AUTHOR=Hoyle Deborah V. , Wee Bryan A. , Macleod Kareen , Chase-Topping Margo E. , Bease Andrew G. , Tongue Sue C. , Gally David L. , Delannoy Sabine , Fach Patrick , Pearce Michael C. , Gunn George J. , Holmes Anne , Allison Lesley 

TITLE=Phylogenetic relationship and virulence composition of Escherichia coli O26:H11 cattle and human strain collections in Scotland; 2002–2020

JOURNAL=Frontiers in Microbiology

VOLUME=14

YEAR=2023

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2023.1260422

DOI=10.3389/fmicb.2023.1260422

ISSN=1664-302X

ABSTRACT=<p>O26 is the commonest non-O157 Shiga toxin (<italic>stx</italic>)-producing <italic>Escherichia coli</italic> serogroup reported in human infections worldwide. Ruminants, particularly cattle, are the primary reservoir source for human infection. In this study, we compared the whole genomes and virulence profiles of O26:H11 strains (<italic>n</italic> = 99) isolated from Scottish cattle with strains from human infections (<italic>n</italic> = 96) held by the Scottish <italic>Escherichia coli</italic> O157/STEC Reference Laboratory, isolated between 2002 and 2020. Bovine strains were from two national cross-sectional cattle surveys conducted between 2002–2004 and 2014–2015. A maximum likelihood phylogeny was constructed from a core-genome alignment with the O26:H11 strain 11368 reference genome. Genomes were screened against a panel of 2,710 virulence genes using the Virulence Finder Database. All <italic>stx</italic>-positive bovine O26:H11 strains belonged to the ST21 lineage and were grouped into three main clades. Bovine and human source strains were interspersed, and the <italic>stx</italic> subtype was relatively clade-specific. Highly pathogenic <italic>stx</italic>2a-only ST21 strains were identified in two herds sampled in the second cattle survey and in human clinical infections from 2010 onwards. The closest pairwise distance was 9 single-nucleotide polymorphisms (SNPs) between Scottish bovine and human strains and 69 SNPs between the two cattle surveys. Bovine O26:H11 was compared to public EnteroBase ST29 complex genomes and found to have the greatest commonality with O26:H11 strains from the rest of the UK, followed by France, Italy, and Belgium. Virulence profiles of <italic>stx</italic>-positive bovine and human strains were similar but more conserved for the <italic>stx2a</italic> subtype. O26:H11 <italic>stx</italic>-negative ST29 (<italic>n</italic> = 17) and ST396 strains (<italic>n</italic> = 5) were isolated from 19 cattle herds; all were <italic>eae</italic>-positive, and 10 of these herds yielded strains positive for <italic>ehxA</italic>, <italic>espK</italic>, and <italic>Z2098</italic>, gene markers suggestive of enterohaemorrhagic potential. There was a significant association (<italic>p</italic> &lt; 0.001) between nucleotide sequence percent identity and <italic>stx</italic> status for the bacteriophage insertion site genes <italic>yecE</italic> for <italic>stx2</italic> and <italic>yehV</italic> for <italic>stx1</italic>. Acquired antimicrobial resistance genes were identified <italic>in silico</italic> in 12.1% of bovine and 17.7% of human O26:H11 strains, with s<italic>ul2</italic>, <italic>tet</italic>, <italic>aph(3″),</italic> and <italic>aph(6″)</italic> being most common. This study describes the diversity among Scottish bovine O26:H11 strains and investigates their relationship to human STEC infections.</p>