Comparative genomics of Clostridioides difficile toxinotypes identifies module-based toxin gene evolution

Clostridioides difficile is a common cause of nosocomial diarrhoea. Toxins TcdA and TcdB are considered to be the main virulence factors and are encoded by the PaLoc region, while the binary toxin encoded in the CdtLoc region also contributes to pathogenicity. Variant toxinotypes reflect the genetic diversity of a key toxin-encoding 19 kb genetic element (the PaLoc). Here, we present analysis of a comprehensive collection of all known major C. difficile toxinotypes to address the evolutionary relationships of the toxin gene variants, the mechanisms underlying the origin and development of variability in toxin genes and the PaLoc, and the relationship between structure and function in TcdB variants. The structure of both toxin genes is modular, composed of interspersed blocks of sequences corresponding to functional domains and having different evolutionary histories, as shown by the distribution of mutations along the toxin genes and by incongruences of domain phylogenies compared to overall C. difficile cluster organization. In TcdB protein, four mutation patterns could be differentiated, which correlated very well with the type of TcdB cytopathic effect (CPE) on cultured cells. Mapping these mutations to the three-dimensional structure of the TcdB showed that the majority of the variation occurs in surface residues and that point mutation at residue 449 in alpha helix 16 differentiated strains with different types of CPE. In contrast to the PaLoc, phylogenetic trees of the CdtLoc were more consistent with the core genome phylogenies, but there were clues that CdtLoc can also be exchanged between strains.

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High levels of toxigenic Clostridioides difficile contamination of hospital environments: a hidden threat in hospital-acquired infections in Kenya

Access Microbiology ◽

10.1099/acmi.0.000171 ◽

2020 ◽

Vol 2 (12) ◽

Author(s):

Erick Odoyo ◽

Cecilia Kyanya ◽

Winnie Mutai ◽

Lillian Musila

Keyword(s):

Type Species ◽

Hospital Environment ◽

Toxin Gene ◽

Enrichment Broth ◽

Content Type ◽

Link Type ◽

Clostridioides Difficile ◽

Hospital Environments ◽

Genes Encoding ◽

Binary Toxins

Introduction. The contribution of Clostridioides difficile (formerly Clostridium difficile ) to the burden of hospital-associated infections (HAIs) remains undetermined in many African countries. Aim. This study aimed to identify a sensitive and readily adaptable C. difficile detection assay and to evaluate the C. difficile HAI risk in Kenya. Methodology. Sterile swabs in neutralizing buffer were used to sample equipment or surfaces that patients and clinical staff touched frequently. These swabs were either plated directly on chromogenic agar or cultured in an enrichment broth before plating. The swab suspensions, enrichment broth and plate cultures were screened by quantitative PCR (qPCR) to determine the most efficient detection method. The HAI risk was evaluated by testing the C. difficile -positive samples by qPCR for the A, B and binary toxins. Results. C. difficile was detected on 4/57 (7.0 %) equipment and surfaces by direct culture. The additional enrichment step increased the detection rate 10-fold to 43/57 (75.4 %). In total, 51/57 (89.5 %) environmental samples were positive for C. difficile detected through either culture or qPCR. The genes encoding the primary toxins, tcdA and tcdB, were detected on six surfaces, while the genes encoding the binary toxins, cdtA and cdtB, were detected on 2/57 (3.5 %) and 3/57 (5.3 %) surfaces, respectively. Different C. difficile toxin gene profiles were detected: the tcdA+/tcdB− gene profile on 4/10 (40 %) high-touch surfaces, tcdA−/tcdB+ on 3/10 (30 %) surfaces, tcdA+/tcdB+/cdtA+/cdtB+ on 2/10 (20 %) surfaces and tcdA−/tcdB+/cdtB+ on one high-touch surface. Conclusion. The widespread contamination of hospital environments by toxigenic C. difficile gives a strong indication of the high risk of C. difficile infections (CDIs). The two-step culture process described can easily be adapted for monitoring hospital environment contamination by C. difficile .

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RstA Is a Major Regulator ofClostridioides difficileToxin Production and Motility

mBio ◽

10.1128/mbio.01991-18 ◽

2019 ◽

Vol 10 (2) ◽

Cited By ~ 10

Author(s):

Adrianne N. Edwards ◽

Brandon R. Anjuwon-Foster ◽

Shonna M. McBride

Keyword(s):

Gene Expression ◽

Dna Binding ◽

Toxin Production ◽

Toxin Gene ◽

Dna Binding Domain ◽

Content Type ◽

Toxin Genes ◽

Clostridioides Difficile ◽

Species Specific ◽

Toxin Gene Expression

ABSTRACTClostridioides difficileinfection (CDI) is a toxin-mediated diarrheal disease. Several factors have been identified that influence the production of the two majorC. difficiletoxins, TcdA and TcdB, but prior published evidence suggested that additional unknown factors were involved in toxin regulation. Previously, we identified aC. difficileregulator, RstA, that promotes sporulation and represses motility and toxin production. We observed that the predicted DNA-binding domain of RstA was required for RstA-dependent repression of toxin genes, motility genes, andrstAtranscription. In this study, we further investigated the regulation of toxin and motility gene expression by RstA. DNA pulldown assays confirmed that RstA directly binds therstApromoter via the predicted DNA-binding domain. Through mutational analysis of therstApromoter, we identified several nucleotides that are important for RstA-dependent transcriptional regulation. Further, we observed that RstA directly binds and regulates the promoters of the toxin genestcdAandtcdB, as well as the promoters for thesigDandtcdRgenes, which encode regulators of toxin gene expression. Complementation analyses with theClostridium perfringensRstA ortholog and a multispecies chimeric RstA protein revealed that theC. difficileC-terminal domain is required for RstA DNA-binding activity, suggesting that species-specific signaling controls RstA function. Our data demonstrate that RstA is a transcriptional repressor that autoregulates its own expression and directly inhibits transcription of the two toxin genes and two positive toxin regulators, thereby acting at multiple regulatory points to control toxin production.IMPORTANCEClostridioides difficileis an anaerobic, gastrointestinal pathogen of humans and other mammals.C. difficileproduces two major toxins, TcdA and TcdB, which cause the symptoms of the disease, and forms dormant endospores to survive the aerobic environment outside the host. A recently discovered regulatory factor, RstA, inhibits toxin production and positively influences spore formation. Herein, we determine that RstA directly binds its own promoter DNA to repress its own gene transcription. In addition, our data demonstrate that RstA directly represses toxin gene expression and gene expression of two toxin gene activators, TcdR and SigD, creating a complex regulatory network to tightly control toxin production. This study provides a novel regulatory link betweenC. difficilesporulation and toxin production. Further, our data suggest thatC. difficiletoxin production is regulated through a direct, species-specific sensing mechanism.

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Influence of SOS-inducing agents on the expression of ArtAB toxin gene in Salmonella enterica and Salmonella bongori

Microbiology ◽

10.1099/mic.0.000939 ◽

2020 ◽

Vol 166 (8) ◽

pp. 785-793

Author(s):

Shou Miura ◽

Yukino Tamamura ◽

Mariko Takayasu ◽

Miwa Sasaki ◽

Natsuko Nishimura ◽

...

Keyword(s):

Salmonella Enterica ◽

Type Species ◽

Phage Type ◽

Sos Response ◽

Toxin Gene ◽

Efficient Production ◽

Prophage Induction ◽

Content Type ◽

Link Type ◽

Quinolone Antibiotics

Salmonella enterica subspecies enterica serovar Typhimurium (S. Typhimurium) definitive phage type 104 (DT104), S. enterica subspecies enterica serovar Worthington (S. Worthington) and S. bongori produce ArtA and ArtB (ArtAB) toxin homologues, which catalyse ADP-ribosylation of pertussis toxin-sensitive G protein. ArtAB gene (artAB) is encoded on prophage in DT104 and its expression is induced by mitomycin C (MTC) and hydrogen peroxide (H2O2) that trigger the bacterial SOS response. Although the genetic regulatory mechanism associated with artAB expression is not characterized, it is thought to be associated with prophage induction, which occurs when the RecA-mediated SOS response is triggered. Here we show that subinhibitory concentration of quinolone antibiotics that are SOS-inducing agents, also induce ArtAB production in these Salmonella strains. Both MTC and fluoroquinolone antibiotics such as enrofloxacin-induced artA and recA transcription and artAB-encoding prophage (ArtAB-prophage) in DT104 and S. Worthington. However, in S. bongori , which harbours artAB genes on incomplete prophage, artA transcription was induced by MTC and enrofloxacin, but prophage induction was not observed. Taken together, these results suggest that SOS response followed by induction of artAB transcription is essential for ArtAB production. H2O2-mediated induction of ArtAB prophage and efficient production of ArtAB was observed in DT104 but not in S. Worthington and S. bongori . Therefore, induction of artAB expression with H2O2 is strain-specific, and the mode of action of H2O2 as an SOS-inducing agent might be different from those of MTC and quinolone antibiotics.

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A global to local genomics analysis of Clostridioides difficile ST1/RT027 identifies cryptic transmission events in a northern Arizona healthcare network

Microbial Genomics ◽

10.1099/mgen.0.000271 ◽

2019 ◽

Vol 5 (7) ◽

Cited By ~ 2

Author(s):

Charles H. D. Williamson ◽

Nathan E. Stone ◽

Amalee E. Nunnally ◽

Heidie M. Hornstra ◽

David M. Wagner ◽

...

Keyword(s):

Type Species ◽

Sequence Type ◽

Infection Prevention And Control ◽

Polymorphism Analysis ◽

Whole Genome ◽

Content Type ◽

Northern Arizona ◽

Healthcare Network ◽

Link Type ◽

Clostridioides Difficile

Clostridioides difficile is a ubiquitous, diarrhoeagenic pathogen often associated with healthcare-acquired infections that can cause a range of symptoms from mild, self-limiting disease to toxic megacolon and death. Since the early 2000s, a large proportion of C. difficile cases have been attributed to the ribotype 027 (RT027) lineage, which is associated with sequence type 1 (ST1) in the C. difficile multilocus sequence typing scheme. The spread of ST1 has been attributed, in part, to resistance to fluoroquinolones used to treat unrelated infections, which creates conditions ideal for C. difficile colonization and proliferation. In this study, we analysed 27 isolates from a healthcare network in northern Arizona, USA, and 1352 publicly available ST1 genomes to place locally sampled isolates into a global context. Whole genome, single nucleotide polymorphism analysis demonstrated that at least six separate introductions of ST1 were observed in healthcare facilities in northern Arizona over an 18-month sampling period. A reconstruction of transmission networks identified potential nosocomial transmission of isolates, which were only identified via whole genome sequence analysis. Antibiotic resistance heterogeneity was observed among ST1 genomes, including variability in resistance profiles among locally sampled ST1 isolates. To investigate why ST1 genomes are so common globally and in northern Arizona, we compared all high-quality C. difficile genomes and identified that ST1 genomes have gained and lost a number of genomic regions compared to all other C. difficile genomes; analyses of other toxigenic C. difficile sequence types demonstrate that this loss may be anomalous and could be related to niche specialization. These results suggest that a combination of antimicrobial resistance and gain and loss of specific genes may explain the prominent association of this sequence type with C. difficile infection cases worldwide. The degree of genetic variability in ST1 suggests that classifying all ST1 genomes into a quinolone-resistant hypervirulent clone category may not be appropriate. Whole genome sequencing of clinical C. difficile isolates provides a high-resolution surveillance strategy for monitoring persistence and transmission of C. difficile and for assessing the performance of infection prevention and control strategies.

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Genetic diversity and epidemiology of accessory gene regulator loci in Clostridioides difficile

Access Microbiology ◽

10.1099/acmi.0.000134 ◽

2020 ◽

Vol 2 (7) ◽

Author(s):

Yuta Okada ◽

Shu Okugawa ◽

Mahoko Ikeda ◽

Tatsuya Kobayashi ◽

Ryoichi Saito ◽

...

Keyword(s):

Genetic Diversity ◽

In Silico ◽

Type Species ◽

Clinical Samples ◽

Pcr Analysis ◽

Accessory Gene ◽

Content Type ◽

Link Type ◽

Accessory Gene Regulator ◽

Clostridioides Difficile

Quorum sensing is known to regulate bacterial virulence, and the accessory gene regulator (agr) loci is one of the genetic loci responsible for its regulation. Recent reports examining Clostridioides difficile show that two agr loci, agr1 and agr2, regulate toxin production, but the diversity of agr loci and their epidemiology is unknown. In our study, in silico analysis was performed to research genetic diversity of agr, and C. difficile isolates from clinical samples underwent multilocus sequence typing (MLST) and PCR analysis of agr loci. To reveal the distribution of agr among different strains, phylogenetic analysis was also performed. In our in silico analysis, two different subtypes, named agr2R and agr2M, were found in agr2, which were previously reported. PCR analysis of 133 C . difficile isolates showed that 131 strains had agr1, 61 strains had agr2R, and 26 strains had agr2M; agr2R was mainly found in clade 1 or clade 2 organisms, whereas agr2M was only found in clade 4. With rare exception, agr1-negative sequence types (STs) belonged to clade C-Ⅰ and C-Ⅲ, and one clade 4 strain had agr2R. Our study revealed subtypes of agr2 not previously recognized, and the distribution of several agr loci in C. difficile . These findings provide a foundation for further functional and clinical research of the agr loci.

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Clostridioides difficile strain-dependent and strain-independent adaptations to a microaerobic environment

Microbial Genomics ◽

10.1099/mgen.0.000738 ◽

2021 ◽

Vol 7 (12) ◽

Author(s):

Andy Weiss ◽

Christopher A. Lopez ◽

William N. Beavers ◽

Jhoana Rodriguez ◽

Eric P. Skaar

Keyword(s):

Type Species ◽

Clinical Manifestations ◽

Transcriptional Response ◽

Low Oxygen ◽

Independent Manner ◽

Content Type ◽

Link Type ◽

Clostridioides Difficile ◽

Conserved Genes ◽

Oxygen Concentrations

Clostridioides difficile (formerly Clostridium difficile ) colonizes the gastrointestinal tract following disruption of the microbiota and can initiate a spectrum of clinical manifestations ranging from asymptomatic to life-threatening colitis. Following antibiotic treatment, luminal oxygen concentrations increase, exposing gut microbes to potentially toxic reactive oxygen species. Though typically regarded as a strict anaerobe, C. difficile can grow at low oxygen concentrations. How this bacterium adapts to a microaerobic environment and whether those responses to oxygen are conserved amongst strains is not entirely understood. Here, two C. difficile strains (630 and CD196) were cultured in 1.5% oxygen and the transcriptional response to long-term oxygen exposure was evaluated via RNA-sequencing. During growth in a microaerobic environment, several genes predicted to protect against oxidative stress were upregulated, including those for rubrerythrins and rubredoxins. Transcription of genes involved in metal homeostasis was also positively correlated with increased oxygen levels and these genes were amongst the most differentially transcribed. To directly compare the transcriptional landscape between C. difficile strains, a ‘consensus-genome’ was generated. On the basis of the identified conserved genes, basal transcriptional differences as well as variations in the response to oxygen were evaluated. While several responses were similar between the strains, there were significant differences in the abundance of transcripts involved in amino acid and carbohydrate metabolism. Furthermore, intracellular metal concentrations significantly varied both in an oxygen-dependent and oxygen-independent manner. Overall, these results indicate that C. difficile adapts to grow in a low oxygen environment through transcriptional changes, though the specific strategy employed varies between strains.

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In vitro antivirulence activity of baicalin against Clostridioides difficile

Journal of Medical Microbiology ◽

10.1099/jmm.0.001179 ◽

2020 ◽

Vol 69 (4) ◽

pp. 631-639

Author(s):

Abraham Joseph Pellissery ◽

Poonam Gopika Vinayamohan ◽

Kumar Venkitanarayanan

Keyword(s):

Spore Germination ◽

Type Species ◽

Brain Heart Infusion ◽

Toxin Production ◽

Strictly Anaerobic ◽

Content Type ◽

Link Type ◽

Clostridioides Difficile ◽

Spore Outgrowth

Introduction. Clostridioides difficile is an enteric pathogen that causes a serious toxin-mediated colitis in humans. Bacterial exotoxins and sporulation are critical virulence components that contribute to pathogenesis, and disease transmission and relapse, respectively. Therefore, reducing toxin production and sporulation could significantly minimize C. difficile pathogenicity and disease outcome in affected individuals. Aim. This study investigated the efficacy of a natural flavone glycoside, baicalin, in reducing toxin synthesis, sporulation and spore germination in C. difficile in vitro. Methodology. Hypervirulent C. difficile isolates BAA 1870 or 1803 were cultured in brain heart infusion broth with or without the subinhibitory concentration (SIC) of baicalin, and incubated at 37 °C for 24 h under strictly anaerobic conditions. The supernatant was harvested after 24 h for determining C. difficile toxin production by ELISA. In addition, a similar experiment was performed wherein samples were harvested for assessing total viable counts, and heat-resistant spore counts at 72 h of incubation. Furthermore, C. difficile spore germination and spore outgrowth kinetics, with or without baicalin treatment, was measured in a plate reader by recording optical density at 600 nm. Finally, the effect of baicalin on C. difficile toxin, sporulation and virulence-associated genes was investigated using real-time quantitative PCR. Results. The SIC of baicalin significantly reduced toxin synthesis, sporulation and spore outgrowth when compared to control. In addition, C. difficile genes critical for pathogenesis were significantly down-regulated in the presence of baicalin. Conclusion. Our results suggest that baicalin could potentially be used to control C. difficile , and warrant future studies in vivo.

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A publicly accessible database for Clostridioides difficile genome sequences supports tracing of transmission chains and epidemics

Microbial Genomics ◽

10.1099/mgen.0.000410 ◽

2020 ◽

Vol 6 (8) ◽

Cited By ~ 5

Author(s):

Martinique Frentrup ◽

Zhemin Zhou ◽

Matthias Steglich ◽

Jan P. Meier-Kolthoff ◽

Markus Göker ◽

...

Keyword(s):

Hierarchical Clustering ◽

Type Species ◽

Global Scale ◽

Comparative Genomic ◽

Polymorphism Analysis ◽

Genome Sequences ◽

Single Linkage ◽

Content Type ◽

Link Type ◽

Clostridioides Difficile

Clostridioides difficile is the primary infectious cause of antibiotic-associated diarrhea. Local transmissions and international outbreaks of this pathogen have been previously elucidated by bacterial whole-genome sequencing, but comparative genomic analyses at the global scale were hampered by the lack of specific bioinformatic tools. Here we introduce a publicly accessible database within EnteroBase (http://enterobase.warwick.ac.uk) that automatically retrieves and assembles C. difficile short-reads from the public domain, and calls alleles for core-genome multilocus sequence typing (cgMLST). We demonstrate that comparable levels of resolution and precision are attained by EnteroBase cgMLST and single-nucleotide polymorphism analysis. EnteroBase currently contains 18 254 quality-controlled C. difficile genomes, which have been assigned to hierarchical sets of single-linkage clusters by cgMLST distances. This hierarchical clustering is used to identify and name populations of C. difficile at all epidemiological levels, from recent transmission chains through to epidemic and endemic strains. Moreover, it puts newly collected isolates into phylogenetic and epidemiological context by identifying related strains among all previously published genome data. For example, HC2 clusters (i.e. chains of genomes with pairwise distances of up to two cgMLST alleles) were statistically associated with specific hospitals (P<10−4) or single wards (P=0.01) within hospitals, indicating they represented local transmission clusters. We also detected several HC2 clusters spanning more than one hospital that by retrospective epidemiological analysis were confirmed to be associated with inter-hospital patient transfers. In contrast, clustering at level HC150 correlated with k-mer-based classification and was largely compatible with PCR ribotyping, thus enabling comparisons to earlier surveillance data. EnteroBase enables contextual interpretation of a growing collection of assembled, quality-controlled C. difficile genome sequences and their associated metadata. Hierarchical clustering rapidly identifies database entries that are related at multiple levels of genetic distance, facilitating communication among researchers, clinicians and public-health officials who are combatting disease caused by C. difficile .

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A species-wide genetic atlas of antimicrobial resistance in Clostridioides difficile

Microbial Genomics ◽

10.1099/mgen.0.000696 ◽

2021 ◽

Vol 7 (11) ◽

Author(s):

Korakrit Imwattana ◽

César Rodríguez ◽

Thomas V. Riley ◽

Daniel R. Knight

Keyword(s):

Antimicrobial Resistance ◽

Type Species ◽

Strong Association ◽

Tetracycline Resistance ◽

Multidrug Resistant ◽

Fluoroquinolone Resistance ◽

Content Type ◽

Link Type ◽

Clostridioides Difficile ◽

Geographical Regions

Antimicrobial resistance (AMR) plays an important role in the pathogenesis and spread of Clostridioides difficile infection (CDI), the leading healthcare-related gastrointestinal infection in the world. An association between AMR and CDI outbreaks is well documented, however, data is limited to a few ‘epidemic’ strains in specific geographical regions. Here, through detailed analysis of 10 330 publicly-available C. difficile genomes from strains isolated worldwide (spanning 270 multilocus sequence types (STs) across all known evolutionary clades), this study provides the first species-wide snapshot of AMR genomic epidemiology in C. difficile . Of the 10 330 C . difficile genomes, 4532 (43.9 %) in 89 STs across clades 1–5 carried at least one genotypic AMR determinant, with 901 genomes (8.7 %) carrying AMR determinants for three or more antimicrobial classes (multidrug-resistant, MDR). No AMR genotype was identified in any strains belonging to the cryptic clades. C. difficile from Australia/New Zealand had the lowest AMR prevalence compared to strains from Asia, Europe and North America (P<0.0001). Based on the phylogenetic clade, AMR prevalence was higher in clades 2 (84.3 %), 4 (81.5 %) and 5 (64.8 %) compared to other clades (collectively 26.9 %) (P<0.0001). MDR prevalence was highest in clade 4 (61.6 %) which was over three times higher than in clade 2, the clade with the second-highest MDR prevalence (18.3 %). There was a strong association between specific AMR determinants and three major epidemic C. difficile STs: ST1 (clade 2) with fluoroquinolone resistance (mainly T82I substitution in GyrA) (P<0.0001), ST11 (clade 5) with tetracycline resistance (various tet-family genes) (P<0.0001) and ST37 (clade 4) with macrolide-lincosamide-streptogramin B (MLSB) resistance (mainly ermB) (P<0.0001) and MDR (P<0.0001). A novel and previously overlooked tetM-positive transposon designated Tn6944 was identified, predominantly among clade 2 strains. This study provides a comprehensive review of AMR in the global C. difficile population which may aid in the early detection of drug-resistant C. difficile strains, and prevention of their dissemination worldwide.

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Duplication and diversification of a unique chromosomal virulence island hosting the subtilase cytotoxin in Escherichia coli ST58

Microbial Genomics ◽

10.1099/mgen.0.000387 ◽

2020 ◽

Vol 6 (6) ◽

Author(s):

Ethan R. Wyrsch ◽

Piklu Roy Chowdhury ◽

Veronica M. Jarocki ◽

Kate J. Brandis ◽

Steven P. Djordjevic

Keyword(s):

Escherichia Coli ◽

North American ◽

Type Species ◽

Pathogenicity Island ◽

Duplication Event ◽

Toxin Gene ◽

Nucleotide Polymorphisms ◽

Content Type ◽

E Coli ◽

Link Type

The AB5 cytotoxins are important virulence factors in Escherichia coli . The most notable members of the AB5 toxin families include Shiga toxin families 1 (Stx1) and 2 (Stx2), which are associated with enterohaemorrhagic E. coli infections causing haemolytic uraemic syndrome and haemorrhagic colitis. The subAB toxins are the newest and least well understood members of the AB5 toxin gene family. The subtilase toxin genes are divided into a plasmid-based variant, subAB1, originally described in enterohaemorrhagic E. coli O113:H21, and distinct chromosomal variants, subAB2, that reside in pathogenicity islands encoding additional virulence effectors. Previously we identified a chromosomal subAB2 operon within an E. coli ST58 strain IBS28 (ONT:H25) taken from a wild ibis nest at an inland wetland in New South Wales, Australia. Here we show the subAB2 toxin operon comprised part of a 140 kb tRNA–Phe chromosomal island that co-hosted tia, encoding an outer-membrane protein that confers an adherence and invasion phenotype and additional virulence and accessory genetic content that potentially originated from known virulence island SE-PAI. This island shared a common evolutionary history with a secondary 90 kb tRNA–Phe pathogenicity island that was presumably generated via a duplication event. IBS28 is closely related [200 single-nucleotide polymorphisms (SNPs)] to four North American ST58 strains. The close relationship between North American isolates of ST58 and IBS28 was further supported by the identification of the only copy of a unique variant of IS26 within the O-antigen gene cluster. Strain ISB28 may be a historically important E. coli ST58 genome sequence hosting a progenitor pathogenicity island encoding subAB.

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