansea, United Kingdom; Department of Zoology, University of Oxford, Oxford, United Kingdom.
authors.forename: Samuel K
authors.initials: SK
authors.lastname: Sheppard
authors.affiliation: Gut Health and Food Safety, Institute of Food Research, Norwich, United Kingdom.
authors.forename: Sacha
authors.initials: S
authors.lastname: Lucchini
mesh_terms: D000220:Adaptation, Biological; D000818:Animals; D004758:Enterobactin / Q000031:analogs & derivatives / Q000235:genetics / Q000378:metabolism; D004783:Environmental Microbiology; D004926:Escherichia coli / Q000235:genetics / Q000302:isolation & purification* / Q000378:metabolism; D029968:Escherichia coli Proteins / Q000235:genetics / Q000378:metabolism*; D005243:Feces / Q000382:microbiology*; D005960:Glucosides / Q000235:genetics / Q000378:metabolism; D006801:Humans; D006877:Hydroxamic Acids / Q000378:metabolism; D007501:Iron / Q000378:metabolism; D010636:Phenols / Q000378:metabolism; D010944:Plants / Q000382:microbiology*; D017262:Siderophores / Q000235:genetics / Q000378:metabolism*; D013844:Thiazoles / Q000378:metabolism; D037521:Virulence Factors / Q000235:genetics / Q000378:metabolism
chemical_list: D029968:Escherichia coli Proteins; D005960:Glucosides; D006877:Hydroxamic Acids; D010636:Phenols; D017262:Siderophores; D013844:Thiazoles; D037521:Virulence Factors; C508254:salmochelin S4; C104398:yersiniabactin; C031819:aerobactin; D004758:Enterobactin; D007501:Iron