Genomic population structure associated with repeated escape of Salmonella enterica ATCC14028s from the laboratory into nature

Salmonella enterica serovar Typhimurium strain ATCC14028s is commercially available from multiple national type culture collections, and has been widely used since 1960 for quality control of growth media and experiments on fitness (“laboratory evolution”). ATCC14028s has been implicated in multiple cross-contaminations in the laboratory, and has also caused multiple laboratory infections and one known attempt at bioterrorism. According to hierarchical clustering of 3002 core gene sequences, ATCC14028s belongs to HierCC cluster HC20_373 in which most internal branch lengths are only one to three SNPs long. Many natural Typhimurium isolates from humans, domesticated animals and the environment also belong to HC20_373, and their core genomes are almost indistinguishable from those of laboratory strains. These natural isolates have infected humans in Ireland and Taiwan for decades, and are common in the British Isles as well as the Americas. The isolation history of some of the natural isolates confirms the conclusion that they do not represent recent contamination by the laboratory strain, and 10% carry plasmids or bacteriophages which have been acquired in nature by HGT from unrelated bacteria. We propose that ATCC14028s has repeatedly escaped from the laboratory environment into nature via laboratory accidents or infections, but the escaped micro-lineages have only a limited life span. As a result, there is a genetic gap separating HC20_373 from its closest natural relatives due to a divergence between them in the late 19th century followed by repeated extinction events of escaped HC20_373.

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The Odyssey of the Ancestral Escherich Strain through Culture Collections: an Example of Allopatric Diversification

mSphere ◽

10.1128/msphere.00553-17 ◽

2018 ◽

Vol 3 (1) ◽

Cited By ~ 6

Author(s):

M. Desroches ◽

G. Royer ◽

D. Roche ◽

M. Mercier-Darty ◽

D. Vallenet ◽

...

Keyword(s):

Experimental Evolution ◽

Efflux Pump ◽

Strain History ◽

Culture Collections ◽

E Coli ◽

Molecular Features ◽

Natural Isolates ◽

History Of ◽

Encoding Genes

Mutator phenotypes have been described in laboratory-evolved bacteria, as well as in natural isolates. Several genes can be impacted, each of them being associated with a typical mutational spectrum. By studying one of the oldest strains available, the ancestral Escherich strain, we were able to identify its mutator status leading to tremendous genetic diversity among the isolates from various collections and allowing us to reconstruct the phylogeographic history of the strain. This mutator phenotype was probably acquired during the storage of the strain, promoting adaptation to a specific environment. Other mutations inrpoSand efflux pump- and porin-encoding genes highlight the acclimatization of the strain through self-preservation and nutritional competence regulation. This strain history can be viewed as unintentional experimental evolution in culture collections all over the word since 1885, mimicking the long-term experimental evolution ofE. coliof Lenski et al. (O. Tenaillon, J. E. Barrick, N. Ribeck, D. E. Deatherage, J. L. Blanchard, A. Dasgupta, G. C. Wu, S. Wielgoss, S. Cruveiller, C. Médigue, D. Schneider, and R. E. Lenski, Nature 536:165–170, 2016, https://doi.org/10.1038/nature18959) that shares numerous molecular features.

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Infected subdural haematoma due to Salmonella enterica serovar Typhimurium in an adult

Journal of Medical Microbiology ◽

10.1099/jmm.0.019323-0 ◽

2010 ◽

Vol 59 (8) ◽

pp. 976-979 ◽

Cited By ~ 4

Author(s):

Kayoko Hayakawa ◽

Akihiro Oikawa ◽

Naoto Takeda ◽

Kuri Sasaki ◽

Shuji Hatakeyama

Keyword(s):

Case Report ◽

Salmonella Enterica ◽

Subdural Haematoma ◽

Salmonella Enterica Serovar Typhimurium ◽

Subdural Empyema ◽

Surgical Drainage ◽

Detailed Case ◽

Serovar Typhimurium ◽

History Of ◽

Detailed Case Report

A 65-year-old man with a history of alcoholism and gastrectomy was diagnosed with an infected subdural haematoma due to Salmonella enterica serovar Typhimurium. He was successfully treated with surgical drainage and intravenous ceftriaxone. To our knowledge, there has been no detailed case report in English of infected subdural haematoma or subdural empyema due to Salmonella Typhimurium in adults.

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A soxRS-Constitutive Mutation Contributing to Antibiotic Resistance in a Clinical Isolate of Salmonella enterica (Serovar Typhimurium)

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.45.1.38-43.2001 ◽

2001 ◽

Vol 45 (1) ◽

pp. 38-43 ◽

Cited By ~ 71

Author(s):

Anastasia Koutsolioutsou ◽

Elizabeth A. Martins ◽

D. G. White ◽

S. B. Levy ◽

Bruce Demple

Keyword(s):

Antibiotic Resistance ◽

Salmonella Enterica ◽

Constitutive Expression ◽

Laboratory Strain ◽

Quinolone Resistance ◽

Clinical Strain ◽

Enteropathogenic Bacteria ◽

Development Of Resistance ◽

Serovar Typhimurium ◽

Constitutive Mutation

ABSTRACT The soxRS regulon is activated by redox-cycling drugs such as paraquat and by nitric oxide. The >15 genes of this system provide resistance to both oxidants and multiple antibiotics. An association between clinical quinolone resistance and elevated expression of the soxRS regulon has been observed inEscherichia coli, but this association has not been explored for other enteropathogenic bacteria. Here we describe asoxRS-constitutive mutation in a clinical strain ofSalmonella enterica (serovar Typhimurium) that arose with the development of resistance to quinolones during treatment. The elevated quinolone resistance in this strain derived from a point mutation in the soxR gene and could be suppressed intrans by multicopy wild-type soxRS. Multiple-antibiotic resistance was also transferred to a laboratory strain of S. enterica by introducing the cloned mutantsoxR gene from the clinical strain. The results show that constitutive expression of soxRS can contribute to antibiotic resistance in clinically relevant S. enterica.

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Global Genomic Epidemiology of Salmonella enterica Serovar Typhimurium DT104

Applied and Environmental Microbiology ◽

10.1128/aem.03821-15 ◽

2016 ◽

Vol 82 (8) ◽

pp. 2516-2526 ◽

Cited By ~ 49

Author(s):

Pimlapas Leekitcharoenphon ◽

Rene S. Hendriksen ◽

Simon Le Hello ◽

François-Xavier Weill ◽

Dorte Lau Baggesen ◽

...

Keyword(s):

Salmonella Enterica ◽

Phylogenetic Trees ◽

Demographic History ◽

Credible Interval ◽

The United States ◽

Multidrug Resistant ◽

Content Type ◽

Genomic Epidemiology ◽

Serovar Typhimurium ◽

History Of

ABSTRACTIt has been 30 years since the initial emergence and subsequent rapid global spread of multidrug-resistantSalmonella entericaserovar Typhimurium DT104 (MDR DT104). Nonetheless, its origin and transmission route have never been revealed. We used whole-genome sequencing (WGS) and temporally structured sequence analysis within a Bayesian framework to reconstruct temporal and spatial phylogenetic trees and estimate the rates of mutation and divergence times of 315S. Typhimurium DT104 isolates sampled from 1969 to 2012 from 21 countries on six continents. DT104 was estimated to have emerged initially as antimicrobial susceptible in ∼1948 (95% credible interval [CI], 1934 to 1962) and later became MDR DT104 in ∼1972 (95% CI, 1972 to 1988) through horizontal transfer of the 13-kbSalmonellagenomic island 1 (SGI1) MDR region into susceptible strains already containing SGI1. This was followed by multiple transmission events, initially from central Europe and later between several European countries. An independent transmission to the United States and another to Japan occurred, and from there MDR DT104 was probably transmitted to Taiwan and Canada. An independent acquisition of resistance genes took place in Thailand in ∼1975 (95% CI, 1975 to 1990). In Denmark, WGS analysis provided evidence for transmission of the organism between herds of animals. Interestingly, the demographic history of Danish MDR DT104 provided evidence for the success of the program to eradicateSalmonellafrom pig herds in Denmark from 1996 to 2000. The results from this study refute several hypotheses on the evolution of DT104 and suggest that WGS may be useful in monitoring emerging clones and devising strategies for prevention ofSalmonellainfections.

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Low tyrosine content of growth media yields aflagellate Salmonella enterica serovar Typhimurium

Microbiology ◽

10.1099/mic.0.28442-0 ◽

2006 ◽

Vol 152 (1) ◽

pp. 23-28 ◽

Cited By ~ 5

Author(s):

Victoria L. Gray ◽

Michael O'Reilly ◽

Carsten T. Müller ◽

Ian D. Watkins ◽

David Lloyd

Keyword(s):

Salmonella Enterica ◽

Culture Media ◽

Growth Media ◽

Carbohydrate Source ◽

Serovar Typhimurium ◽

Peptone Water ◽

Flagellar Filament ◽

Morphological Differences ◽

Tyrosine Concentration ◽

Tyrosine Content

Identification of Salmonella serotypes is based on flagellar and somatic antigens. The absence of flagella may consequently affect complete identification of the serotype; here it is shown that Salmonella enterica serovar Typhimurium exhibits morphological differences dependent on the peptone constituents of the culture medium. Aflagellate salmonella were produced in certain media where the nutritional ingredient was casein-based peptone or gelatin-based peptone; in gelatin-based peptone, aggregates of salmonella were observed. However, in media containing soy-based peptone as the primary nutrient, salmonella displayed a normal flagellated morphology. Transfer of aflagellate salmonella from nutritionally poor media, with casein- or gelatin-based peptone, into rich nutrient broth allowed flagella synthesis, indicating that the aflagellate form is still able to produce flagella. Amino acid sequencing of the peptones producing aflagellate organisms showed a relatively low tyrosine concentration: only 0·03±0·01 g l−1 for gelatin-based buffered peptone water, compared to 0·21±0·01 for soy-based buffered peptone water. Tyrosine is essential for flagellin, which is the subunit of the salmonella flagellar filament. The addition of 200 μM tyrosine to casein-based peptone media produced flagellate salmonella; 2 mM glucose was needed in addition to tyrosine to achieve a similar morphology in gelatin-based media. Therefore, culture media containing less than 1·20 g tyrosine l−1, and of limited carbohydrate source, when used for serological testing of clinical isolates, may result in an incomplete serological identification.

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Pigeon-Associated Strains of Salmonella enterica Serovar Typhimurium Phage Type DT2 Have Genomic Rearrangements at rRNA Operons

Infection and Immunity ◽

10.1128/iai.72.12.7338-7341.2004 ◽

2004 ◽

Vol 72 (12) ◽

pp. 7338-7341 ◽

Cited By ~ 9

Author(s):

R. Allen Helm ◽

Steffen Porwollik ◽

April E. Stanley ◽

Stanley Maloy ◽

Michael McClelland ◽

...

Keyword(s):

Salmonella Enterica ◽

Salmonella Enterica Serovar Typhimurium ◽

Phage Type ◽

Laboratory Strain ◽

Genomic Rearrangements ◽

Serovar Typhimurium ◽

The Common ◽

Genomic Anomalies ◽

Common Laboratory

ABSTRACT Strains from a subgroup of Salmonella enterica serovar Typhimurium frequently associated with pigeon infections were tested for genomic anomalies and virulence in mice. Some strains have a genomic inversion between rrn operons. Two prophages found in the common laboratory strain LT2 were absent. Pigeon-associated strains are still virulent in mice.

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Fusidic Acid-Resistant Mutants of Salmonella enterica Serovar Typhimurium Have Low Levels of Heme and a Reduced Rate of Respiration and Are Sensitive to Oxidative Stress

Antimicrobial Agents and Chemotherapy ◽

10.1128/aac.48.10.3877-3883.2004 ◽

2004 ◽

Vol 48 (10) ◽

pp. 3877-3883 ◽

Cited By ~ 15

Author(s):

Mirjana Macvanin ◽

Andras Ballagi ◽

Diarmaid Hughes

Keyword(s):

Oxidative Stress ◽

Hydrogen Peroxide ◽

Fusidic Acid ◽

Salmonella Enterica ◽

Heme Biosynthesis ◽

Growth Media ◽

Fluorescence Measurements ◽

Serovar Typhimurium ◽

Low Levels ◽

Reduced Rate

ABSTRACT Mutations in the translation elongation factor G (EF-G) make Salmonella enterica serovar Typhimurium resistant to the antibiotic fusidic acid. Fusr mutants are hypersensitive to oxidative stress and rapidly lose viability in the presence of hydrogen peroxide. We show that this phenotype is associated with reduced activity of two catalase enzymes, HPI (a bifunctional catalase-hydroperoxidase) and HPII (a monofunctional catalase). These catalases require the iron-binding cofactor heme for their activity. Fusr mutants have a reduced rate of transcription of hemA, a gene whose product catalyzes the first committed step in heme biosynthesis. Hypersensitivity of Fusr mutants to hydrogen peroxide is abolished by the presence of δ-aminolevulinic acid, the precursor of heme synthesis, in the growth media and by the addition of glutamate or glutamine, amino acids required for the first step in heme biosynthesis. Fluorescence measurements show that the level of heme in a Fusr mutant is significantly lower than it is in the wild type. Heme is also an essential cofactor of cytochromes in the electron transport chain of respiration. We found that the rate of respiration is reduced significantly in Fusr mutants. Sequestration of divalent iron in the growth media decreases the sensitivity of Fusr mutants to oxidative stress. Taken together, these results suggest that Fusr mutants are hypersensitive to oxidative stress because their low levels of heme reduce both catalase activity and respiration capacity. The sensitivity of Fusr mutants to oxidative stress could be associated with loss of viability due to iron-mediated DNA damage in the presence of hydrogen peroxide. We argue that understanding the specific nature of antibiotic resistance fitness costs in different environments may be a generally useful approach in identifying physiological processes that could serve as novel targets for antimicrobial agents.

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