Virulence Factors, Enterotoxin Production and Antibiotic Resistance of Staphylococci Isolated from Food

A special issue of Pathogens (ISSN 2076-0817). This special issue belongs to the section "Bacterial Pathogens".

Deadline for manuscript submissions: closed (31 December 2020) | Viewed by 26279

Special Issue Editor


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Guest Editor
Department of Industrial and Food Microbiology, University of Warmia and Mazury in Olsztyn, Olsztyn, Poland
Interests: antimicrobial resistance; food microbiology; coagulase-negative staphylococci; enterococci; Listeria monocytogenes; pathogens; biofilm; virulence factors
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Special Issue Information

Dear Colleagues,

Staphylococci are one of the most common groups of bacteria in food. Staphylococcus aureus has been considered the major pathogen, however, the role of coagulase-negative staphylococci (CNS) in human diseases is currently growing worldwide. The pathogenicity of staphylococci is related to the production of several virulence factors, such as biofilm formation and enterotoxigenic potential, which are responsible for development of the disease process. Studies on clinical strains have shown the extreme potential of staphylococci for the exchange of genetic material. The increasing role of staphylococci during the last decade has been facilitated by the emergence of new clonal types with increased expression of virulence factors and the capacity to neutralize the host immune response. In recent years, the spread of MRSA and MR-CNS strains has been increasing, and represents a hazard to human health. As food microflora, staphylococci can transfer antibiotic resistance genes and virulence factors to other microorganisms present in food. The food chain may be the key site where resistance is transmitted between the environment and humans.

Potential topics include, but are not limited to:

  • Diversity of antimicrobial resistance of coagulase-positive and coagulase-negative staphylococci from food;
  • Virulence factors in staphylococci;
  • Biofilm formation of coagulase-positive and coagulase-negative staphylococci from food;
  • Enterotoxigenic potential of coagulase-positive and coagulase-negative staphylococci from food;
  • Potential exchange of mobile genetic elements (MGEs);
  • Genomic epidemiology of antibiotic-resistant staphylococci from food;
  • Coagulase-negative staphylococci—role as pathogens;
  • Species identification and molecular characterization of staphylococci from food.

We invite you to submit a review article or original research article related to these topics. In particular, we welcome manuscripts that provide new insights into the role of virulence factors or antibiotic resistance determinants in contributing to the pathogenicity of staphylococci.

Dr. Wioleta  Chajȩcka-Wierzchowska
Guest Editor

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Keywords

  • antibiotic resistance
  • virulence factors
  • biofilm
  • enterotoxigenic potential
  • coagulase-negative staphylococci

Published Papers (6 papers)

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Research

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11 pages, 507 KiB  
Article
Occurrence and Characteristics of Staphylococcus aureus in a Hungarian Dairy Farm during a Control Program
by Flóra M. Petróczki, Ákos Pásztor, Kata D. Szűcs, Károly Pál, Gábor Kardos, Ervin Albert, Brigitta Horváth, Erika Ungvári, Béla Béri and Ferenc Peles
Pathogens 2021, 10(2), 104; https://doi.org/10.3390/pathogens10020104 - 21 Jan 2021
Cited by 2 | Viewed by 1726
Abstract
In this research, our aim was to assess the occurrence of Staphylococcus aureus in a Hungarian large-scale dairy farm during the S. aureus control program conducted in the course of our studies. Furthermore, the phenotypic and genotypic properties of the isolates (type of [...] Read more.
In this research, our aim was to assess the occurrence of Staphylococcus aureus in a Hungarian large-scale dairy farm during the S. aureus control program conducted in the course of our studies. Furthermore, the phenotypic and genotypic properties of the isolates (type of haemolysis, antibiotic susceptibility, staphylococcal enterotoxin (SE) gene carrying ability and spa type) were determined. S. aureus was detected in all bulk tank milk samples collected during this study. Two different spa types were identified among the 17 strains isolated in the farm. A total of 14 of the 17 studied strains (82%) showed β-haemolysis on blood agar, 2/17 strains (12%) expressed double zone and 1/17 strains (6%) showed weak β-haemolysis. All strains were susceptible to most antibiotics tested (cefoxitin, chloramphenicol, clindamycin, erythromycin, gentamicin, tetracycline and trimethoprim/sulphamethoxazole), but all strains were resistant to penicillin G. A total of 11 of the 17 strains (65%) were found to harbour seg, sei, selm, seln, selo genes; 4/17 strains (24%) harboured sei, selm, seln, selo genes and 2/17 strains (11%) harboured sei gene. Since the new SEs/SEls can also cause foodborne outbreaks potentially and all strains were found to be resistant to penicillin G, it is essential to decrease and keep the prevalence of S. aureus low in the dairy farm and the implementation of the S. aureus control program is also highly justified. The results showed that the S. aureus count decreased by the end of our studies, so the control program was proved to be effective. Full article
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12 pages, 271 KiB  
Article
Enterotoxigenic Potential of Coagulase-Negative Staphylococci from Ready-to-Eat Food
by Wioleta Chajęcka-Wierzchowska, Joanna Gajewska, Patryk Wiśniewski and Anna Zadernowska
Pathogens 2020, 9(9), 734; https://doi.org/10.3390/pathogens9090734 - 6 Sep 2020
Cited by 26 | Viewed by 4281
Abstract
Although coagulase-positive staphylococci are considered to be the main factor responsible for food poisoning, an increasing role for the coagulase-negative staphylococci in the production of enterotoxins has been observed in recent years. This study was conducted to assess the occurrence of genes responsible [...] Read more.
Although coagulase-positive staphylococci are considered to be the main factor responsible for food poisoning, an increasing role for the coagulase-negative staphylococci in the production of enterotoxins has been observed in recent years. This study was conducted to assess the occurrence of genes responsible for the production of staphylococcal enterotoxins (SE), enterotoxin-like toxins (SEI) and toxic shock syndrome toxin-1 (TSST-1) in coagulase-negative staphylococci (CoNS) isolated from ready-to-eat food from bars and restaurants. One hundred and eighteen CoNS strains were tested using polymerase chain reaction (PCR) to five superantigenic toxin genes, including five different types of classical enterotoxins (sea, seb, sec, sed and see) and the toxic shock syndrome toxin-1 (tsst-1) as well as to supertoxin-like genes. PCR-positive isolates were then tested using immunoenzymatic methods (SET-RPLA, Vidas SET 2) for toxin expression. Out of 118 CoNS strains, the presence of staphylococcal enterotoxins was confirmed in 72% of them. The most frequently found enterotoxin-like genotype was ser, selu. Two of the tested strains had up to ten different enterotoxin genes in the genome at the same time. Although no production of enterotoxins was detected in the CoNS, which means that their possible role in the epidemiology of food-borne diseases is minimal, the data demonstrated that the toxigenic capacity of the CoNS should not be ignored, and that this group of microorganisms should be continuously monitored in food. Full article
12 pages, 265 KiB  
Article
Biofilm Formation Ability and Presence of Adhesion Genes among Coagulase-Negative and Coagulase-Positive Staphylococci Isolates from Raw Cow’s Milk
by Joanna Gajewska and Wioleta Chajęcka-Wierzchowska
Pathogens 2020, 9(8), 654; https://doi.org/10.3390/pathogens9080654 - 14 Aug 2020
Cited by 30 | Viewed by 4539
Abstract
The capacity for biofilm formation is one of the crucial factors of staphylococcal virulence. The occurrence of biofilm-forming staphylococci in raw milk may result in disturbances in technological processes in dairy factories as well as the contamination of finished food products. Therefore, this [...] Read more.
The capacity for biofilm formation is one of the crucial factors of staphylococcal virulence. The occurrence of biofilm-forming staphylococci in raw milk may result in disturbances in technological processes in dairy factories as well as the contamination of finished food products. Therefore, this study aimed to determine the prevalence and characteristics of staphylococcal biofilm formation in raw milk samples and to explore the genetic background associated with biofilm formation in those isolates. The material subjected to testing included 30 cow’s milk samples acquired from farms in the central part of Poland. A total of 54 staphylococcal strains were isolated from the samples, of which 42 were classified as coagulase-negative (CoNS) staphylococci belonging to the following species: S. haemolyticus, S. simulans, S. warneri, S. chromogenes, S. hominis, S. sciuri, S. capitis, S. xylosus and S. saprophyticus, while 12 were classified as S. aureus. The study examined the isolates’ capacity for biofilm formation and the staphylococcal capacity for slime production and determined the presence of genetic determinants responsible for biofilm formation, i.e., the icaA, icaD, bap and eno and, additionally, among coagulase-negative staphylococci, i.e., the aap, bhp, fbe, embP and atlE. Each tested isolate exhibited the capacity for biofilm formation, of which most of them (79.6%) were capable of forming a strong biofilm, while 5.6% formed a moderate biofilm, and 14.8% a weak biofilm. A capacity for slime production was demonstrated in 51.9% isolates. Most of the tested staphylococcal strains (90.7%) had at least one of the tested genes. Nearly half (47.6%) of the CoNS had the eno gene, while for S. aureus, the eno gene was demonstrated in 58.3% isolates. The frequency of the bap gene occurrence was 23.8% and 25% in CoNS strains and S. aureus, respectively. The fbe gene was demonstrated in only three CoNS isolates. The presence of the icaA was only demonstrated in CoNS strains (24.1%), while the icaD was found in both CoNS strains (21.4%) and S. aureus (100%). Among the CoNS, the presence of the embP (16.7%), aap (28.6%) and atlE (23.8%) was demonstrated as well. The obtained study results indicate that bacteria of the Staphylococcus spp. genus have a strong potential to form a biofilm, which may pose a hazard to consumer health. Full article
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23 pages, 1464 KiB  
Article
Genome Mining and Comparative Pathogenomic Analysis of An Endemic Methicillin-Resistant Staphylococcus Aureus (MRSA) Clone, ST612-CC8-t1257-SCCmec_IVd(2B), Isolated in South Africa
by Daniel Gyamfi Amoako, Anou M. Somboro, Akebe Luther King Abia, Mushal Allam, Arshad Ismail, Linda A. Bester and Sabiha Y. Essack
Pathogens 2019, 8(4), 166; https://doi.org/10.3390/pathogens8040166 - 27 Sep 2019
Cited by 9 | Viewed by 5073
Abstract
This study undertook genome mining and comparative genomics to gain genetic insights into the dominance of the methicillin-resistant Staphylococcus aureus (MRSA) endemic clone ST612-CC8-t1257-SCCmec_IVd(2B), obtained from the poultry food chain in South Africa. Functional annotation of the genome revealed a vast array of [...] Read more.
This study undertook genome mining and comparative genomics to gain genetic insights into the dominance of the methicillin-resistant Staphylococcus aureus (MRSA) endemic clone ST612-CC8-t1257-SCCmec_IVd(2B), obtained from the poultry food chain in South Africa. Functional annotation of the genome revealed a vast array of similar central metabolic, cellular and biochemical networks within the endemic clone crucial for its survival in the microbial community. In-silico analysis of the clone revealed the possession of uniform defense systems, restriction-modification system (type I and IV), accessory gene regulator (type I), arginine catabolic mobile element (type II), and type 1 clustered, regularly interspaced, short palindromic repeat (CRISPR)Cas array (N = 7 ± 1), which offer protection against exogenous attacks. The estimated pathogenic potential predicted a higher probability (average Pscore ≈ 0.927) of the clone being pathogenic to its host. The clone carried a battery of putative virulence determinants whose expression are critical for establishing infection. However, there was a slight difference in their possession of adherence factors (biofilm operon system) and toxins (hemolysins and enterotoxins). Further analysis revealed a conserved environmental tolerance and persistence mechanisms related to stress (oxidative and osmotic), heat shock, sporulation, bacteriocins, and detoxification, which enable it to withstand lethal threats and contribute to its success in diverse ecological niches. Phylogenomic analysis with close sister lineages revealed that the clone was closely related to the MRSA isolate SHV713 from Australia. The results of this bioinformatic analysis provide valuable insights into the biology of this endemic clone. Full article
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Review

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45 pages, 1344 KiB  
Review
Virulence Factors in Coagulase-Negative Staphylococci
by Angela França, Vânia Gaio, Nathalie Lopes and Luís D. R. Melo
Pathogens 2021, 10(2), 170; https://doi.org/10.3390/pathogens10020170 - 4 Feb 2021
Cited by 71 | Viewed by 6720
Abstract
Coagulase-negative staphylococci (CoNS) have emerged as major pathogens in healthcare-associated facilities, being S. epidermidis, S. haemolyticus and, more recently, S. lugdunensis, the most clinically relevant species. Despite being less virulent than the well-studied pathogen S. aureus, the number of CoNS [...] Read more.
Coagulase-negative staphylococci (CoNS) have emerged as major pathogens in healthcare-associated facilities, being S. epidermidis, S. haemolyticus and, more recently, S. lugdunensis, the most clinically relevant species. Despite being less virulent than the well-studied pathogen S. aureus, the number of CoNS strains sequenced is constantly increasing and, with that, the number of virulence factors identified in those strains. In this regard, biofilm formation is considered the most important. Besides virulence factors, the presence of several antibiotic-resistance genes identified in CoNS is worrisome and makes treatment very challenging. In this review, we analyzed the different aspects involved in CoNS virulence and their impact on health and food. Full article
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12 pages, 344 KiB  
Review
Novel Treatments and Preventative Strategies Against Food-Poisoning Caused by Staphylococcal Species
by Álvaro Mourenza, José A. Gil, Luis M. Mateos and Michal Letek
Pathogens 2021, 10(2), 91; https://doi.org/10.3390/pathogens10020091 - 20 Jan 2021
Cited by 11 | Viewed by 3288
Abstract
Staphylococcal infections are a widespread cause of disease in humans. In particular, S. aureus is a major causative agent of infection in clinical medicine. In addition, these bacteria can produce a high number of staphylococcal enterotoxins (SE) that may cause food intoxications. Apart [...] Read more.
Staphylococcal infections are a widespread cause of disease in humans. In particular, S. aureus is a major causative agent of infection in clinical medicine. In addition, these bacteria can produce a high number of staphylococcal enterotoxins (SE) that may cause food intoxications. Apart from S. aureus, many coagulase-negative Staphylococcus spp. could be the source of food contamination. Thus, there is an active research work focused on developing novel preventative interventions based on food supplements to reduce the impact of staphylococcal food poisoning. Interestingly, many plant-derived compounds, such as polyphenols, flavonoids, or terpenoids, show significant antimicrobial activity against staphylococci, and therefore these compounds could be crucial to reduce the incidence of food intoxication in humans. Here, we reviewed the most promising strategies developed to prevent staphylococcal food poisoning. Full article
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