Large-scale genome analysis of bovine commensal Escherichia coli reveals that bovine-adapted E. Coli lineages are serving as evolutionary sources of the emergence of human intestinal pathogenic strains

Yoko Arimizu, Yumi Kirino, Mitsuhiko P. Sato, Koichi Uno, Toshio Sato, Yasuhiro Gotoh, Frédéric Auvray, Hubert Brugere, Eric Oswald, Jacques G. Mainil, Kelly S. Anklam, Dörte Döpfer, Shuji Yoshino, Tadasuke Ooka, Yasuhiro Tanizawa, Yasukazu Nakamura, Atsushi Iguchi, Tomoko Morita-Ishihara, Makoto Ohnishi, Koichi AkashiTetsuya Hayashi, Yoshitoshi Ogura

Research output: Contribution to journalArticle

Abstract

How pathogens evolve their virulence to humans in nature is a scientific issue of great medical and biological importance. Shiga toxin (Stx)–producing Escherichia coli (STEC) and enteropathogenic E. coli (EPEC) are the major foodborne pathogens that can cause hemolytic uremic syndrome and infantile diarrhea, respectively. The locus of enterocyte effacement (LEE)–encoded type 3 secretion system (T3SS) is the major virulence determinant of EPEC and is also possessed by major STEC lineages. Cattle are thought to be the primary reservoir of STEC and EPEC. However, genome sequences of bovine commensal E. coli are limited, and the emerging process of STEC and EPEC is largely unknown. Here, we performed a large-scale genomic comparison of bovine commensal E. coli with human commensal and clinical strains, including EPEC and STEC, at a global level. The analyses identified two distinct lineages, in which bovine and human commensal strains are enriched, respectively, and revealed that STEC and EPEC strains have emerged in multiple sublineages of the bovine-associated lineage. In addition to the bovine-associated lineage-specific genes, including fimbriae, capsule, and nutrition utilization genes, specific virulence gene communities have been accumulated in stx- and LEE-positive strains, respectively, with notable overlaps of community members. Functional associations of these genes probably confer benefits to these E. coli strains in inhabiting and/or adapting to the bovine intestinal environment and drive their evolution to highly virulent human pathogens under the bovine-adapted genetic background. Our data highlight the importance of large-scale genome sequencing of animal strains in the studies of zoonotic pathogens.

Original languageEnglish
Pages (from-to)1495-1505
Number of pages11
JournalGenome Research
Volume29
Issue number9
DOIs
Publication statusPublished - Jan 1 2019

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Enteropathogenic Escherichia coli
Genome
Escherichia coli
Virulence
Enterocytes
Genes
Infantile Diarrhea
Shiga-Toxigenic Escherichia coli
Hemolytic-Uremic Syndrome
Zoonoses
Capsules

All Science Journal Classification (ASJC) codes

  • Genetics
  • Genetics(clinical)

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Large-scale genome analysis of bovine commensal Escherichia coli reveals that bovine-adapted E. Coli lineages are serving as evolutionary sources of the emergence of human intestinal pathogenic strains. / Arimizu, Yoko; Kirino, Yumi; Sato, Mitsuhiko P.; Uno, Koichi; Sato, Toshio; Gotoh, Yasuhiro; Auvray, Frédéric; Brugere, Hubert; Oswald, Eric; Mainil, Jacques G.; Anklam, Kelly S.; Döpfer, Dörte; Yoshino, Shuji; Ooka, Tadasuke; Tanizawa, Yasuhiro; Nakamura, Yasukazu; Iguchi, Atsushi; Morita-Ishihara, Tomoko; Ohnishi, Makoto; Akashi, Koichi; Hayashi, Tetsuya; Ogura, Yoshitoshi.

In: Genome Research, Vol. 29, No. 9, 01.01.2019, p. 1495-1505.

Research output: Contribution to journalArticle

Arimizu, Y, Kirino, Y, Sato, MP, Uno, K, Sato, T, Gotoh, Y, Auvray, F, Brugere, H, Oswald, E, Mainil, JG, Anklam, KS, Döpfer, D, Yoshino, S, Ooka, T, Tanizawa, Y, Nakamura, Y, Iguchi, A, Morita-Ishihara, T, Ohnishi, M, Akashi, K, Hayashi, T & Ogura, Y 2019, 'Large-scale genome analysis of bovine commensal Escherichia coli reveals that bovine-adapted E. Coli lineages are serving as evolutionary sources of the emergence of human intestinal pathogenic strains', Genome Research, vol. 29, no. 9, pp. 1495-1505. https://doi.org/10.1101/gr.249268.119
Arimizu, Yoko ; Kirino, Yumi ; Sato, Mitsuhiko P. ; Uno, Koichi ; Sato, Toshio ; Gotoh, Yasuhiro ; Auvray, Frédéric ; Brugere, Hubert ; Oswald, Eric ; Mainil, Jacques G. ; Anklam, Kelly S. ; Döpfer, Dörte ; Yoshino, Shuji ; Ooka, Tadasuke ; Tanizawa, Yasuhiro ; Nakamura, Yasukazu ; Iguchi, Atsushi ; Morita-Ishihara, Tomoko ; Ohnishi, Makoto ; Akashi, Koichi ; Hayashi, Tetsuya ; Ogura, Yoshitoshi. / Large-scale genome analysis of bovine commensal Escherichia coli reveals that bovine-adapted E. Coli lineages are serving as evolutionary sources of the emergence of human intestinal pathogenic strains. In: Genome Research. 2019 ; Vol. 29, No. 9. pp. 1495-1505.
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AU - Morita-Ishihara, Tomoko

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