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Genetics and Genomics of Zoonotic Foodborne Pathogens

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A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Microbial Genetics and Genomics".

Deadline for manuscript submissions: closed (31 December 2020) | Viewed by 20190

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Special Issue Editors

Dr. Jonathan Frye

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Guest Editor

United States Department of Agriculture, Agricultural Research Service, Athens, GA 30605, USA
Interests: foodborne pathogens; antibiotic resistance; pathogenicity; genomics
Special Issues, Collections and Topics in MDPI journals

Dr. Elizabeth McMillan

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Co-Guest Editor

Bacterial Epidemiology and Antimicrobial Resistance Research Unit, Department of Microbiology and the USDA, Agricultural Research Service, The University of Georgia, Athens, GA 30605, USA
Interests: genomics; bioinformatics; plasmids and other mobile genetic elements; foodborne pathogens; antimicrobial resistance; resistance to biocides and metals; pathogenicity

Dr. Sushim Gupta

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Co-Guest Editor

Department of Biochemistry and Molecular Biology, Oklahoma State University, Stillwater, OK 74078, USA
Interests: genomics; pan-genome analysis; phylogenetics; phylogenomics; foodborne pathogens; antimicrobial resistance; bioinformatics; bioinformatics tool development

Dr. Charlene Jackson

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Co-Guest Editor

Bacterial Epidemiology and Antimicrobial Resistance Research Unit, USDA Agricultural Research Service, Athens, GA 30605, USA
Interests: Enterococcus; MRSA; Gram positive bacteria; genetics; genomics; antimicrobial resistance; Escherichia coli; plasmid biology

Special Issue Information

Dear Colleagues,

Foodborne and zoonotic pathogens are responsible for illnesses, deaths, burdens to healthcare systems, and lost productivity. Our understanding of many of these diseases and the organisms that cause them is limited. Research into the genetics of these pathogens has revealed many key features of the bacterial interactions with the host to colonize, establish an infection, replicate, and be transmitted to new hosts. However, many key features of these zoonotic bacteria are poorly understood.

The goal of this Special Issue is to better elucidate the genetic and genomic features that make zoonotic foodborne pathogens capable of survival in the animal host and able to cause infections in the human host. This issue will focus on expanding our knowledge of well-studied bacterial pathogens as well as introducing research into emerging zoonotic and foodborne pathogens.

Classic recombinant DNA techniques have been used to investigate the molecular pathogenics of these organisms and have revealed much about the transmission and disease process. In addition, these techniques have also explored the development of antimicrobial resistance in these zoonotic pathogens, which may be an additional risk factor for human illnesses. In the past twenty years, the development of whole genome sequencing (WGS) as a method to investigate these pathogens has transformed our understanding of them. Currently, this method of research has reached the point where WGS can be used to screen the genetics of these pathogens, helping us to understand the genomics behind successful zoonotic foodborne pathogens. In addition, other methods such as microarrays and RNAseq based on WGS data have been developed to understand the gene expression and regulation of the pathogen’s whole genome during the infection process, as well as other aspects necessary for its survival and transmission.

This Special Issue welcomes papers of original research using these or other methods to answer questions about the genetics and genomics of zoonotic foodborne pathogens. Papers focusing on pathogen–host interactions, phylogenetics and evolution of pathogens, genetics of host range and pathogenicity, acquisition or development of new traits such as antimicrobial resistance, and investigations into how food animal management may affect the level of risk to human health by zoonotic foodborne pathogens are welcome. Additionally, review articles are welcome which cover the current literature and present a synthesis of our current knowledge of these pathogens and the genetic processes that make them successful.

Dr. Jonathan Frye
Guest Editor

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Genes is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2600 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

zoonotic
foodborne
pathogen
genomics
transcriptomics
Salmonella
E. coli
Listeria
Campylobacter
antimicrobial resistance
virulence
pathogenicity
host range

Published Papers (6 papers)

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Research

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15 pages, 1328 KiB

Open AccessArticle

Carriage and Gene Content Variability of the pESI-Like Plasmid Associated with Salmonella Infantis Recently Established in United States Poultry Production

by Elizabeth A. McMillan, Jamie L. Wasilenko, Kaitlin A. Tagg, Jessica C. Chen, Mustafa Simmons, Sushim K. Gupta, Glenn E. Tillman, Jason Folster, Charlene R. Jackson and Jonathan G. Frye

Genes 2020, 11(12), 1516; https://doi.org/10.3390/genes11121516 - 18 Dec 2020

Cited by 25 | Viewed by 4234

Abstract

Salmonella Infantis carrying extended spectrum β-lactamase bla_CTX-M-65 on a pESI-like megaplasmid has recently emerged in United States poultry. In order to determine the carriage rate and gene content variability of this plasmid in U.S. Salmonella Infantis, whole genome sequences of Salmonella isolates from humans and animals in the U.S. and internationally containing the pESI-like plasmid were analyzed. The U.S. Department of Agriculture Food Safety and Inspection Service (FSIS) identified 654 product sampling isolates containing pESI-like plasmids through hazard analysis and critical control point (HACCP) verification testing in 2017 and 2018. The Centers for Disease Control and Prevention identified 55 isolates with pESI-like plasmids in 2016–2018 through the National Antimicrobial Resistance Monitoring System. Approximately 49% of pESI-like plasmids from FSIS verification isolates and 71% from CDC NARMS contained bla_CTX-M-65. Pan-plasmid genome analysis was also performed. All plasmids contained traN and more than 95% contained 172 other conserved genes; 61% contained bla_CTX-M-65. In a hierarchical clustering analysis, some plasmids from U.S. animal sources clustered together and some plasmids from South America clustered together, possibly indicating multiple plasmid lineages. However, most plasmids contained similar genes regardless of origin. Carriage of the pESI-like plasmid in U.S. appears to be limited to Salmonella Infantis and carriage rates increased from 2017 to 2018. Full article

(This article belongs to the Special Issue Genetics and Genomics of Zoonotic Foodborne Pathogens)

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17 pages, 2573 KiB

Open AccessArticle

Genomic Investigation into the Virulome, Pathogenicity, Stress Response Factors, Clonal Lineages, and Phylogenetic Relationship of Escherichia coli Strains Isolated from Meat Sources in Ghana

by Frederick Adzitey, Jonathan Asante, Hezekiel M. Kumalo, Rene B. Khan, Anou M. Somboro and Daniel G. Amoako

Genes 2020, 11(12), 1504; https://doi.org/10.3390/genes11121504 - 14 Dec 2020

Cited by 8 | Viewed by 2273

Abstract

Escherichia coli are among the most common foodborne pathogens associated with infections reported from meat sources. This study investigated the virulome, pathogenicity, stress response factors, clonal lineages, and the phylogenomic relationship of E. coli isolated from different meat sources in Ghana using whole-genome sequencing. Isolates were screened from five meat sources (beef, chevon, guinea fowl, local chicken, and mutton) and five areas (Aboabo, Central market, Nyorni, Victory cinema, and Tishegu) based in the Tamale Metropolis, Ghana. Following microbial identification, the E. coli strains were subjected to whole-genome sequencing. Comparative visualisation analyses showed different DNA synteny of the strains. The isolates consisted of diverse sequence types (STs) with the most common being ST155 (n = 3/14). Based Upon Related Sequence Types (eBURST) analyses of the study sequence types identified four similar clones, five single-locus variants, and two satellite clones (more distantly) with global curated E. coli STs. All the isolates possessed at least one restriction-modification (R-M) and CRISPR defence system. Further analysis revealed conserved stress response mechanisms (detoxification, osmotic, oxidative, and periplasmic stress) in the strains. Estimation of pathogenicity predicted a higher average probability score (P_score ≈ 0.937), supporting their pathogenic potential to humans. Diverse virulence genes that were clonal-specific were identified. Phylogenomic tree analyses coupled with metadata insights depicted the high genetic diversity of the E. coli isolates with no correlation with their meat sources and areas. The findings of this bioinformatic analyses further our understanding of E. coli in meat sources and are broadly relevant to the design of contamination control strategies in meat retail settings in Ghana. Full article

(This article belongs to the Special Issue Genetics and Genomics of Zoonotic Foodborne Pathogens)

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26 pages, 2935 KiB

Open AccessArticle

Genotypic and Phenotypic Characterization of Incompatibility Group FIB Positive Salmonella enterica Serovar Typhimurium Isolates from Food Animal Sources

by Nesreen H. Aljahdali, Bijay K. Khajanchi, Kennedi Weston, Joanna Deck, Justin Cox, Ruby Singh, Jeffrey Gilbert, Yasser M. Sanad, Jing Han, Rajesh Nayak and Steven L. Foley

Genes 2020, 11(11), 1307; https://doi.org/10.3390/genes11111307 - 04 Nov 2020

Cited by 9 | Viewed by 3271

Abstract

Salmonella enterica is one of the most common bacterial foodborne pathogens in the United States, causing illnesses that range from self-limiting gastroenteritis to more severe, life threatening invasive disease. Many Salmonella strains contain plasmids that carry virulence, antimicrobial resistance, and/or transfer genes which allow them to adapt to diverse environments, and these can include incompatibility group (Inc) FIB plasmids. This study was undertaken to evaluate the genomic and phenotypic characteristics of IncFIB-positive Salmonella enterica serovar Typhimurium isolates from food animal sources, to identify their plasmid content, assess antimicrobial resistance and virulence properties, and compare their genotypic isolates with more recently isolated S. Typhimurium isolates from food animal sources. Methods: We identified 71 S. Typhimurium isolates that carried IncFIB plasmids. These isolates were subjected to whole genome sequencing and evaluated for bacteriocin production, antimicrobial susceptibility, the ability to transfer resistance plasmids, and a subset was evaluated for their ability to invade and persist in intestinal human epithelial cells. Results: Approximately 30% of isolates (n = 21) displayed bacteriocin inhibition of Escherichia coli strain J53. Bioinformatic analyses using PlasmidFinder software confirmed that all isolates contained IncFIB plasmids along with multiple other plasmid replicon types. Comparative analyses showed that all strains carried multiple antimicrobial resistance genes and virulence factors including iron acquisition genes, such as iucABCD (75%), iutA (94%), sitABCD (76%) and sitAB (100%). In 17 cases (71%), IncFIB plasmids, along with other plasmid replicon types, were able to conjugally transfer antimicrobial resistance and virulence genes to the susceptible recipient strain. For ten strains, persistence cell counts (27%) were noted to be significantly higher than invasion bacterial cell counts. When the genome sequences of the study isolates collected from 1998–2003 were compared to those published from subsequent years (2005–2018), overlapping genotypes were found, indicating the perseverance of IncFIB positive strains in food animal populations. This study confirms that IncFIB plasmids can play a potential role in disseminating antimicrobial resistance and virulence genes amongst bacteria from several food animal species. Full article

(This article belongs to the Special Issue Genetics and Genomics of Zoonotic Foodborne Pathogens)

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19 pages, 2359 KiB

Open AccessArticle

The Role of Salmonella Genomic Island 4 in Metal Tolerance of Salmonella enterica Serovar I 4,[5],12:i:- Pork Outbreak Isolate USDA15WA-1

by Bradley L. Bearson, Julian M. Trachsel, Daniel C. Shippy, Sathesh K. Sivasankaran, Brian J. Kerr, Crystal L. Loving, Brian W. Brunelle, Shelby M. Curry, Nicholas K. Gabler and Shawn M. D. Bearson

Genes 2020, 11(11), 1291; https://doi.org/10.3390/genes11111291 - 30 Oct 2020

Cited by 12 | Viewed by 2821

Abstract

Multidrug-resistant (MDR; resistance to >3 antimicrobial classes) Salmonella enterica serovar I 4,[5],12:i:- strains were linked to a 2015 foodborne outbreak from pork. Strain USDA15WA-1, associated with the outbreak, harbors an MDR module and the metal tolerance element Salmonella Genomic Island 4 (SGI-4). Characterization of SGI-4 revealed that conjugational transfer of SGI-4 resulted in the mobile genetic element (MGE) replicating as a plasmid or integrating into the chromosome. Tolerance to copper, arsenic, and antimony compounds was increased in Salmonella strains containing SGI-4 compared to strains lacking the MGE. Following Salmonella exposure to copper, RNA-seq transcriptional analysis demonstrated significant differential expression of diverse genes and pathways, including induction of at least 38 metal tolerance genes (copper, arsenic, silver, and mercury). Evaluation of swine administered elevated concentrations of zinc oxide (2000 mg/kg) and copper sulfate (200 mg/kg) as an antimicrobial feed additive (Zn+Cu) in their diet for four weeks prior to and three weeks post-inoculation with serovar I 4,[5],12:i:- indicated that Salmonella shedding levels declined at a slower rate in pigs receiving in-feed Zn+Cu compared to control pigs (no Zn+Cu). The presence of metal tolerance genes in MDR Salmonella serovar I 4,[5],12:i:- may provide benefits for environmental survival or swine colonization in metal-containing settings. Full article

(This article belongs to the Special Issue Genetics and Genomics of Zoonotic Foodborne Pathogens)

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16 pages, 1225 KiB

Open AccessArticle

Comparative Genomic Analysis of 450 Strains of Salmonella enterica Isolated from Diseased Animals

by Shaohua Zhao, Cong Li, Chih-Hao Hsu, Gregory H. Tyson, Errol Strain, Heather Tate, Thu-Thuy Tran, Jason Abbott and Patrick F. McDermott

Genes 2020, 11(9), 1025; https://doi.org/10.3390/genes11091025 - 01 Sep 2020

Cited by 29 | Viewed by 4283

Abstract

Salmonella is a leading cause of bacterial infections in animals and humans. We sequenced a collection of 450 Salmonella strains from diseased animals to better understand the genetic makeup of their virulence and resistance features. The presence of Salmonella pathogenicity islands (SPIs) varied by serotype. S. Enteritidis carried the most SPIs (n = 15), while S. Mbandaka, S. Cerro, S. Meleagridis, and S. Havana carried the least (n = 10). S. Typhimurium, S. Choleraesuis, S. I 4,5,12:i:-, and S. Enteritidis each contained the spv operon on IncFII or IncFII-IncFIB hybrid plasmids. Two S. IIIa carried a spv operon with spvD deletion on the chromosome. Twelve plasmid types including 24 hybrid plasmids were identified. IncA/C was frequently associated with S. Newport (83%) and S. Agona (100%) from bovine, whereas IncFII (100%), IncFIB (100%), and IncQ1 (94%) were seen in S. Choleraesuis from swine. IncX (100%) was detected in all S. Kentucky from chicken. A total of 60 antimicrobial resistance genes (ARGs), four disinfectant resistances genes (DRGs) and 33 heavy metal resistance genes (HMRGs) were identified. The Salmonella strains from sick animals contained various SPIs, resistance genes and plasmid types based on the serotype and source of the isolates. Such complicated genomic structures shed light on the strain characteristics contributing to the severity of disease and treatment failures in Salmonella infections, including those causing illnesses in animals. Full article

(This article belongs to the Special Issue Genetics and Genomics of Zoonotic Foodborne Pathogens)

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Review

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13 pages, 1257 KiB

Open AccessReview

Salmonella enterica’s “Choice”: Itaconic Acid Degradation or Bacteriocin Immunity Genes

by Rolf D. Joerger

Genes 2020, 11(7), 797; https://doi.org/10.3390/genes11070797 - 15 Jul 2020

Cited by 2 | Viewed by 2670

Abstract

Itaconic acid is an immunoregulatory metabolite produced by macrophages in response to pathogen invasion. It also exhibits antibacterial activity because it is an uncompetitive inhibitor of isocitrate lyase, whose activity is required for the glyoxylate shunt to be operational. Some bacteria, such as Yersinia pestis, encode enzymes that can degrade itaconic acid and therefore eliminate this metabolic inhibitor. Studies, primarily with Salmonella enterica subspecies enterica serovar Typhimurium, have demonstrated the presence of similar genes in this pathogen and the importance of these genes for the persistence of the pathogen in murine hosts. This minireview demonstrates that, based on Blast searches of 1063 complete Salmonella genome sequences, not all Salmonella serovars possess these genes. It is also shown that the growth of Salmonella isolates that do not possess these genes is sensitive to the acid under glucose-limiting conditions. Interestingly, most of the serovars without the three genes, including serovar Typhi, harbor DNA at the corresponding genomic location that encodes two open reading frames that are similar to bacteriocin immunity genes. It is hypothesized that these genes could be important for Salmonella that finds itself in strong competition with other Enterobacteriacea in the intestinal tract—for example, during inflammation. Full article

(This article belongs to the Special Issue Genetics and Genomics of Zoonotic Foodborne Pathogens)

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