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Antibiotic Resistance in Biofilm

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A special issue of Life (ISSN 2075-1729). This special issue belongs to the section "Microbiology".

Deadline for manuscript submissions: closed (31 March 2023) | Viewed by 31609

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Dr. Adriana Morar

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Guest Editor

Faculty of Veterinary Medicine, Banat's University of Agricultural Sciences and Veterinary Medicine "King Michael I of Romania" Timișoara, 300642 Timișoara, Romania
Interests: food safety; food quality; microbial biofilm; antibiotic resistance; pathogenic bacteria
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Dear Colleagues,

The biofilm is a complex group of microorganisms, attached to solid surfaces, in humid environments. It is characterized by structural heterogeneity, genetic diversity, complex interactions, and an extracellular matrix of polymeric substances. The biofilm provides the component microorganisms for certain nutrients, trace elements, and water, and helps to protect against harmful factors, including biocides. Thus, biofilm is commonly found in the food industry, as well as in wet processing conditions (e.g., dairy products, slaughterhouses, meat-processing plants, beverages industry, etc.), and can act as a reservoir of germs with pathogenic potential for humans and animals.

Both pathogenic and non-pathogenic microorganisms can be embedded in the biofilm structure. Occasionally, parts of the biofilm may be removed and spread in moist environments, resulting in subsequent contamination of other surfaces.

Bacteria embedded in biofilm are more resistant to antimicrobials compared to planktonic cells. The increase in bacterial resistance to antibiotics is due to several mechanisms. One of these refers to the different structure of the internal biofilm, which generates the unequal diffusion of antimicrobials. Consequently, bacterial cells will be exposed to different concentrations of antibiotics, depending on their spatial location, which favors the selection of cells with mutational antimicrobial resistance. Another factor is the increase in conjugation frequency, due to the proximity of the cells in the biofilm structures, enhancing the spread of antibiotic resistance.

In this Special Issue, advances in understanding the role of bacterial biofilms in antibiotic resistance in the food industry and the control strategies will be presented.

Dr. Adriana Morar
Guest Editor

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Keywords

biofilm
food industry
antimicrobial resistance
antibiotic resistance gene transfer
antibiofilm activity
control strategies

Published Papers (9 papers)

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Research

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18 pages, 2260 KiB

Open AccessArticle

Molecular Identification of Bacteria Isolated from Marketed Sparus aurata and Penaeus indicus Sea Products: Antibiotic Resistance Profiling and Evaluation of Biofilm Formation

by Mohammad A. Abdulhakeem, Mousa Alreshidi, Fevzi Bardakci, Walid Sabri Hamadou, Vincenzo De Feo, Emira Noumi and Mejdi Snoussi

Life 2023, 13(2), 548; https://0-doi-org.brum.beds.ac.uk/10.3390/life13020548 - 16 Feb 2023

Cited by 3 | Viewed by 2287

Abstract

Background: Marketed fish and shellfish are a source of multidrug-resistant and biofilm-forming foodborne pathogenic microorganisms. Methods: Bacteria isolated from Sparus aurata and Penaeus indicus collected from a local market in Hail region (Saudi Arabia) were isolated on selective and chromogenic media and identified by using 16S RNA sequencing technique. The exoenzyme production and the antibiotic susceptibility patterns of all identified bacteria were also tested. All identified bacteria were tested for their ability to form biofilm by using both qualitative and quantitative assays. Results: Using 16S RNA sequencing method, eight genera were identified dominated by Vibrio (42.85%), Aeromonas (23.80%), and Photobacterium (9.52%). The dominant species were V. natrigens (23.8%) and A. veronii (23.80%). All the identified strains were able to produce several exoenzymes (amylases, gelatinase, haemolysins, lecithinase, DNase, lipase, and caseinase). All tested bacteria were multidrug-resistant with a high value of the multiple antibiotic index (MARI). The antibiotic resistance index (ARI) was about 0.542 for Vibrio spp. and 0.553 for Aeromonas spp. On Congo red agar, six morphotypes were obtained, and 33.33% were slime-positive bacteria. Almost all tested microorganisms were able to form a biofilm on glass tube. Using the crystal violet technique, the tested bacteria were able to form a biofilm on glass, plastic, and polystyrene abiotic surfaces with different magnitude. Conclusions: Our findings suggest that marketed S. aurata and P. indicus harbor various bacteria with human interest that are able to produce several related-virulence factors. Full article

(This article belongs to the Special Issue Antibiotic Resistance in Biofilm)

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12 pages, 296 KiB

Open AccessArticle

Biofilm Formation Capacity and Presence of Virulence Determinants among Enterococcus Species from Milk and Raw Milk Cheeses

by Joanna Gajewska, Wioleta Chajęcka-Wierzchowska, Zuzanna Byczkowska-Rostkowska and Morteza Saki

Life 2023, 13(2), 495; https://0-doi-org.brum.beds.ac.uk/10.3390/life13020495 - 10 Feb 2023

Cited by 7 | Viewed by 1975

Abstract

Bacterial biofilm is one of the major hazards facing the food industry. Biofilm-forming ability is one of the most important virulence properties of enterococci. The genus Enterococcus includes pathogenic, spoilage, and pro-technological bacteria. The presence of enterococci in milk and dairy products is usually associated with inadequate hygiene practices. The study examined the isolates’ capacity for biofilm formation and identification of the genetic determinants of its formation among 85 Enterococcus strains isolated from raw milk (n = 49) and soft-ripened cheeses made from unpasteurized milk (n = 36). E. faecalis and E. faecium were the dominant species. The obtained results showed that 41.4% isolates from milk and 50.0% isolates from cheeses were able to form biofilm. All of the isolates analyzed had at least one of the studied genes. As regards the isolates from raw milk, the most prevalent gene was the gelE (85.6%), followed by the asa1 (66.7%). None of the isolates from cheeses showed the presence of cylA and sprE. The most prevalent gene among the strains from this source was the epbC (94.4%), followed by the gelE (88.9%). In isolates from both sources, the presence of proteins from the Fsr group was noted the least frequently. Nevertheless, results showed that were no significant differences between the biofilm-producing Enterococcus spp. and non-biofilm-producing isolates in term of occurrences of tested virulence genes. The ability to produce a biofilm by enterococci isolated from raw milk or ready-to-eat products emphasizes the need for continuous monitoring of the mechanisms of microbial adhesion. Full article

(This article belongs to the Special Issue Antibiotic Resistance in Biofilm)

17 pages, 1876 KiB

Open AccessArticle

Characterization of Probiotic Properties of Lacticaseibacillus paracasei L2 Isolated from a Traditional Fermented Food “Lben”

by Amina Cheikh M’hamed, Karima Ncib, Abderrahmen Merghni, Mariem Migaou, Houda Lazreg, Mejdi Snoussi, Emira Noumi, Mohamed Ben Mansour and Raoui Mounir Maaroufi

Life 2023, 13(1), 21; https://0-doi-org.brum.beds.ac.uk/10.3390/life13010021 - 21 Dec 2022

Cited by 6 | Viewed by 2337

Abstract

Lben is a dairy fermented food that is largely consumed in Tunisia for its numerous health benefits that are related to the existence of probiotics. Lactic Acid Bacteria (LAB) are well known for their beneficial probiotic properties for humans, especially when administered in adequate amounts. The aim of this study was to isolate and investigate the probiotics properties of Lacticaseibacillus paracasei L2 from Lben. The isolated strain was identified by 16S r-RNA gene sequences and MALDI- TOF MS. To evaluate the probiotic potential of the isolated bacterium, in vitro tests were performed, including adhesion ability to HCT-116 cells, survival in acid and bile salt conditions, lysozyme resistance, biofilm formation, hemolytic activity, antioxidant activity, and antimicrobial activity. Our results revealed that the selected Lacticaseibacillus paracasei L2 strain expressed a high adherence to HCT-116 cells (45.03%), survived under acidic conditions (pH3), and showed a resistance to bile salts. The strain was considered as safe (α-hemolysis). L. paracasei L2 showed a high biofilm-formation ability (OD 570 > 1.7) after 24 h of incubation. It also demonstrated an important antioxidant activity in the range of 85.31% for the intact cells. However, an antimicrobial activity against pathogens, namely Staphylococcus aureus, was detected with an IZ that was above 19 mm. In conjunction with the results obtained and the technological properties of Lacticaseibacillus paracasei L2 (proteolytic property, autolytic activity, acidifying activity, and EPS production), this strain may be used as a probiotic for manufacturing fermented foods. Full article

(This article belongs to the Special Issue Antibiotic Resistance in Biofilm)

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15 pages, 5422 KiB

Open AccessArticle

Antibiofilm Potential and Exoenzyme Inhibition by Elattaria cardamomum Essential Oil in Candida spp. Strains

by Emira Noumi, Ghada Salamah Alshammari, Tarek Zmantar, Abdulrahman S. Bazaid, Khulood Fahad Alabbosh, Abdelbaset Mohamed Elasbali, Waleed Abu Al-Soud, Sami Ghazi Alrashidi and Mejdi Snoussi

Life 2022, 12(11), 1756; https://0-doi-org.brum.beds.ac.uk/10.3390/life12111756 - 1 Nov 2022

Cited by 3 | Viewed by 1461

Abstract

Fungal infections caused by Candida species have attracted great interest due to their resistance to commercial antifungal agents. Essential oils from aromatic and medicinal plants have many bioactive compounds that are known for their important biological activities, mainly their antimicrobial effects. In the present study, we aimed to evaluate the antifungal ability of Elettaria cardamomum essential oil (EO) against different clinical Candida isolates. Then, we investigated the anti-phospholipase, anti-protease, and anti-biofilm activity of E. cardamomum EO against the selected isolates. Twenty-four Candida strains (clinical and reference) were tested for virulence factors such as biofilm formation, protease, and phospholipase activity. The minimum inhibitory (MIC) and fungicidal (MFC) concentrations of E. cardamomum were determined, and their effects were tested against all Candida strains. Our results revealed that E. cardamomum EO was rich in α-terpinyl acetate (56.5%), limonene (12.6%), and mentha-2.4(8)-diene (7.65%). The tested EO showed activity against all tested Candida strains in their planktonic form and against exoenzymes and biofilm production. Based on our findings, we promote the use of E. cardamomum EO as a treatment against clinical Candida isolates active on the virulence factors of this fungus. Full article

(This article belongs to the Special Issue Antibiotic Resistance in Biofilm)

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8 pages, 475 KiB

Open AccessArticle

Antibiofilm Activity of LL-37 Peptide and D-Amino Acids Associated with Antibiotics Used in Regenerative Endodontics on an Ex Vivo Multispecies Biofilm Model

by Ana C. C. Pereira, Alana P. S. Aguiar, Leticia M. P. Araujo, Larissa O. Dantas, Marcia P. A. Mayer, Lamprini Karygianni, Thomas Thurnheer and Ericka T. Pinheiro

Life 2022, 12(11), 1686; https://0-doi-org.brum.beds.ac.uk/10.3390/life12111686 - 24 Oct 2022

Cited by 4 | Viewed by 1596

Abstract

The antimicrobial peptide LL-37 and D-amino acids (D-AAs) have been proposed as antibiofilm agents. Therefore, this study aimed to test the antimicrobial effect of antibiofilm agents associated with antibiotics used in regenerative endodontic procedures (the triple antibiotic paste—TAP: ciprofloxacin + metronidazole + minocycline). An endodontic-like biofilm model grown on bovine dentin discs was used in this study. After 21-day growth, the biofilms were treated with 1 mg/mL TAP, 10 μM LL-37, an association of LL-37 + TAP, 40 mM D-AAs solution, an association of D-AAs + TAP, and phosphate-buffered saline (negative control). Colony forming unit (CFU) data were analyzed by two-way ANOVA and Tukey’s multiple comparison test (p < 0.05). LL-37 + TAP showed the best antibacterial activity (7-log¹⁰ CFU/mL ± 0.5), reaching a 1 log reduction of cells in relation to the negative control (8-log¹⁰ CFU/mL ± 0.7) (p < 0.05). In turn, no significant reduction in bacterial cells was observed with TAP, LL-37, D-AAs, and D-AAs + TAP compared to the negative control. In conclusion, the combination of antibiotics and LL-37 peptide showed mild antibacterial activity, while the combination of antibiotics and D-AAs showed no activity against complex biofilms. Full article

(This article belongs to the Special Issue Antibiotic Resistance in Biofilm)

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11 pages, 1486 KiB

Open AccessArticle

Comparative Study of Antibacterial, Antibiofilm, Antiswarming and Antiquorum Sensing Activities of Origanum vulgare Essential Oil and Terpinene-4-ol against Pathogenic Bacteria

by Abderrahmen Merghni, Najla Haddaji, Nouha Bouali, Khulood Fahad Alabbosh, Mohd Adnan, Mejdi Snoussi and Emira Noumi

Life 2022, 12(10), 1616; https://0-doi-org.brum.beds.ac.uk/10.3390/life12101616 - 17 Oct 2022

Cited by 9 | Viewed by 1979

Abstract

Essential oils from aromatic and medicinal plants have many bioactive compounds known for their important biological activities mainly their antibacterial effects. Here we evaluated qualitatively and quantitatively the biofilm formation capability of pathogenic bacterial strains (n = 8). Then, we investigated the antibacterial, antibiofilm, antiquorum-sensing, and antiswarming efficacy of Origanum vulgare essential oil (EO) and terpinene-4-ol. Our results revealed that EO exhibited a more potent inhibitory effect against the tested strains. While the terpinene-4-ol was found to be more effective against developed Staphylococcus aureus biofilm. Regarding the anti quorum-sensing activity, we noticed that O. vulgare displayed better inhibition percentages in violacein production even at a low concentration (MIC/4). Additionally, this EO showed better inhibition of Pseudomonas aeruginosa PAO1 migration in comparison with the terpinene-4-ol. Our findings revealed that using pure O. vulgare EO demonstrated better competitive effects against pathogenic bacteria with a different mode of action when compared to the terpinene-4-ol. Hence, exploration and development of efficient anti-infection agents from natural resources such as full EOs represent promising tools in anti-infective therapy. Full article

(This article belongs to the Special Issue Antibiotic Resistance in Biofilm)

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Review

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24 pages, 2039 KiB

Open AccessReview

Therapeutic Strategies against Biofilm Infections

by Sonal Mishra, Amit Gupta, Vijay Upadhye, Suresh C. Singh, Rajeshwar P. Sinha and Donat-P. Häder

Life 2023, 13(1), 172; https://0-doi-org.brum.beds.ac.uk/10.3390/life13010172 - 6 Jan 2023

Cited by 23 | Viewed by 5870

Abstract

A biofilm is an aggregation of surface-associated microbial cells that is confined in an extracellular polymeric substance (EPS) matrix. Infections caused by microbes that form biofilms are linked to a variety of animals, including insects and humans. Antibiotics and other antimicrobials can be used to remove or eradicate biofilms in order to treat infections. However, due to biofilm resistance to antibiotics and antimicrobials, clinical observations and experimental research clearly demonstrates that antibiotic and antimicrobial therapies alone are frequently insufficient to completely eradicate biofilm infections. Therefore, it becomes crucial and urgent for clinicians to properly treat biofilm infections with currently available antimicrobials and analyze the results. Numerous biofilm-fighting strategies have been developed as a result of advancements in nanoparticle synthesis with an emphasis on metal oxide np. This review focuses on several therapeutic strategies that are currently being used and also those that could be developed in the future. These strategies aim to address important structural and functional aspects of microbial biofilms as well as biofilms’ mechanisms for drug resistance, including the EPS matrix, quorum sensing (QS), and dormant cell targeting. The NPs have demonstrated significant efficacy against bacterial biofilms in a variety of bacterial species. To overcome resistance, treatments such as nanotechnology, quorum sensing, and photodynamic therapy could be used. Full article

(This article belongs to the Special Issue Antibiotic Resistance in Biofilm)

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35 pages, 2601 KiB

Open AccessReview

Natural Strategies as Potential Weapons against Bacterial Biofilms

by Syeda Tasmia Asma, Kálmán Imre, Adriana Morar, Mirela Imre, Ulas Acaroz, Syed Rizwan Ali Shah, Syed Zajif Hussain, Damla Arslan-Acaroz, Fatih Ramazan Istanbullugil, Khodir Madani, Christos Athanassiou, Alexander Atanasoff, Doru Morar, Viorel Herman and Kui Zhu

Life 2022, 12(10), 1618; https://0-doi-org.brum.beds.ac.uk/10.3390/life12101618 - 17 Oct 2022

Cited by 10 | Viewed by 5196

Abstract

Microbial biofilm is an aggregation of microbial species that are either attached to surfaces or organized into an extracellular matrix. Microbes in the form of biofilms are highly resistant to several antimicrobials compared to planktonic microbial cells. Their resistance developing ability is one of the major root causes of antibiotic resistance in health sectors. Therefore, effective antibiofilm compounds are required to treat biofilm-associated health issues. The awareness of biofilm properties, formation, and resistance mechanisms facilitate researchers to design and develop combating strategies. This review highlights biofilm formation, composition, major stability parameters, resistance mechanisms, pathogenicity, combating strategies, and effective biofilm-controlling compounds. The naturally derived products, particularly plants, have demonstrated significant medicinal properties, producing them a practical approach for controlling biofilm-producing microbes. Despite providing effective antibiofilm activities, the plant-derived antimicrobial compounds may face the limitations of less bioavailability and low concentration of bioactive molecules. The microbes-derived and the phytonanotechnology-based antibiofilm compounds are emerging as an effective approach to inhibit and eliminate the biofilm-producing microbes. Full article

(This article belongs to the Special Issue Antibiotic Resistance in Biofilm)

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31 pages, 5882 KiB

Open AccessReview

An Overview of Biofilm Formation–Combating Strategies and Mechanisms of Action of Antibiofilm Agents

by Syeda Tasmia Asma, Kálmán Imre, Adriana Morar, Viorel Herman, Ulas Acaroz, Hamid Mukhtar, Damla Arslan-Acaroz, Syed Rizwan Ali Shah and Robin Gerlach

Life 2022, 12(8), 1110; https://0-doi-org.brum.beds.ac.uk/10.3390/life12081110 - 23 Jul 2022

Cited by 41 | Viewed by 7377

Abstract

Biofilm formation on surfaces via microbial colonization causes infections and has become a major health issue globally. The biofilm lifestyle provides resistance to environmental stresses and antimicrobial therapies. Biofilms can cause several chronic conditions, and effective treatment has become a challenge due to increased antimicrobial resistance. Antibiotics available for treating biofilm-associated infections are generally not very effective and require high doses that may cause toxicity in the host. Therefore, it is essential to study and develop efficient anti-biofilm strategies that can significantly reduce the rate of biofilm-associated healthcare problems. In this context, some effective combating strategies with potential anti-biofilm agents, including plant extracts, peptides, enzymes, lantibiotics, chelating agents, biosurfactants, polysaccharides, organic, inorganic, and metal nanoparticles, etc., have been reviewed to overcome biofilm-associated healthcare problems. From their extensive literature survey, it can be concluded that these molecules with considerable structural alterations might be applied to the treatment of biofilm-associated infections, by evaluating their significant delivery to the target site of the host. To design effective anti-biofilm molecules, it must be assured that the minimum inhibitory concentrations of these anti-biofilm compounds can eradicate biofilm-associated infections without causing toxic effects at a significant rate. Full article

(This article belongs to the Special Issue Antibiotic Resistance in Biofilm)

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