Elsevier

Microbial Pathogenesis

Volume 53, Issues 3–4, September–October 2012, Pages 180-182
Microbial Pathogenesis

Short communication
Escherichia coli strains with the capacity for long-term persistence in the bowel microbiota carry the potentially genotoxic pks island

https://doi.org/10.1016/j.micpath.2012.05.011Get rights and content

Abstract

The pks genomic island found in Escherichia coli strains of phylogenetic group B2 encodes colibactin, a polyketide-peptide genotoxin that causes DNA double-strand breaks. We investigated the relationship between carriage of the pks island and the capacity of E. coli strains to persist in the gut microbiota of 130 Swedish infants, who were followed from birth to 18 months of age. Long-term colonizers were significantly more likely to have the pks island than either intermediate-term colonizers or transient strains, which suggests that the pks island contributes to the pronounced gut-colonizing capacity of group B2 strains. Long-term persistence in the colon of pks island-containing E. coli strains may be associated with the induction of genomic mutations in the host intestine.

Introduction

Escherichia coli is a ubiquitous member of the gut microbiota and is also a pathogen. E. coli segregates into four main phylogenetic lineages: A, B1, B2, and D. Certain phylogenetic group B2 strains possess a genomic island, named pks, which carries a gene set that enables the production of a peptide-polyketide hybrid compound called “colibactin”. Strains that harbor the pks island cause DNA double-strand breaks that activate the DNA damage checkpoint pathway in mammalian cells, leading to cell cycle arrest and eventually causing cell death [1]. The pks island is widely distributed among E. coli group B2 strains isolated from the gut or from extra-intestinal sites [1], [2], [3].

Intestinal E. coli strains differ in their capacities to persist in the gut microbiota of the colonized individual. Long-term colonizers, i.e., resident strains, persist in the intestine for months or years, while transient strains disappear from the intestinal microbiota within weeks [4]. In several epidemiological studies, we have shown that certain virulence factor genes, which including the genes for adhesins (P- and type 1-fimbriae), hemolysin, capsular antigens (K1 and K5), and aerobactin, as well as the pathogenicity islands (PAI) PAI I–IV536, PAI IICFT073, and PAI IIJ96, and the PAI markers malX and usp are much more prevalent among strains that persist in the microbiota than among transient strains. Furthermore, the resident strains mostly belong to phylogenetic group B2 [5], [6], [7], [8], [9], [10], which also dominates the strains that cause extra-intestinal infections.

In the present study, we examined the ecological importance of the pks island for E. coli in the intestinal microbiota and whether it is associated with other pathogenicity traits. In this regard, we took advantage of a collection of 100 E. coli strains that were obtained from 130 healthy Swedish infants, who were followed longitudinally over the first 18 months of life. The colonization capacity of each strain has previously been determined. In the present study, we compared the pks island carriage rates of long-term colonizers, intermediate-term colonizers, and transient strains, and we studied the association between the presence of the pks island and several pathogenicity traits, including PAI markers and virulence factor genes.

Section snippets

Bacterial strains

The E. coli strains examined in the present study have been described previously [10]. In total, 100 E. coli strains from 130 healthy infants were examined. The infants participated in the ALLERGYFLORA birth-cohort study, which investigated the relationship between gut microbiota composition and allergy development [6], [10]. A rectal swab was obtained at 3 days of age and fecal samples were taken at 1, 2, 4, and 8 weeks, as well as at 6, 12, and 18 months of age. The isolates were processed as

Results

Of the 100 E. coli strains that were studied, 48 were assigned to phylogenetic group B2. We found that 33 (69%) of the B2 strains carried the pks island, which was not detected in the strains from the other phylogenetic groups. All the pks-positive strains (with the exception of one strain) were able to induce DNA double-strand breaks in the HeLa cells, which suggests that the pks island in these strains is functional. The presence of the pks island was examined in the long-term colonizers (n

Discussion

In the present study, we investigated the prevalence of the pks island and its association with the ability of bacteria to persist in the gut microbiota in 100 E. coli strains obtained from healthy Swedish infants who were followed during the first 18 months of life. In addition, we examined the linkages between the presence of the pks island and several PAI markers and virulence factor genes that have been previously shown to be associated with the persistence of E. coli strains in the gut.

Acknowledgments

We thank Michèle Boury for excellent technical assistance. This study was supported by the French National Research Agency (ANR-09-MIEN-005-01).

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