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Microorganisms
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Enterococci for Probiotic Use: Safety and Risk
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Enterococci for Probiotic Use: Safety and Risk

A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Gut Microbiota".

Deadline for manuscript submissions: closed (31 December 2021) | Viewed by 26797

Special Issue Editors

Dr. Nathalie Connil

E-Mail Website
Guest Editor
Research Unit Bacterial Communication and Anti-Infectious Strategies (CBSA, UR4312), University of Rouen Normandie, 27000 Evreux, France
Interests: gut microbiota; gut-brain axis; host-microbe interactions; probiotics; health benefits; virulence; antibiotic resistance; safety
Special Issues, Collections and Topics in MDPI journals
Dr. Mohamed Zommiti

E-Mail Website
Guest Editor
Research Unit Bacterial Communication and Anti-infectious Strategies (UR CBSA), University of Rouen Normandie, 27000 Evreux, France
Interests: food microbiology; beneficial microbes; gut microbiota; probiotics; bacteriocins; Organ-On-Chip; microfluidics
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

The genus Enterococcus, as the third largest genus of lactic acid bacteria, encompasses a considerable number of bacterial strains that are highly competitive due to their astonishing resistance to hostile environments. Enterococcus faecalis and Enterococcus faecium are the most studied representatives of this genus, in terms of medical and food microbiology fields, especially as potential probiotics. Enterococci are known to produce lactic acid, as the end product of sugar fermentation, and antimicrobials, also known as enterocins, a family of safe and ribosomally synthesized antimicrobial peptides which are active against a wide range of sturdy pathogens. Although Enterococcus species are not “generally recognized as safe” (GRAS status), different Enterococcus species have been investigated as probiotics, such as E. faecalis, E. faecium, E. lactis, and more recently E. hirae and E. durans. The use of enterococci as probiotics remains contentious: while the probiotic benefits of some strains have been well established, the increase in enterococcal ailments associated with human health and resistance to multiple classes of antibiotics has raised critical concerns about their use reflecting a heavy burden on public health system. Despite this controversy, some strains are commercialized as probiotics and are currently in use as therapeutic treatments. These latters are marketed as Cylactins, Fargo 688s, ECOFLOR, or Symbioflor 1 in order to assuage the symptoms of diverse disorders and diseases such as the irritable bowel syndrome, recurrent infections of the upper/lower respiratory tracts, and recurrent chronic sinusitis or bronchitis.

This Special Issue looks into the assessment of diverse aspects of Enterococcus spp. related to their probiotic properties and safety concerns, as well as the current and potential application in food systems and treatment of infections, particularly Enterococcus faecalis, with the aim of presenting newest trends and developments in probiotic and medicopharmaceutical applications. The regulatory status of commensal Enterococcus candidates for food, feed, probiotic use, and recommended approaches to appraise and ensure their safety will also be included.

Dr. Nathalie Connil
Dr. Mohamed Zommiti
Guest Editors

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. Microorganisms 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 2700 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

  • gut microbiota
  • Enterococcus
  • probiotics
  • health benefits
  • human
  • livestock
  • virulence
  • antibiotic resistance
  • safety

Published Papers (5 papers)

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Editorial

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3 pages, 191 KiB  
Editorial
Special Issue “Enterococci for Probiotic Use: Safety and Risk”: Editorial
by Mohamed Zommiti, Sylvie Chevalier, Marc G. J. Feuilloley and Nathalie Connil
Microorganisms 2022, 10(3), 604; https://doi.org/10.3390/microorganisms10030604 - 12 Mar 2022
Cited by 10 | Viewed by 3015
Abstract
Microorganisms, their activity, and metabolites are now considered as intrinsic elements of the human body and this awareness gave was leading to the concept of holobiont [...] Full article
(This article belongs to the Special Issue Enterococci for Probiotic Use: Safety and Risk)

Research

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21 pages, 7440 KiB  
Article
Norepinephrine and Serotonin Can Modulate the Behavior of the Probiotic Enterococcus faecium NCIMB10415 towards the Host: Is a Putative Surface Sensor Involved?
by Rossella Scardaci, Francesca Bietto, Pierre-Jean Racine, Amine M. Boukerb, Olivier Lesouhaitier, Marc G. J. Feuilloley, Sara Scutera, Tiziana Musso, Nathalie Connil and Enrica Pessione
Microorganisms 2022, 10(3), 487; https://doi.org/10.3390/microorganisms10030487 - 22 Feb 2022
Cited by 10 | Viewed by 2256
Abstract
The human gut microbiota has co-evolved with humans by exchanging bidirectional signals. This study aims at deepening the knowledge of this crucial relationship by analyzing phenotypic and interactive responses of the probiotic Enterococcus faecium NCIMB10415 (E. faecium SF68) to the top-down signals [...] Read more.
The human gut microbiota has co-evolved with humans by exchanging bidirectional signals. This study aims at deepening the knowledge of this crucial relationship by analyzing phenotypic and interactive responses of the probiotic Enterococcus faecium NCIMB10415 (E. faecium SF68) to the top-down signals norepinephrine (NE) and serotonin (5HT), two neuroactive molecules abundant in the gut. We treated E. faecium NCIMB10415 with 100 µM NE and 50 µM 5HT and tested its ability to form static biofilm (Confocal Laser Scanning Microscopy), adhere to the Caco-2/TC7 monolayer, affect the epithelial barrier function (Transepithelial Electrical Resistance) and human dendritic cells (DC) maturation, differentiation, and cytokines production. Finally, we evaluated the presence of a putative hormone sensor through in silico (whole genome sequence and protein modelling) and in vitro (Micro-Scale Thermophoresis) analyses. The hormone treatments increase biofilm formation and adhesion on Caco-2/TC7, as well as the epithelial barrier function. No differences concerning DC differentiation and maturation between stimulated and control bacteria were detected, while an enhanced TNF-α production was observed in NE-treated bacteria. Investigations on the sensor support the hypothesis that a two-component system on the bacterial surface can sense 5HT and NE. Overall, the data demonstrate that E. faecium NCIMB10415 can sense both NE and 5HT and respond accordingly. Full article
(This article belongs to the Special Issue Enterococci for Probiotic Use: Safety and Risk)
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13 pages, 15471 KiB  
Article
New Insights into the Virulence Traits and Antibiotic Resistance of Enterococci Isolated from Diverse Probiotic Products
by Fengru Deng, Yunsheng Chen, Xiaoyu Zhou, Huiying Xiao, Tianyu Sun, Yiqun Deng and Jikai Wen
Microorganisms 2021, 9(4), 726; https://doi.org/10.3390/microorganisms9040726 - 31 Mar 2021
Cited by 8 | Viewed by 2370
Abstract
The GRAS (generally recognized as safe) status of Enterococcus has not yet been authenticated, but enterococci, as probiotics, have been increasingly applied in human healthcare and animal husbandry, for instance as a dietary supplement, feed additive, or growth promotor. The food chain is [...] Read more.
The GRAS (generally recognized as safe) status of Enterococcus has not yet been authenticated, but enterococci, as probiotics, have been increasingly applied in human healthcare and animal husbandry, for instance as a dietary supplement, feed additive, or growth promotor. The food chain is the important route for introducing enterococci into the human gut. The pathogenicity of Enterococcus from probiotic products requires investigation. In the study, 110 commercial probiotic products used for human, animal, aquaculture, and plants were examined, among which 36 enterococci were identified, including 31 from Enterococcus faecium, 2 from E. faecalis, 2 from E. casseliflavus, and 1 from E. gallinarum. Strikingly, 28 of the 36 enterococci isolated from probiotics here did not mention the presence of Enterococcus in the labeled ingredients, and no Enterococcus isolates were found from 5 animal probiotics that were labeled with the genus. In total, 35 of the 110 products exhibited hemolysis, including 5 (10.6%) human probiotics, 14 (41.2%) animal probiotics, 8 (57.1%) aquaculture probiotics, and 8 (53.3%) plant probiotics. The detection rates of virulence factors associated with adhesion, antiphagocytosis, exoenzyme, biofilm, and other putative virulence markers (PVM) in 36 enterococci were 94.4%, 91.7%, 5.6%, 94.4% and 8.3%. Twenty-six of the 36 isolated strains exhibited biofilm formation ability, where 25 strains (69.4%) and one (2.8%) were strong and weak biofilm producers, respectively. We analyzed the resistance rates against erythromycin (97%), vancomycin and ciprofloxacin (8%), tetracycline (3%), and high-level aminoglycosides (0%), respectively. High detection rates of msrC/lsaA (86%) and aac(6′)-Ii (86%) were observed, followed by vanC (8%), tetM (3%). The Tn5801-tetM-like integrative conjugative element (ICE) was identified in E. gallinarum, exhibiting resistance to tetracycline (64 μg/mL). Seven probiotic E. faecalis and E. faecium, as active ingredients in human probiotics, shared the same STs (sequence types) and were distinct from the STs of other contaminated or mislabeled enterococci, indicating that two particular STs belonged to native probiotic isolates. These findings advocate appropriate assessments of enterococci when used in probiotics. Full article
(This article belongs to the Special Issue Enterococci for Probiotic Use: Safety and Risk)
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Review

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33 pages, 521 KiB  
Review
Enterococcus spp.: Is It a Bad Choice for a Good Use—A Conundrum to Solve?
by Mounir Ferchichi, Khaled Sebei, Amine Mohamed Boukerb, Najoua Karray-Bouraoui, Sylvie Chevalier, Marc G. J. Feuilloley, Nathalie Connil and Mohamed Zommiti
Microorganisms 2021, 9(11), 2222; https://doi.org/10.3390/microorganisms9112222 - 26 Oct 2021
Cited by 18 | Viewed by 3591
Abstract
Since antiquity, the ubiquitous lactic acid bacteria (LAB) Enterococci, which are just as predominant in both human and animal intestinal commensal flora, have been used (and still are) as probiotics in food and feed production. Their qualities encounter several hurdles, particularly in terms [...] Read more.
Since antiquity, the ubiquitous lactic acid bacteria (LAB) Enterococci, which are just as predominant in both human and animal intestinal commensal flora, have been used (and still are) as probiotics in food and feed production. Their qualities encounter several hurdles, particularly in terms of the array of virulence determinants, reflecting a notorious reputation that nearly prevents their use as probiotics. Additionally, representatives of the Enterococcus spp. genus showed intrinsic resistance to several antimicrobial agents, and flexibility to acquire resistance determinants encoded on a broad array of conjugative plasmids, transposons, and bacteriophages. The presence of such pathogenic aspects among some species represents a critical barrier compromising their use as probiotics in food. Thus, the genus neither has Generally Recognized as Safe (GRAS) status nor has it been included in the Qualified Presumption of Safety (QPS) list implying drastic legislation towards these microorganisms. To date, the knowledge of the virulence factors and the genetic structure of foodborne enterococcal strains is rather limited. Although enterococcal infections originating from food have never been reported, the consumption of food carrying virulence enterococci seems to be a risky path of transfer, and hence, it renders them poor choices as probiotics. Auspiciously, enterococcal virulence factors seem to be strain specific suggesting that clinical isolates carry much more determinants that food isolates. The latter remain widely susceptible to clinically relevant antibiotics and subsequently, have a lower potential for pathogenicity. In terms of the ideal enterococcal candidate, selected strains deemed for use in foods should not possess any virulence genes and should be susceptible to clinically relevant antibiotics. Overall, implementation of an appropriate risk/benefit analysis, in addition to the case-by-case assessment, the establishment of a strain’s innocuity, and consideration for relevant guidelines, legislation, and regulatory aspects surrounding functional food development seem to be the crucial elements for industries, health-staff and consumers to accept enterococci, like other LAB, as important candidates for useful and beneficial applications in food industry and food biotechnology. The present review aims at shedding light on the world of hurdles and limitations that hampers the Enterococcus spp. genus and its representatives from being used or proposed for use as probiotics. The future of enterococci use as probiotics and legislation in this field are also discussed. Full article
(This article belongs to the Special Issue Enterococci for Probiotic Use: Safety and Risk)
21 pages, 1658 KiB  
Review
The Many Faces of Enterococcus spp.—Commensal, Probiotic and Opportunistic Pathogen
by Beata Krawczyk, Paweł Wityk, Mirosława Gałęcka and Michał Michalik
Microorganisms 2021, 9(9), 1900; https://doi.org/10.3390/microorganisms9091900 - 07 Sep 2021
Cited by 107 | Viewed by 13831
Abstract
Enterococcus spp. are Gram-positive, facultative, anaerobic cocci, which are found in the intestinal flora and, less frequently, in the vagina or mouth. Enterococcus faecalis and Enterococcus faecium are the most common species found in humans. As commensals, enterococci colonize the digestive system and [...] Read more.
Enterococcus spp. are Gram-positive, facultative, anaerobic cocci, which are found in the intestinal flora and, less frequently, in the vagina or mouth. Enterococcus faecalis and Enterococcus faecium are the most common species found in humans. As commensals, enterococci colonize the digestive system and participate in the modulation of the immune system in humans and animals. For many years reference enterococcal strains have been used as probiotic food additives or have been recommended as supplements for the treatment of intestinal dysbiosis and other conditions. The use of Enterococcus strains as probiotics has recently become controversial due to the ease of acquiring different virulence factors and resistance to various classes of antibiotics. Enterococci are also seen as opportunistic pathogens. This problem is especially relevant in hospital environments, where enterococcal outbreaks often occur. Their ability to translocate from the gastro-intestinal tract to various tissues and organs as well as their virulence and antibiotic resistance are risk factors that hinder eradication. Due to numerous reports on the plasticity of the enterococcal genome and the acquisition of pathogenic microbial features, we ask ourselves, how far is this commensal genus from acquiring pathogenicity? This paper discusses both the beneficial properties of these microorganisms and the risk factors related to their evolution towards pathogenicity. Full article
(This article belongs to the Special Issue Enterococci for Probiotic Use: Safety and Risk)
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