Whole-Genome Analysis of
            <i>Salmonella enterica</i>
            Serovar Typhimurium T000240 Reveals the Acquisition of a Genomic Island Involved in Multidrug Resistance via IS
            <i>1</i>
            Derivatives on the Chromosome

Izumiya, Hidemasa; Sekizuka, Tsuyoshi; Nakaya, Hideo; Taguchi, Masumi; Oguchi, Akio; Ichikawa, Natsuko; Nishiko, Rika; Yamazaki, Shuji; Fujita, Nobuyuki; Watanabe, Haruo; Ohnishi, Makoto; Kuroda, Makoto

doi:10.1128/aac.01215-10

Cited by 44 publications

(41 citation statements)

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“…A unique 82-kb genomic island, GI-DT12, was recently reported in an S. Typhi-murium isolate collected from a human gastroenteritis case. The region was believed to have been acquired by horizontal gene transfer and harbored a class one integron, a mer operon, and several resistance genes believed to contribute to survival ability in adverse environments (39). This raises the issue of whether the acquisition of the chromosomal translocated region of the Zambian S. Typhi isolates was the consequence of an adverse environment due to poor sanitation.…”

Section: Discussionmentioning

confidence: 99%

Genomic Signature of Multidrug-Resistant Salmonella enterica Serovar Typhi Isolates Related to a Massive Outbreak in Zambia between 2010 and 2012

et al. 2015

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dRetrospectively, we investigated the epidemiology of a massive Salmonella enterica serovar Typhi outbreak in Zambia during 2010 to 2012. Ninety-four isolates were susceptibility tested by MIC determinations. Whole-genome sequence typing (WGST) of 33 isolates and bioinformatic analysis identified the multilocus sequence type (MLST), haplotype, plasmid replicon, antimicrobial resistance genes, and genetic relatedness by single nucleotide polymorphism (SNP) analysis and genomic deletions. The outbreak affected 2,040 patients, with a fatality rate of 0.5%. Most (83.0%) isolates were multidrug resistant (MDR). The isolates belonged to MLST ST1 and a new variant of the haplotype, H58B. Most isolates contained a chromosomally translocated region containing seven antimicrobial resistance genes, catA1, bla TEM-1 , dfrA7, sul1, sul2, strA, and strB, and fragments of the incompatibility group Q1 (IncQ1) plasmid replicon, the class 1 integron, and the mer operon. The genomic analysis revealed 415 SNP differences overall and 35 deletions among 33 of the isolates subjected to whole-genome sequencing. In comparison with other genomes of H58, the Zambian isolates separated from genomes from Central Africa and India by 34 and 52 SNPs, respectively. The phylogenetic analysis indicates that 32 of the 33 isolates sequenced belonged to a tight clonal group distinct from other H58 genomes included in the study. The small numbers of SNPs identified within this group are consistent with the short-term transmission that can be expected over a period of 2 years. The phylogenetic analysis and deletions suggest that a single MDR clone was responsible for the outbreak, during which occasional other S. Typhi lineages, including sensitive ones, continued to cocirculate. The common view is that the emerging global S. Typhi haplotype, H58B, containing the MDR IncHI1 plasmid is responsible for the majority of typhoid infections in Asia and sub-Saharan Africa; we found that a new variant of the haplotype harboring a chromosomally translocated region containing the MDR islands of IncHI1 plasmid has emerged in Zambia. This could change the perception of the term "classical MDR typhoid" currently being solely associated with the IncHI1 plasmid. It might be more common than presently thought that S. Typhi haplotype H58B harbors the IncHI1 plasmid or a chromosomally translocated MDR region or both.

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Section: Discussionmentioning

confidence: 99%

Genomic Signature of Multidrug-Resistant Salmonella enterica Serovar Typhi Isolates Related to a Massive Outbreak in Zambia between 2010 and 2012

et al. 2015

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“…The complete or partial loss of core genes was noted primarily in invasive strain D23580, MDR strain T000240, and in two closely related strains, UK-1 (called the "universal killer" for its pronounced invasion and virulence properties) and 14028S (15,17,39,40). This finding highlights a possible central role for gene inactivation in the evolution of fitness diversity in Salmonella Typhimurium strains.…”

Section: Discussionmentioning

confidence: 73%

“…Previous work demonstrated that this island has most likely helped the isolate to adapt to adverse environmental conditions such as extremely polluted sewage (17). In the additional 12 genomes, only two more genomic islands (in strains DT104, 138736, and L-3553) were identified that also carried both MDR and fitness genes.…”

Section: Discussionmentioning

confidence: 97%

“…Interestingly, however, the S. Heidelberg strain had the longer gene, whereas the shorter version was found in several other serovars, such as Enteritidis, Gallinarum, and Pullorum (data not shown). A detailed examination of the 114 strain-specific genes in T000240 showed that 100 genes were clustered in a single 82-kb chromosomal island GI-DT12 identified previously (17). The insertion site of GI-DT12 was in the middle of the putative regulatory gene STM14_4564 (as annotated in strain 14028S).…”

Section: Resultsmentioning

confidence: 99%

“…Salmonella serovar Typhimurium represents a broad-host-range spectrum and is one of the most commonly isolated serovars from human, retail meats of diverse origins, and the environment. Although S. Typhimurium is primarily known to cause self-limiting gastroenteritis, it can also be systemically invasive and exhibit a multidrug resistance (MDR) phenotype (15)(16)(17). Because Typhimurium serves as a complex serovar involving multiple eco-/pathovars, the horizontal acquisition of genetic material might play a pivotal role in the emergence and evolution of different S. Typhimurium strains.…”

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confidence: 99%

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Corrected Genome Annotations Reveal Gene Loss and Antibiotic Resistance as Drivers in the Fitness Evolution of Salmonella enterica Serovar Typhimurium

2016

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Horizontal acquisition of novel chromosomal genes is considered to be a key process in the evolution of bacterial pathogens. However, the identification of gene presence or absence could be hindered by the inconsistencies in bacterial genome annotations. Here, we performed a cross-annotation of omnipresent core and mosaic accessory genes in the chromosome of Salmonella enterica serovar Typhimurium across a total of 20 fully assembled genomes deposited into GenBank. Cross-annotation resulted in a 32% increase in the number of core genes and a 3-fold decrease in the number of genes identified as mosaic genes (i.e., genes present in some strains only) by the original annotation. Of the remaining noncore genes, the vast majority were prophage genes, and 255 of the nonphage genes were actually of core origin but lost in some strains upon the emergence of the S. Typhimurium serovar, suggesting that the chromosomal portion of the S. Typhimurium genome acquired a very limited number of novel genes other than prophages. Only horizontally acquired nonphage genes related to bacterial fitness or virulence were found in four recently sequenced isolates, all located on three different genomic islands that harbor multidrug resistance determinants. Thus, the extensive use of antimicrobials could be the main selection force behind the new fitness gene acquisition and the emergence of novel Salmonella pathotypes. IMPORTANCESignificant discrepancies in the annotations of bacterial genomes could mislead the conclusions about evolutionary origin of chromosomal genes, as we demonstrate here via a cross-annotation-based analysis of Salmonella Typhimurium genomes from GenBank. We conclude that despite being able to infect a broad range of vertebrate hosts, the genomic diversity of S. Typhimurium strains is almost exclusively limited to gene loss and the transfer of prophage DNA. Only nonphage chromosomal genes acquired after the emergence of the serovar are linked to the genomic islands harboring multidrug resistance factors. Since the fitness factors could lead to increased virulence, this poses an important research question: could overuse or misuse of antimicrobials act as selection forces for the emergence of more pathogenic strains of Salmonella? H orizontal gene transfer in bacteria is a major force in adaptation to novel environments, in genome diversification, and, in particular, in the evolution of bacterial virulence (1-4). Horizontally transferred genes create a mosaic structure of the species pangenome, where the so-called accessory genes are present only in some strains, in contrast to the core genes that are typically present in all strains (5-7). The chromosomal accessory genes can be subdivided into genes of phage origin and nonphage genes. The latter usually are acquired in the form of genomic islands, episomes, or transposons that are often related to bacterial physiology, antigenic diversification, and thus fitness (4,7,8). In contrast, the phage genes are directly related to phage physiology, although many p...

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DNA Traffic in the Environment and Antimicrobial Resistance

Hooton

Millard

Baker

et al. 2019

DNA Traffic in the Environment

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Whole-Genome Analysis of Salmonella enterica Serovar Typhimurium T000240 Reveals the Acquisition of a Genomic Island Involved in Multidrug Resistance via IS 1 Derivatives on the Chromosome

Cited by 44 publications

References 44 publications

Genomic Signature of Multidrug-Resistant Salmonella enterica Serovar Typhi Isolates Related to a Massive Outbreak in Zambia between 2010 and 2012

Genomic Signature of Multidrug-Resistant Salmonella enterica Serovar Typhi Isolates Related to a Massive Outbreak in Zambia between 2010 and 2012

Corrected Genome Annotations Reveal Gene Loss and Antibiotic Resistance as Drivers in the Fitness Evolution of Salmonella enterica Serovar Typhimurium

DNA Traffic in the Environment and Antimicrobial Resistance

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