Jason P. Folster

Centers for Disease Control and Prevention

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Jean M. Whichard

Centers for Disease Control and Prevention

Louise Francois Watkins

Centers for Disease Control and Prevention

Kaitlin A. Tagg

Waterborne Environmental (United States)

Shaohua Zhao

Center for Veterinary Medicine

Patrick F. McDermott

Center for Veterinary Medicine

Jessica C. Chen

National Center for Emerging and Zoonotic Infectious Diseases

Cindy R. Friedman

Centers for Disease Control and Prevention

Gary Pecic

Centers for Disease Control and Prevention

Regan Rickert

Organisation internationale de police criminelle

Beth Tolar

National Center for Emerging and Zoonotic Infectious Diseases

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Centers for Disease Control and Prevention

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National Center for Emerging and Zoonotic Infectious Diseases

126

Waterborne Environmental (United States)

United States Food and Drug Administration

Public Health Agency of Canada

United States Department of Agriculture

Oak Ridge Associated Universities

Minnesota Department of Health

Oak Ridge Institute for Science and Education

Epidemic Intelligence Service

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Characterization of bla_CMY-Encoding Plasmids Among Salmonella Isolated in the United States in 2007

Foodborne Pathogens and Disease (2011)

Jason P. Folster Gary Pecic Andre McCullough Regan Rickert Jean M. Whichard

Salmonella enterica is one of the most common bacterial causes of foodborne illness, and nontyphoidal Salmonella is estimated to cause ∼1.2 million illnesses in the United States each year. Plasmids are mobile genetic elements that play a critical role in the dissemination of antimicrobial resistance determinants. AmpC-type CMY β-lactamases (blaCMY) confer resistance to extended-spectrum cephalosporins and β-lactam/β-lactamase inhibitor combinations and are commonly plasmid-encoded. A variety of plasmids have been shown to encode CMY β-lactamases and certain plasmids may be associated with particular Salmonella serotypes or environmental sources. In this study, we characterized blaCMY β-lactamase-encoding plasmids among Salmonella isolates. Isolates of Salmonella from specimens collected from humans in 2007 were submitted to the Centers for Disease Control and Prevention National Antimicrobial Resistance Monitoring System laboratory for susceptibility testing. Three percent (65/2161) of Salmonella isolates displayed resistance to ceftriaxone (minimum inhibitory concentration [MIC] ≥4 mg/L) and amoxicillin/clavulanic acid (MIC ≥32 mg/L), a combination associated with the presence of a blaCMY mechanism of resistance. Sixty-four (98.5%) isolates were polymerase chain reaction-positive for blaCMY genes. Transformation and conjugation studies showed that 95% (61/64) of the blaCMY genes were plasmid-encoded. Most of the blaCMY-positive isolates were serotype Typhimurium, Newport, Heidelberg, and Agona. Forty-three plasmids were replicon type IncA/C, 15 IncI1, 2 contained multiple replicon loci, and 1 was untypeable. IncI1 plasmids conferred only the blaCMY-associated resistance phenotype, whereas IncA/C plasmids conferred additional multi-drug resistance (MDR) phenotypes to drugs such as chloramphenicol, sulfisoxazole, and tetracycline. Most of the IncI1 plasmids (12/15) were sequence type 12 by plasmid multi-locus sequence typing. CMY β-lactamase-encoding plasmids among human isolates of Salmonella in the United States tended to be large MDR IncA/C plasmids or single resistance determinant IncI1 plasmids. In general, IncI1 plasmids were identified among serotypes commonly associated with poultry, whereas IncA/C plasmids were more likely to be identified among cattle/beef-associated serotypes.

Replicon

Salmonella enterica

10.1089/fpd.2011.0944

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Citations (55)

Comparison of Molecular Subtyping and Antimicrobial Resistance Detection Methods Used in a Large Multistate Outbreak of Extensively Drug-Resistant Campylobacter jejuni Infections Linked to Pet Store Puppies

Journal of Clinical Microbiology (2020)

Lavin A. Joseph Louise Francois Watkins Jessica Chen Kaitlin A. Tagg Christy Bennett

is a leading cause of enteric bacterial illness in the United States. Traditional molecular subtyping methods, such as pulsed-field gel electrophoresis (PFGE) and 7-gene multilocus sequence typing (MLST), provided limited resolution to adequately identify

Multilocus sequence typing

Subtyping

Molecular Epidemiology

10.1128/jcm.00771-20

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Citations (16)

FarRRegulates thefarAB-Encoded Efflux Pump ofNeisseriagonorrhoeaevia an MtrR RegulatoryMechanism

Journal of Bacteriology (2003)

E.-H. Lee Corinne E. Rouquette-Loughlin Jason P. Folster William M. Shafer

ABSTRACT The farAB operon of Neisseria gonorrhoeae encodes an efflux pump which mediates gonococcal resistance to antibacterial fatty acids. It was previously observed that expression of the farAB operon was positively regulated by MtrR, which is a repressor of the mtrCDE -encoded efflux pump system (E.-H. Lee and W. M. Shafer, Mol. Microbiol. 33:839-845, 1999). This regulation was believed to be indirect since MtrR did not bind to the farAB promoter. In this study, computer analysis of the gonococcal genome sequence database, lacZ reporter fusions, and gel mobility shift assays were used to elucidate the regulatory mechanism by which expression of the farAB operon is modulated by MtrR in gonococci. We identified a regulatory protein belonging to the MarR family of transcriptional repressors and found that it negatively controls expression of farAB by directly binding to the farAB promoter. We designated this regulator FarR to signify its role in regulating the farAB operon. We found that MtrR binds to the farR promoter, thereby repressing farR expression. Hence, MtrR regulates farAB in a positive fashion by modulating farR expression. This MtrR regulatory cascade seems to play an important role in adjusting levels of the FarAB and MtrCDE efflux pumps to prevent their excess expression in gonococci.

MTRR

Efflux

Neisseria gonorrhoeae

10.1128/jb.185.24.7145-7152.2003

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Citations (79)

Characterization of Isolates from an Outbreak of Multidrug-Resistant, Shiga Toxin-Producing Escherichia coli O145 in the United States

Antimicrobial Agents and Chemotherapy (2011)

Jason P. Folster Gary Pecic Ethel Taylor Jean M. Whichard

Characterization of Isolates from an Outbreak of Multidrug-Resistant, ShigaToxin-Producing Escherichia coli O145 in the United States ᰔ Shiga toxin-producing Escherichia coli (STEC) is an important cause of food-borne illness, and several outbreaks of non-O157 serotype infections have been reported recently (10,17).In 2010, a multistate outbreak of STEC O145:NM (nonmotile) infections was investigated and linked to shredded romaine lettuce (4).Twenty-six confirmed and five probable cases were reported from Michigan, New York, Ohio, Pennsylvania, and Tennessee.Eleven (35%) patients required hospitalization, and three (10%) developed hemolytic uremic syndrome (HUS).No deaths were reported.Although antimicrobial treatment for STEC infections is not recommended, some patients receive antimicrobial treatment prior to the diagnosis, and identification of antimicrobial resistance may provide clues about potential sources of these infections (13,14).Therefore, understanding antimicrobial resistance patterns among STEC isolates remains important.Three representative outbreak isolates from ill patients were sent to the National Antimicrobial Resistance Monitoring System (NARMS) at the CDC for antimicrobial susceptibility testing (AST).MICs to 15 antimicrobial drugs were determined by broth microdilution (Sensititre; Trek Diagnostics, Westlake, OH).All three isolates displayed resistance to chloramphenicol, nalidixic acid, streptomycin, sulfisoxazole, and tetracycline and decreased susceptibility to ciprofloxacin (MIC ϭ 0.25 g/ml) (Table 1).Cell lysates were screened for antimicrobial resistance genes by PCR (7).All three isolates contained the floR, strA, strB, sul2, and tetA resistance genes.Sequence analysis confirmed that the gene content and orientation matched those of the floR accessory gene element found in some IncA/C plasmids

10.1128/aac.05545-11

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Citations (17)

Whole-Genome Sequencing for Detecting Antimicrobial Resistance in Nontyphoidal Salmonella

Antimicrobial Agents and Chemotherapy (2016)

Patrick F. McDermott Gregory H. Tyson Claudine Kabera Yuansha Chen Cong Li

Laboratory-based in vitro antimicrobial susceptibility testing is the foundation for guiding anti-infective therapy and monitoring antimicrobial resistance trends. We used whole-genome sequencing (WGS) technology to identify known antimicrobial resistance determinants among strains of nontyphoidal Salmonella and correlated these with susceptibility phenotypes to evaluate the utility of WGS for antimicrobial resistance surveillance. Six hundred forty Salmonella of 43 different serotypes were selected from among retail meat and human clinical isolates that were tested for susceptibility to 14 antimicrobials using broth microdilution. The MIC for each drug was used to categorize isolates as susceptible or resistant based on Clinical and Laboratory Standards Institute clinical breakpoints or National Antimicrobial Resistance Monitoring System (NARMS) consensus interpretive criteria. Each isolate was subjected to whole-genome shotgun sequencing, and resistance genes were identified from assembled sequences. A total of 65 unique resistance genes, plus mutations in two structural resistance loci, were identified. There were more unique resistance genes (n = 59) in the 104 human isolates than in the 536 retail meat isolates (n = 36). Overall, resistance genotypes and phenotypes correlated in 99.0% of cases. Correlations approached 100% for most classes of antibiotics but were lower for aminoglycosides and beta-lactams. We report the first finding of extended-spectrum β-lactamases (ESBLs) (blaCTX-M1 and blaSHV2a) in retail meat isolates of Salmonella in the United States. Whole-genome sequencing is an effective tool for predicting antibiotic resistance in nontyphoidal Salmonella, although the use of more appropriate surveillance breakpoints and increased knowledge of new resistance alleles will further improve correlations.

Broth microdilution

10.1128/aac.01030-16

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Citations (346)

CTX-M-65 Extended-Spectrum β-Lactamase–Producing Salmonella enterica Serotype Infantis, United States1

Emerging infectious diseases (2018)

Allison C. Brown Jessica C. Chen Louise Francois Watkins Davina Campbell Jason P. Folster

Extended-spectrum β-lactamases (ESBLs) confer resistance to clinically important third-generation cephalosporins, which are often used to treat invasive salmonellosis. In the United States, ESBLs are rarely found in Salmonella. However, in 2014, the US Food and Drug Administration found bla

Salmonella enterica

Broth microdilution

10.3201/eid2412.180500

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Citations (91)

Genomic Comparison of Escherichia coli O104:H4 Isolates from 2009 and 2011 Reveals Plasmid, and Prophage Heterogeneity, Including Shiga Toxin Encoding Phage stx2

PLoS ONE (2012)

Sanaa Ahmed Joy Awosika Carson Baldwin Kimberly A. Bishop‐Lilly Biswajit Biswas

In May of 2011, an enteroaggregative Escherichia coli O104:H4 strain that had acquired a Shiga toxin 2-converting phage caused a large outbreak of bloody diarrhea in Europe which was notable for its high prevalence of hemolytic uremic syndrome cases. Several studies have described the genomic inventory and phylogenies of strains associated with the outbreak and a collection of historical E. coli O104:H4 isolates using draft genome assemblies. We present the complete, closed genome sequences of an isolate from the 2011 outbreak (2011C-3493) and two isolates from cases of bloody diarrhea that occurred in the Republic of Georgia in 2009 (2009EL-2050 and 2009EL-2071). Comparative genome analysis indicates that, while the Georgian strains are the nearest neighbors to the 2011 outbreak isolates sequenced to date, structural and nucleotide-level differences are evident in the Stx2 phage genomes, the mer/tet antibiotic resistance island, and in the prophage and plasmid profiles of the strains, including a previously undescribed plasmid with homology to the pMT virulence plasmid of Yersinia pestis. In addition, multiphenotype analysis showed that 2009EL-2071 possessed higher resistance to polymyxin and membrane-disrupting agents. Finally, we show evidence by electron microscopy of the presence of a common phage morphotype among the European and Georgian strains and a second phage morphotype among the Georgian strains. The presence of at least two stx2 phage genotypes in host genetic backgrounds that may derive from a recent common ancestor of the 2011 outbreak isolates indicates that the emergence of stx2 phage-containing E. coli O104:H4 strains probably occurred more than once, or that the current outbreak isolates may be the result of a recent transfer of a new stx2 phage element into a pre-existing stx2-positive genetic background.

Prophage

Phage therapy

10.1371/journal.pone.0048228

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Citations (120)

MtrR Modulates rpoH Expression and Levels of Antimicrobial Resistance in Neisseria gonorrhoeae

Journal of Bacteriology (2008)

Jason P. Folster Paul J. Johnson Lydgia Jackson Vijaya Dhulipali David W. Dyer

The MtrR transcriptional-regulatory protein is known to repress transcription of the mtrCDE operon, which encodes a multidrug efflux pump possessed by Neisseria gonorrhoeae that is important in the ability of gonococci to resist certain hydrophobic antibiotics, detergents, dyes, and host-derived antimicrobials. In order to determine whether MtrR can exert regulatory action on other gonococcal genes, we performed a whole-genome microarray analysis using total RNA extracted from actively growing broth cultures of isogenic MtrR-positive and MtrR-negative gonococci. We determined that, at a minimum, 69 genes are directly or indirectly subject to MtrR control, with 47 being MtrR repressed and 22 being MtrR activated. rpoH, which encodes the general stress response sigma factor RpoH (sigma 32), was found by DNA-binding studies to be directly repressed by MtrR, as it was found to bind to a DNA sequence upstream of rpoH that included sites within the rpoH promoter. MtrR also repressed the expression of certain RpoH-regulated genes, but this regulation was likely indirect and a reflection of MtrR control of rpoH expression. Inducible expression of MtrR was found to repress rpoH expression and to increase gonococcal susceptibility to hydrogen peroxide (H(2)O(2)) and an antibiotic (erythromycin) recognized by the MtrC-MtrD-MtrE efflux pump system. We propose that, apart from its ability to control the expression of the mtrCDE-encoded efflux pump operon and, as a consequence, levels of gonococcal resistance to host antimicrobials (e.g., antimicrobial peptides) recognized by the efflux pump, the ability of MtrR to regulate the expression levels of rpoH and RpoH-regulated genes also modulates levels of gonococcal susceptibility to H(2)O(2).

MTRR

Neisseria gonorrhoeae

Sigma factor

Efflux

Regulon

10.1128/jb.01165-08

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Citations (61)

Genome Sequences from a Reemergence of Vibrio cholerae in Haiti, 2022 Reveal Relatedness to Previously Circulating Strains

Journal of Clinical Microbiology (2023)

Cynney Walters Jessica Chen Steven Stroika Lee S. Katz Maryann Turnsek

After more than 3 years without a documented cholera case, the Republic of Haiti reported its first resurgent case on 30 September 2022 (1–3). As of 18 February 2023, more than 27,000 cholera cases have been hospitalized and 594 deaths confirmed from all 10 departments (4). Here, we describe Vibrio cholerae isolates first characterized by the Laboratoire National de Santé Publique (LNSP) and include both genotypic and phenotypic antimicrobial resistance profiles. Whole-genome sequencing (WGS) analysis was compared with recently circulating cholera toxin-producing V. cholerae O1 in a maximum likelihood phylogeny.

Cholera

10.1128/jcm.00142-23

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Citations (1)

Mobile genetic elements define the non-random structure of the Salmonella enterica serovar Typhi pangenome

mSystems (2024)

Arancha Peñil-Celis Kaitlin A. Tagg Hattie E. Webb Santiago Redondo Louise Francois Watkins

Bacterial relatedness measured using select chromosomal loci forms the basis of public health genomic surveillance. While approximating vertical evolution through this approach has proven exceptionally valuable for understanding pathogen dynamics, it excludes a fundamental dimension of bacterial evolution-horizontal gene transfer. Incorporating the accessory genome is the logical remediation and has recently shown promise in expanding epidemiological resolution for enteric pathogens. Employing

Horizontal Gene Transfer

Salmonella enterica

Opportunistic pathogen

10.1128/msystems.00365-24

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Citations (2)