Abstract

Tellurite is highly toxic to most bacteria owing to its strong oxidative ability. However, some bacteria demonstrate tellurite resistance. In particular, some Escherichia coli strains, including Shiga toxin-producing E. coli O157:H7, are known to be resistant to tellurite. This resistance is involved in ter operon, which is usually located on a prophage-like element of the chromosome. The characteristics of the ter operon have been investigated mainly by genome analysis of pathogenic E. coli; however, the distribution and structural characteristics of the ter operon in other E. coli are almost unknown. To clarify these points, we examined 106 E. coli strains carrying the ter operon from various animals. The draft genomes of 34 representative strains revealed that ter operons were clearly classified into four subtypes, ter-type 1–4, at the nucleotide sequence level. Complete genomic sequences revealed that operons belonging to three ter-types (1, 3, and 4) were located on the prophage-like elements on the chromosome, whereas the ter-type 2 operon was located on the IncHI2 plasmid. The positions of the tRNASer, tRNAMet, and tRNAPhe indicated the insertion sites of elements carrying the ter operons. Using the PCR method developed in this study, 106 strains were classified as type 1 (n = 66), 2 (n = 13), 3 (n = 8), and 4 (n = 17), and two strains carried both types 1 and 2. Furthermore, significant differences in the minimum inhibitory concentration (MIC) of tellurite were observed between strains carrying ter-type 4 and the others (p < 0.05). The ter-type was also closely related to the isolation source, with types 2 and 4 associated with chickens and deer, respectively. This study provided new insights related not only to genetic characteristics of the ter operons, but also to phenotypic and ecological characteristics that may be related to the diversity of the operon.

Highlights

  • Tellurium (Te) is a rare element on Earth (Ibers, 2009) and is found in metal ores such as gold and copper (Terziev, 1966; Adams, 2016)

  • When a phylogenetic tree was created by adding 13 types of ter operons possessed by bacteria other than E. coli (Supplementary Table 2), three operons from Yersinia pseudotuberculosis, Salmonella enterica, and Klebsiella pneumoniae belonged to type-2, operons from seven Enterobacteriaceae genera formed an additional clade inside the group of E. coli-derived operons but no E. coli strain belonged to this clade, and the remaining three from Proteus mirabilis, Yersinia pestis, and Pseudomonas aeruginosa were distant from the E. coli-derived group (Supplementary Figure 2)

  • The integrase genes on the elements carrying the ter-type 1 operon were divided into two types according to the sequence homology: elements with one type of integrase gene were inserted into tRNASer and elements with the other type of integrase gene were inserted into tRNAMet (Figures 2, 6)

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Summary

Introduction

Tellurium (Te) is a rare element on Earth (Ibers, 2009) and is found in metal ores such as gold and copper (Terziev, 1966; Adams, 2016). Tellurite (TeO32−), the oxyanion of tellurium, is highly toxic to most bacteria owing to its strong oxidative ability. Tellurite toxicity is related to the generation of reactive oxygen species (ROS) (Turner et al, 2001; Pérez et al, 2007; Tremaroli et al, 2007; Calderón et al, 2009; Díaz-Vásquez et al, 2014; Sandoval et al, 2015), which induce damage. Most Shiga toxin-producing Escherichia coli (STEC) belonging to O157:H7 and other serotypes such as O26:H11, O103:H2, O111:H8, O121:H19, O145:H28, and O45:H2, which are responsible for numerous foodborne disease outbreaks, are known to possess tellurite resistance. When STEC is efficiently isolated from patient and food samples, selective agar plates containing potassium tellurite (K2TeO3), such as cefixime-tellurite sorbitol MacConkey (CT-SMAC) agar and CHROMagar STEC are routinely used in laboratories

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