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Genetics and Genomics of 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 (30 March 2018) | Viewed by 85114

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Special Issue Editors

Dr. Kieran Jordan

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Guest Editor

Food Safety Department, Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, Ireland
Interests: Listeria monocytogenes; Escherichia coli; food safety microbiology; mycobacterium paratuberculosis; milk quality; dairy food safety

Dr. Avelino Álvarez-Ordoñez

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Guest Editor

Department of Food Hygiene and Technology and Institute of Food Science and Technology, University of León, León, Spain
Interests: food safety; foodborne pathogens; bacterial physiology; bacterial stress responses; ecology and biocontrol of microbial biofilms; antimicrobial resistance; food microbiome; novel technologies of food preservation
Special Issues, Collections and Topics in MDPI journals

Dr. Olivia McAuliffe

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Guest Editor

Food Biosciences Department, Teagasc Food Research Centre, Moorepark, Fermoy, Co. Cork, P61 C996, Ireland
Interests: whole genome sequencing of foodborne pathogens and their bacteriophages, biocontrol and detection of foodborne pathogens with bacteriophages

Special Issue Information

Dear Colleagues,

Foodborne pathogens are a public health threat and their control is a challenge to the food industry. The occurrence and transcription of genes, which encode specialised functions, plays a vital role in survival of pathogens, growth under harsh conditions and in food, their ability to produce toxins and in virulence, pathogenicity and antimicrobial resistance. Controlling the expression of such genes can result in limiting the ability of pathogens to cause disease. Whole genome sequencing technologies are revolutionising epidemiology of foodborne pathogens and tracing of foodborne pathogens in food and the food processing environment. An increasing amount of information on genes, genomes and transcriptomes of foodborne pathogens is becoming available, which will lead to a greater understanding of survival and virulence of pathogens.

This Special Issue welcomes submissions on issues relating to the genetics and genomics of foodborne pathogens, including on topics such as persistence, virulence, gene detection, whole genome sequencing, transcriptomics, and characterisation of genes involved in toxin production, antimicrobial resistance and virulence, among others.

All contributions to this Special Issue must be in line with the scope of the journal. Manuscripts discovered, during any stage of peer review process, to be outside of the scope may be transferred to a suitable section or field, or withdrawn from review.

Dr. Kieran Jordan
Dr. Olivia McAuliffe
Dr. Avelino Alvarez-Ordonez
Guest Editors

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Keywords

Bacterial virulence
Pathogenicity
Whole genome sequencing
Transcriptomics
Toxin production
Antimicrobial resistance

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Published Papers (13 papers)

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Research

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19 pages, 3298 KiB

Open AccessArticle

Listeria monocytogenes Isolated from Illegally Imported Food Products into the European Union Harbor Different Virulence Factor Variants

by Kathrin Rychli, Beatrix Stessl, Kati Szakmary-Brändle, Anja Strauß, Martin Wagner and Dagmar Schoder

Genes 2018, 9(9), 428; https://doi.org/10.3390/genes9090428 - 23 Aug 2018

Cited by 15 | Viewed by 4459

Abstract

Unregulated international flow of foods poses a danger to human health, as it may be contaminated with pathogens. Recent studies have investigated neglected routes of pathogen transmission and reported the occurrence of Listeria monocytogenes in food illegally imported into the European Union (EU), either confiscated at four international airports or sold illegally on the Romanian black market. In this study we investigated the genotype diversity and the amino acid sequence variability of three main virulence factors of 57 L. monocytogenes isolates. These isolates were derived from 1474 food samples illegally imported into the EU and originated from 17 different countries. Multilocus sequence typing revealed 16 different sequence types (STs) indicating moderate genotype diversity. The most prevalent STs were ST2, ST9, and ST121. The pulsed-field gel electrophoresis (PFGE) analysis resulted in 34 unique pulsotypes. PFGE types assigned to the most prevalent STs (ST2, ST9, and ST121) were highly related in their genetic fingerprint. Internalin A (InlA) was present in 20 variants, including six truncated InlA variants, all harbored by isolates of ST9 and ST121. We detected eight ST-specific listeriolysin O (LLO) variants, and among them, one truncated form. The actin-assembly-inducing protein ActA was present in 15 different ST-specific variants, including four ActA variants with an internal truncation. In conclusion, this study shows that L. monocytogenes, isolated from illegally imported food, have moderate genotype diversity, but diverse virulence factors variants, mainly of InlA. Full article

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

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12 pages, 838 KiB

Open AccessArticle

Genomic Diversity of Listeria monocytogenes Isolated from Clinical and Non-Clinical Samples in Chile

by Viviana Toledo, Henk C. Den Bakker, Juan Carlos Hormazábal, Gerardo González-Rocha, Helia Bello-Toledo, Magaly Toro and Andrea I. Moreno-Switt

Genes 2018, 9(8), 396; https://doi.org/10.3390/genes9080396 - 2 Aug 2018

Cited by 28 | Viewed by 4981

Abstract

Listeria monocytogenes is the causative agent of listeriosis, which is an uncommon but severe infection associated with high mortality rates in humans especially in high-risk groups. This bacterium survives a variety of stress conditions (e.g., high osmolality, low pH), which allows it to colonize different niches especially niches found in food processing environments. Additionally, a considerable heterogeneity in pathogenic potential has been observed in different strains. In this study, 38 isolates of L. monocytogenes collected in Chile from clinical samples (n = 22) and non-clinical samples (n = 16) were analyzed using whole genome sequencing (WGS) to determine their genomic diversity. A core genome Single Nucleotide Polymorphism (SNP) tree using 55 additional L. monocytogenes accessions classified the Chilean isolates in lineages I (n = 25) and II (n = 13). In silico, Multi-locus sequence typing (MLST) differentiated the isolates into 13 sequence types (ST) in which the most common were ST1 (15 isolates) and ST9 (6 isolates) and represented 55% of the isolates. Genomic elements associated with virulence (i.e., LIPI-1, LIPI-3, inlA, inlB, inlC, inlG, inlH, inlD, inlE, inlK, inlF, and inlJ) and stress survival (i.e., stress survival islet 1 and stress survival islet 2) were unevenly distributed among clinical and non-clinical isolates. In addition, one novel inlA premature stop codon (PMSC) was detected. Comparative analysis of L. monocytogenes circulating in Chile revealed the presence of globally distributed sequence types along with differences among the isolates analyzed at a genomic level specifically associated with virulence and stress survival. Full article

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

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13 pages, 508 KiB

Open AccessArticle

Characterization of Antimicrobial Resistance Determinants and Class 1 and Class 2 Integrons in Salmonella enterica spp., Multidrug-Resistant Isolates from Pigs

by Héctor Argüello, Beatriz Guerra, Irene Rodríguez, Pedro Rubio and Ana Carvajal

Genes 2018, 9(5), 256; https://doi.org/10.3390/genes9050256 - 16 May 2018

Cited by 24 | Viewed by 4787

Abstract

Antimicrobial resistance (AMR) and Salmonella spp., are primary concerns in public health. The present study characterizes the AMR determinants of 62 multi-drug resistant (MDR) Salmonella enterica spp., isolates from swine, which were obtained between 2004–2006, a major source of human salmonellosis. The AMR determinants were investigated by PCR, checking the presence of class 1 and class 2 integrons and 29 resistance genes. Genes sul1, blaTEM1-like, aadA2, tet(A), and dfrA12 were more prevalent (p < 0.05) within the determinants that were checked for each of these antimicrobials. Co-existence of different genes conferring resistance to the same antimicrobial was common. No differences in AMR determinants prevalence were observed between Salmonella Typhimurium and other serovars from the study. Class 1 integrons were detected in 48 of 62 isolates, again with no differences being linked to any serovar. Nine different variable regions were observed, 1000 bp/aadA2-1200 bp/blaPSE-1 (13 isolates) and blaOXA-like/aadA1 (eight isolates) were the most common. Four isolates, including S. Typhimurium (2), Salmonella Bredeney (1), and Salmonella Kapemba (1) harboured a class 2 integron 2300 bp estX-sat2-aadA1. Results from the study highlight the importance of class 1 integrons and certain genes in MDR swine Salmonella isolates. The information is of relevance for monitoring in the forthcoming scope of reduction of antibiotic usage in swine production. Full article

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

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16 pages, 2153 KiB

Open AccessArticle

Genomic Characterization of Listeria monocytogenes Isolates Associated with Clinical Listeriosis and the Food Production Environment in Ireland

by Amber Hilliard, Dara Leong, Amy O’Callaghan, Eamonn P. Culligan, Ciara A. Morgan, Niall DeLappe, Colin Hill, Kieran Jordan, Martin Cormican and Cormac G.M. Gahan

Genes 2018, 9(3), 171; https://doi.org/10.3390/genes9030171 - 20 Mar 2018

Cited by 63 | Viewed by 6244

Abstract

Listeria monocytogenes is a major human foodborne pathogen that is prevalent in the natural environment and has a high case fatality rate. Whole genome sequencing (WGS) analysis has emerged as a valuable methodology for the classification of L. monocytogenes isolates and the identification of virulence islands that may influence infectivity. In this study, WGS was used to provide an insight into 25 L. monocytogenes isolates from cases of clinical infection in Ireland between 2013 and 2015. Clinical strains were either lineage I (14 isolates) or lineage II (11 isolates), with 12 clonal complexes (CC) represented, of which CC1 (6) and CC101 (4) were the most common. Single nucleotide polymorphism (SNP) analysis demonstrated that clinical isolates from mother–infant pairs (one isolate from the mother and one from the infant) were highly related (3 SNP differences in each) and also identified close similarities between isolates from otherwise distinct cases (1 SNP difference). Clinical strains were positive for common virulence-associated loci and 13 isolates harbour the LIPI-3 locus. Pulsed-field gel electrophoresis (PFGE) was used to compare strains to a database of 1300 Irish food and food processing environment isolates and determined that 64% of clinical pulsotypes were previously encountered in the food or food processing environment. Five of the matching food and food processing environment isolates were sequenced and results demonstrated a correlation between pulsotype and genotype. Overall, the work provides insights into the nature of L. monocytogenes strains currently causing clinical disease in Ireland and indicates that similar isolates can be found in the food or food processing environment. Full article

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

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11 pages, 910 KiB

Open AccessCommunication

Antibiotic Resistance Genetic Markers and Integrons in White Soft Cheese: Aspects of Clinical Resistome and Potentiality of Horizontal Gene Transfer

by Ana Caroline L. De Paula, Julliane D. Medeiros, Analice C. De Azevedo, Jéssica M. De Assis Chagas, Vânia L. Da Silva and Cláudio G. Diniz

Genes 2018, 9(2), 106; https://doi.org/10.3390/genes9020106 - 19 Feb 2018

Cited by 15 | Viewed by 5992

Abstract

Antibiotic resistance poses an important threat to global public health and has become a challenge to modern medicine. The occurrence of antibiotic-resistant bacteria in a broad range of foods has led to a growing concern about the impact that food may have as a reservoir of antibiotic resistance genes. Considering Minas Frescal Cheese (MFC)—a typical Brazilian white soft cheese—and its economic and cultural values, in this study, medically relevant antimicrobial-resistance genetic markers (AR genes) were screened, and the occurrence of integrons were evaluated in manufactured MFC using culture-independent approaches. Through a fingerprinting analysis, the tested MFCs were brand-clustered, indicating reproducibility along the production chain. A common core of resistance markers in all brands evaluated and related antimicrobials such as β-lactams, tetracyclines, quinolones, and sulfonamide was detected. Several other markers, including efflux pumps and aminoglycosides-resistance were distributed among brands. Class 1 and 2 integrons were observed, respectively, in 77% and 97% of the samples. The presence of AR genes is of special interest due to their clinical relevance. Taken together, the data may suggest that the production chain of MFC might contribute to the spread of putative drug-resistant bacteria, which could greatly impact human health. Furthermore, detection of class 1 and class 2 integrons in MFC has led to discussions about resistance gene spread in this traditional cheese, providing evidence of potential horizontal transfer of AR genes to human gut microbiota. Full article

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

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11 pages, 1659 KiB

Open AccessArticle

Pathogenicity Islands Distribution in Non-O157 Shiga Toxin-Producing Escherichia coli (STEC)

by Jimena Soledad Cadona, Ana Victoria Bustamante, Juliana González and Andrea Mariel Sanso

Genes 2018, 9(2), 81; https://doi.org/10.3390/genes9020081 - 10 Feb 2018

Cited by 9 | Viewed by 4787

Abstract

Shiga toxin-producing Escherichia coli (STEC) are foodborne pathogens associated with outbreaks and hemolytic-uremic syndrome. Cattle and meat foods are the main reservoir and infection source, respectively. Pathogenicity islands (PAIs) play an important role in STEC pathogenicity, and non-locus of the enterocyte effacement(LEE) effector (nle) genes present on them encode translocated substrates of the type III secretion system. A molecular risk assessment based on the evaluation of the nle content has been used to predict which STEC strains pose a risk to humans. The goal was to investigate the distribution of the PAIs OI (O-island)-36 (nleB2, nleC, nleH1-1, nleD), OI-57 (nleG2-3, nleG5-2, nleG6-2), OI-71 (nleA, nleF, nleG, nleG2-1, nleG9, nleH1-2) and OI-122 (ent/espL2, nleB, nleE, Z4321, Z4326, Z4332, Z4333) among 204 clinical, food and animal isolates belonging to 52 non-O157:H7 serotypes. Differences in the frequencies of genetic markers and a wide spectrum of PAI virulence profiles were found. In most LEE-negative strains, only module 1 (Z4321) of OI-122 was present. However, some unusual eae-negative strains were detected, which carried other PAI genes. The cluster analysis, excluding isolates that presented no genes, defined two major groups: eae-negative (determined as seropathotypes (SPTs) D, E or without determination, isolated from cattle or food) and eae-positive (mostly identified as SPTs B, C, or not determined). Full article

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

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13 pages, 3687 KiB

Open AccessArticle

Phenotypic and Genotypic Analysis of Antimicrobial Resistance among Listeria monocytogenes Isolated from Australian Food Production Chains

by Annaleise Wilson, Jessica Gray, P. Scott Chandry and Edward M. Fox

Genes 2018, 9(2), 80; https://doi.org/10.3390/genes9020080 - 9 Feb 2018

Cited by 65 | Viewed by 7054

Abstract

The current global crisis of antimicrobial resistance (AMR) among important human bacterial pathogens has been amplified by an increased resistance prevalence. In recent years, a number of studies have reported higher resistance levels among Listeria monocytogenes isolates, which may have implications for treatment of listeriosis infection where resistance to key treatment antimicrobials is noted. This study examined the genotypic and phenotypic AMR patterns of 100 L. monocytogenes isolates originating from food production supplies in Australia and examined this in the context of global population trends. Low levels of resistance were noted to ciprofloxacin (2%) and erythromycin (1%); however, no resistance was observed to penicillin G or tetracycline. Resistance to ciprofloxacin was associated with a mutation in the fepR gene in one isolate; however, no genetic basis for resistance in the other isolate was identified. Resistance to erythromycin was correlated with the presence of the ermB resistance gene. Both resistant isolates belonged to clonal complex 1 (CC1), and analysis of these in the context of global CC1 isolates suggested that they were more similar to isolates from India rather than the other CC1 isolates included in this study. This study provides baseline AMR data for L. monocytogenes isolated in Australia, identifies key genetic markers underlying this resistance, and highlights the need for global molecular surveillance of resistance patterns to maintain control over the potential dissemination of AMR isolates. Full article

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

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242 KiB

Open AccessArticle

Gene-Based Pathogen Detection: Can We Use qPCR to Predict the Outcome of Diagnostic Metagenomics?

by Sandra Christine Andersen, Mette Sofie Rousing Fachmann, Kristoffer Kiil, Eva Møller Nielsen and Jeffrey Hoorfar

Genes 2017, 8(11), 332; https://doi.org/10.3390/genes8110332 - 20 Nov 2017

Cited by 10 | Viewed by 3698

Abstract

In microbial food safety, molecular methods such as quantitative PCR (qPCR) and next-generation sequencing (NGS) of bacterial isolates can potentially be replaced by diagnostic shotgun metagenomics. However, the methods for pre-analytical sample preparation are often optimized for qPCR, and do not necessarily perform equally well for qPCR and sequencing. The present study investigates, through screening of methods, whether qPCR can be used as an indicator for the optimization of sample preparation for NGS-based shotgun metagenomics with a diagnostic focus. This was used on human fecal samples spiked with 10³ or 10⁶ colony-forming units (CFU)/g Campylobacter jejuni, as well as porcine fecal samples spiked with 10³ or 10⁶ CFU/g Salmonella typhimurium. DNA was extracted from the samples using variations of two widely used kits. The following quality parameters were measured: DNA concentration, qPCR, DNA fragmentation during library preparation, amount of DNA available for sequencing, amount of sequencing data, distribution of data between samples in a batch, and data insert size; none showed any correlation with the target ratio of the spiking organism detected in sequencing data. Surprisingly, diagnostic metagenomics can have better detection sensitivity than qPCR for samples spiked with 10³ CFU/g C. jejuni. The study also showed that qPCR and sequencing results may be different due to inhibition in one of the methods. In conclusion, qPCR cannot uncritically be used as an indicator for the optimization of sample preparation for diagnostic metagenomics. Full article

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

Review

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28 pages, 777 KiB

Open AccessReview

The Present and Future of Whole Genome Sequencing (WGS) and Whole Metagenome Sequencing (WMS) for Surveillance of Antimicrobial Resistant Microorganisms and Antimicrobial Resistance Genes across the Food Chain

by Elena A. Oniciuc, Eleni Likotrafiti, Adrián Alvarez-Molina, Miguel Prieto, Jesús A. Santos and Avelino Alvarez-Ordóñez

Genes 2018, 9(5), 268; https://doi.org/10.3390/genes9050268 - 22 May 2018

Cited by 108 | Viewed by 20138 | Correction

Abstract

Antimicrobial resistance (AMR) surveillance is a critical step within risk assessment schemes, as it is the basis for informing global strategies, monitoring the effectiveness of public health interventions, and detecting new trends and emerging threats linked to food. Surveillance of AMR is currently based on the isolation of indicator microorganisms and the phenotypic characterization of clinical, environmental and food strains isolated. However, this approach provides very limited information on the mechanisms driving AMR or on the presence or spread of AMR genes throughout the food chain. Whole-genome sequencing (WGS) of bacterial pathogens has shown potential for epidemiological surveillance, outbreak detection, and infection control. In addition, whole metagenome sequencing (WMS) allows for the culture-independent analysis of complex microbial communities, providing useful information on AMR genes occurrence. Both technologies can assist the tracking of AMR genes and mobile genetic elements, providing the necessary information for the implementation of quantitative risk assessments and allowing for the identification of hotspots and routes of transmission of AMR across the food chain. This review article summarizes the information currently available on the use of WGS and WMS for surveillance of AMR in foodborne pathogenic bacteria and food-related samples and discusses future needs that will have to be considered for the routine implementation of these next-generation sequencing methodologies with this aim. In particular, methodological constraints that impede the use at a global scale of these high-throughput sequencing (HTS) technologies are identified, and the standardization of methods and protocols is suggested as a measure to upgrade HTS-based AMR surveillance schemes. Full article

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

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14 pages, 479 KiB

Open AccessReview

The Most Important Virulence Markers of Yersinia enterocolitica and Their Role during Infection

by Agata Bancerz-Kisiel, Marta Pieczywek, Piotr Łada and Wojciech Szweda

Genes 2018, 9(5), 235; https://doi.org/10.3390/genes9050235 - 3 May 2018

Cited by 63 | Viewed by 9079

Abstract

Yersinia enterocolitica is the causative agent of yersiniosis, a zoonotic disease of growing epidemiological importance with significant consequences for public health. This pathogenic species has been intensively studied for many years. Six biotypes (1A, 1B, 2, 3, 4, 5) and more than 70 serotypes of Y. enterocolitica have been identified to date. The biotypes of Y. enterocolitica are divided according to their pathogenic properties: the non-pathogenic biotype 1A, weakly pathogenic biotypes 2–5, and the highly pathogenic biotype 1B. Due to the complex pathogenesis of yersiniosis, further research is needed to expand our knowledge of the molecular mechanisms involved in the infection process and the clinical course of the disease. Many factors, both plasmid and chromosomal, significantly influence these processes. The aim of this study was to present the most important virulence markers of Y. enterocolitica and their role during infection. Full article

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

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11 pages, 232 KiB

Open AccessReview

Surveillance of Foodborne Pathogens: Towards Diagnostic Metagenomics of Fecal Samples

by Sandra Christine Andersen and Jeffrey Hoorfar

Genes 2018, 9(1), 14; https://doi.org/10.3390/genes9010014 - 4 Jan 2018

Cited by 14 | Viewed by 5695

Abstract

Diagnostic metagenomics is a rapidly evolving laboratory tool for culture-independent tracing of foodborne pathogens. The method has the potential to become a generic platform for detection of most pathogens and many sample types. Today, however, it is still at an early and experimental stage. Studies show that metagenomic methods, from sample storage and DNA extraction to library preparation and shotgun sequencing, have a great influence on data output. To construct protocols that extract the complete metagenome but with minimal bias is an ongoing challenge. Many different software strategies for data analysis are being developed, and several studies applying diagnostic metagenomics to human clinical samples have been published, detecting, and sometimes, typing bacterial infections. It is possible to obtain a draft genome of the pathogen and to develop methods that can theoretically be applied in real-time. Finally, diagnostic metagenomics can theoretically be better geared than conventional methods to detect co-infections. The present review focuses on the current state of test development, as well as practical implementation of diagnostic metagenomics to trace foodborne bacterial infections in fecal samples from animals and humans. Full article

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

Other

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7 pages, 228 KiB

Open AccessCorrection

Correction: Oniciuc, E. A.; et al. The Present and Future of Whole Genome Sequencing (WGS) and Whole Metagenome Sequencing (WMS) for Surveillance of Antimicrobial Resistant Microorganisms and Antimicrobial Resistance Genes across the Food Chain. Genes 2018, 9, 268.

by Elena A. Oniciuc, Eleni Likotrafiti, Adrián Alvarez-Molina, Miguel Prieto, Jesús A. Santos and Avelino Alvarez-Ordóñez

Genes 2018, 9(7), 315; https://doi.org/10.3390/genes9070315 - 25 Jun 2018

Cited by 7 | Viewed by 3830

Abstract

The authors wish to make the following changes to their paper [1]. Due to an undetected mistake in the references management, certain errors appeared in the reference list and a reference was duplicated in Table 1[...] Full article

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

1 pages, 195 KiB

Open AccessErratum

Erratum: Jimena Soledad Cadona, et al.; Pathogenicity Islands Distribution in Non-O157 Shiga Toxin-Producing Escherichia coli (STEC). Genes 2018, 9, 81

by Jimena Soledad Cadona, Ana Victoria Bustamante, Juliana González and Andrea Mariel Sanso

Genes 2018, 9(4), 222; https://doi.org/10.3390/genes9040222 - 20 Apr 2018

Viewed by 3083

Abstract

We wish to make the following correction to the paper by Soledad-Cadona et al.[...] Full article

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

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