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Feature Papers in Microbial Biofilm Formation

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

Deadline for manuscript submissions: closed (28 February 2023) | Viewed by 34101

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Prof. Dr. Ute Römling

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Department of Microbiology, Tumor and Cell Biology (MTC), Karolinska Institutet, Stockholm, Sweden
Interests: microbial biofilm formation; cyclic di-nucleotide signaling; pathogen-host interaction; protein quality control; Salmonella typhimurium; Pseudomonas aeruginosa; Candida parapsilosis
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Prof. Dr. Grzegorz Wegrzyn

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Department of Molecular Biology, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland
Interests: gene expression regulation; DNA replication; bacteriophages; plasmids; human genetic diseases; neurodegeneration
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Special Issue Information

Dear Colleagues,

Microbial biofilm formation, the coordinated assembly of self-replicating cells into multicellular communities, emerged at least 3.5 billion years ago and is an ancient prototype of tissue-like structures connected by an extracellular matrix that arose in order to more efficiently meet metabolic, physiological, and environmental challenges.

As particular challenges can be met under almost or even all circumstances, the biofilm formation of microorganisms is ubiquitous and diverse. Although beneficial biofilm formation such as biofilm formation of microorganisms in the global terrestrial biosphere, of the commensal flora and of microbes in wastewater treatment is much more common, detrimental biofilm formation in clinical, industrial and agricultural settings can implement undesirable long-term consequences. Due to the complexity of multicellular aggregate formation, theoretical and experimental approaches from different disciplines need to address the various aspects of biofilm formation.

In this volume of featured papers, some of the diverse aspects of biofilm research will be addressed.

Prof. Dr. Ute Römling
Prof. Dr. Grzegorz Wegrzyn
Guest Editors

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Keywords

commensal
environment
metabolism
multi-disciplinarity
pathogen
second messenger signaling

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Published Papers (10 papers)

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18 pages, 7096 KiB

Open AccessArticle

Monitoring Growth and Removal of Pseudomonas Biofilms on Cellulose-Based Fabrics

by María del Rosario Agustín, Peter Stengel, Matthias Kellermeier, Katrin-Stephanie Tücking and Mareike Müller

Microorganisms 2023, 11(4), 892; https://doi.org/10.3390/microorganisms11040892 - 30 Mar 2023

Cited by 4 | Viewed by 2788

Abstract

Biofilms are often tolerant towards routine cleaning and disinfection processes. As they can grow on fabrics in household or healthcare settings, resulting in odors and serious health problems, it is necessary to contain biofilms through eradication strategies. The current study proposes a novel test model for the growth and removal of biofilms on textiles with Pseudomonas fluorescens and the opportunistic nosocomial pathogen Pseudomonas aeruginosa as model organisms. To assess the biofilm removal on fabrics, (1) a detergent-based, (2) enzyme-based, and (3) combined formulation of both detergent and enzymes (F1/2) were applied. Biofilms were analyzed microscopically (FE-SEM, SEM, 3D laser scanning- and epifluorescence microscopy), via a quartz crystal microbalance with mass dissipation monitoring (QCM-D) as well as plate counting of colonies. This study indicated that Pseudomonas spp. form robust biofilms on woven cellulose that can be efficiently removed via F1/2, proven by a significant reduction (p < 0.001) of viable bacteria in biofilms. Moreover, microscopic analysis indicated a disruption and almost complete removal of the biofilms after F1/2 treatment. QCM-D measurements further confirmed a maximal mass dissipation change after applying F1/2. The combination strategy applying both enzymes and detergent is a promising antibiofilm approach to remove bacteria from fabrics. Full article

(This article belongs to the Special Issue Feature Papers in Microbial Biofilm Formation)

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15 pages, 2113 KiB

Open AccessArticle

Evaluation of Biofilm Cultivation Models for Efficacy Testing of Disinfectants against Salmonella Typhimurium Biofilms

by Anja M. Richter, Katharina Konrat, Ane M. Osland, Emma Brook, Claire Oastler, Lene K. Vestby, Rebecca J. Gosling, Live L. Nesse and Mardjan Arvand

Microorganisms 2023, 11(3), 761; https://doi.org/10.3390/microorganisms11030761 - 16 Mar 2023

Cited by 2 | Viewed by 3552

Abstract

Within the European Union, Salmonella is frequently reported in food and feed products. A major route of transmission is upon contact with contaminated surfaces. In nature, bacteria such as Salmonella are often encountered in biofilms, where they are protected against antibiotics and disinfectants. Therefore, the removal and inactivation of biofilms is essential to ensure hygienic conditions. Currently, recommendations for disinfectant usage are based on results of efficacy testing against planktonic bacteria. There are no biofilm-specific standards for the efficacy testing of disinfectants against Salmonella. Here, we assessed three models for disinfectant efficacy testing on Salmonella Typhimurium biofilms. Achievable bacterial counts per biofilm, repeatability, and intra-laboratory reproducibility were analyzed. Biofilms of two Salmonella strains were grown on different surfaces and treated with glutaraldehyde or peracetic acid. Disinfectant efficacy was compared with results for planktonic Salmonella. All methods resulted in highly repeatable cell numbers per biofilm, with one assay showing variations of less than 1 log₁₀ CFU in all experiments for both strains tested. Disinfectant concentrations required to inactivate biofilms were higher compared to planktonic cells. Differences were found between the biofilm methods regarding maximal achievable cell numbers, repeatability, and intra-laboratory reproducibility of results, which may be used to identify the most appropriate method in relation to application context. Developing a standardized protocol for testing disinfectant efficacy on biofilms will help identify conditions that are effective against biofilms. Full article

(This article belongs to the Special Issue Feature Papers in Microbial Biofilm Formation)

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12 pages, 4470 KiB

Open AccessEditor’s ChoiceArticle

Nanoparticle Coatings on Glass Surfaces to Prevent Pseudomonas fluorescens AR 11 Biofilm Formation

by Daniele Marra, Irene Perna, Giulio Pota, Giuseppe Vitiello, Alessandro Pezzella, Giuseppe Toscano, Giuseppina Luciani and Sergio Caserta

Microorganisms 2023, 11(3), 621; https://doi.org/10.3390/microorganisms11030621 - 28 Feb 2023

Cited by 6 | Viewed by 2074

Abstract

Microbial colonization of surfaces is a sanitary and industrial issue for many applications, leading to product contamination and human infections. When microorganisms closely interact with a surface, they start to produce an exo-polysaccaridic matrix to adhere to and protect themselves from adverse environmental conditions. This type of structure is called a biofilm. The aim of our work is to investigate novel technologies able to prevent biofilm formation by surface coatings. We coated glass surfaces with melanin-ZnO₂, melanin-TiO₂, and TiO₂ hybrid nanoparticles. The functionalization was performed using cold plasma to activate glass-substrate-coated surfaces, that were characterized by performing water and soybean oil wetting tests. A quantitative characterization of the antibiofilm properties was done using Pseudomonas fluorescens AR 11 as a model organism. Biofilm morphologies were observed using confocal laser scanning microscopy and image analysis techniques were used to obtain quantitative morphological parameters. The results highlight the efficacy of the proposed surface coating to prevent biofilm formation. Melanin-TiO₂ proved to be the most efficient among the particles investigated. Our results can be a valuable support for future implementation of the technique proposed here in an extended range of applications that may include further testing on other strains and other support materials. Full article

(This article belongs to the Special Issue Feature Papers in Microbial Biofilm Formation)

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16 pages, 3558 KiB

Open AccessArticle

Microbial Dynamics in Mixed-Culture Biofilms of Salmonella Typhimurium and Escherichia coli O157:H7 and Bacteria Surviving Sanitation of Conveyor Belts of Meat Processing Plants

by Xianqin Yang, Hui Wang, Scott Hrycauk, Devin B. Holman and Tim C. Ells

Microorganisms 2023, 11(2), 421; https://doi.org/10.3390/microorganisms11020421 - 7 Feb 2023

Cited by 6 | Viewed by 2314

Abstract

Biofilm formation can lead to the persistence of Salmonella Typhimurium (ST) and E. coli O157:H7 (O157). This study investigated the impact of meat processing surface bacteria (MPB) on biofilm formation by O157 (non-biofilm former; NF) and ST (strong biofilm former; BF). MPB were recovered from the contacting surfaces (CS), non-contacting surfaces (NCS), and roller surfaces (RS) of a beef plant conveyor belt after sanitation. O157 and ST were co-inoculated with MPB (CO), or after a delay of 48 h (IS), into biofilm reactors containing stainless steel coupons and incubated at 15 °C for up to 144 h. Coupons were withdrawn at various intervals and analyzed by conventional plating and 16S rRNA gene amplicon sequencing. The total bacterial counts in biofilms reached approximately 6.5 log CFU/cm², regardless of MPB type or development mode. The mean counts for O157 and ST under equivalent conditions mostly did not differ (p > 0.05), except for the IS set at 50 h, where no O157 was recovered. O157 and ST were 1.6 ± 2.1% and 4.7 ± 5.0% (CO) and 1.1 ± 2.2% and 2.0 ± 2.8% (IS) of the final population. Pseudomonas dominated the MPB inocula and biofilms, regardless of MPB type or development mode. Whether or not a pathogen is deemed BF or NF in monoculture, its successful integration into complex multi-species biofilms ultimately depends on the presence of certain other residents within the biofilm. Full article

(This article belongs to the Special Issue Feature Papers in Microbial Biofilm Formation)

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13 pages, 2767 KiB

Open AccessArticle

VT-1161—A Tetrazole for Management of Mono- and Dual-Species Biofilms

by Angela Maione, Aldo Mileo, Stefano Pugliese, Antonietta Siciliano, Luigi Cirillo, Federica Carraturo, Elisabetta de Alteriis, Maria De Falco, Marco Guida and Emilia Galdiero

Microorganisms 2023, 11(2), 237; https://doi.org/10.3390/microorganisms11020237 - 17 Jan 2023

Cited by 4 | Viewed by 1732

Abstract

VT-1161 is a novel tetrazole antifungal agent with high specificity for fungal CYP51 (compared to human CYP enzymes) which has been proven to have fewer adverse effects and drug–drug interaction profiles due to fewer off-target inhibitors. In this study, we evaluated the anti-biofilm potential of VT-1161 against mono- and dual-species biofilms of Candida albicans, Klebsiella pneumoniae and Staphylococcus aureus. VT-1161 inhibited planktonic growth of all three strains, with an MIC value of 2 µg mL⁻¹ for C. albicans and 0.5 µg mL⁻¹ for K. pneumoniae and S. aureus, and killed 99.9% of the microbial populations, indicating a cytocidal action. Additionally, VT-1161 showed an excellent anti-biofilm action, since it inhibited mono-microbial biofilms by 80% at 0.5 µg mL⁻¹, and dual-species biofilms of C. albicans/K. pneumoniae and C. albicans/S. aureus by 90% at the same concentration. Additionally, the eradication of mature biofilms after 24 h of VT-1161 exposure was excellent, reaching 90% at 2 μg mL⁻¹ for both mono- and dual-species biofilms. In such mixed biofilms, the use of VT-1161 was revealed to be an alternative treatment because it was able to reduce the number of cells of each species during both inhibition and eradication. Since long-term therapy is necessary for most fungal biofilm infections due to their recurrence and obstinacy, VT-1161 showed low cytotoxicity against normal human cell lines and also against the invertebrate model Caenorhabditis elegans. Considering the excellent anti-biofilm potential and its GRAS (generally recognized as safe) status, VT-1161 may find use in the prevention or therapeutic treatment of mono- or poly-microbial biofilms. Full article

(This article belongs to the Special Issue Feature Papers in Microbial Biofilm Formation)

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12 pages, 2686 KiB

Open AccessArticle

Gre Factors Are Required for Biofilm Formation in Salmonella enterica Serovar Typhimurium by Targeting Transcription of the csgD Gene

by Tania Gaviria-Cantin, Andrés Felipe Vargas, Youssef El Mouali, Carlos Jonay Jiménez, Annika Cimdins-Ahne, Cristina Madrid, Ute Römling and Carlos Balsalobre

Microorganisms 2022, 10(10), 1921; https://doi.org/10.3390/microorganisms10101921 - 27 Sep 2022

Cited by 4 | Viewed by 2431

Abstract

Rdar biofilm formation of Salmonella typhimurium and Escherichia coli is a common ancient multicellular behavior relevant in cell–cell and inter-organism interactions equally, as in interaction with biotic and abiotic surfaces. With the expression of the characteristic extracellular matrix components amyloid curli fimbriae and the exopolysaccharide cellulose, the central hub for the delicate regulation of rdar morphotype expression is the orphan transcriptional regulator CsgD. Gre factors are ubiquitously interacting with RNA polymerase to selectively overcome transcriptional pausing. In this work, we found that GreA/GreB are required for expression of the csgD operon and consequently the rdar morphotype. The ability of the Gre factors to suppress transcriptional pausing and the 147 bp 5′-UTR of csgD are required for the stimulatory effect of the Gre factors on csgD expression. These novel mechanism(s) of regulation for the csgD operon might be relevant under specific stress conditions. Full article

(This article belongs to the Special Issue Feature Papers in Microbial Biofilm Formation)

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15 pages, 3129 KiB

Open AccessArticle

Effect of Myrtenol and Its Synergistic Interactions with Antimicrobial Drugs in the Inhibition of Single and Mixed Biofilms of Candida auris and Klebsiella pneumoniae

by Angela Maione, Alessandra La Pietra, Elisabetta de Alteriis, Aldo Mileo, Maria De Falco, Marco Guida and Emilia Galdiero

Microorganisms 2022, 10(9), 1773; https://doi.org/10.3390/microorganisms10091773 - 2 Sep 2022

Cited by 16 | Viewed by 2509

Abstract

The increased incidence of mixed infections requires that the scientific community develop novel antimicrobial molecules. Essential oils and their bioactive pure compounds have been found to exhibit a wide range of remarkable biological activities and are attracting more and more attention. Therefore, the aim of this study was to evaluate myrtenol (MYR), one of the constituents commonly found in some essential oils, for its potential to inhibit biofilms alone and in combination with antimicrobial drugs against Candida auris/Klebsiella pneumoniae single and mixed biofilms. The antimicrobial activity of MYR was evaluated by determining bactericidal/fungicidal concentrations (MIC), and biofilm formation at sub-MICs was analyzed in a 96-well microtiter plate by crystal violet, XTT reduction assay, and CFU counts. The synergistic interaction between MYR and antimicrobial drugs was evaluated by the checkerboard method. The study found that MYR exhibited antimicrobial activity at high concentrations while showing efficient antibiofilm activity against single and dual biofilms. To understand the underlying mechanism by which MYR promotes single/mixed-species biofilm inhibition, we observed a significant downregulation in the expression of mrkA, FKS1, ERG11, and ALS5 genes, which are associated with bacterial motility, adhesion, and biofilm formation as well as increased ROS production, which can play an important role in the inhibition of biofilm formation. In addition, the checkerboard microdilution assay showed that MYR was strongly synergistic with both caspofungin (CAS) and meropenem (MEM) in inhibiting the growth of Candida auris/Klebsiella pneumoniae-mixed biofilms. Furthermore, the tested concentrations showed an absence of toxicity for both mammalian cells in the in vitro and in vivo Galleria mellonella models. Thus, MYR could be considered as a potential agent for the management of polymicrobial biofilms. Full article

(This article belongs to the Special Issue Feature Papers in Microbial Biofilm Formation)

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16 pages, 2545 KiB

Open AccessArticle

Inhibition of In Vitro Clostridioides difficile Biofilm Formation by the Probiotic Yeast Saccharomyces boulardii CNCM I-745 through Modification of the Extracellular Matrix Composition

by Pierre-Alexandre Lacotte, Alexis Simons, Sylvie Bouttier, Jeanne Malet-Villemagne, Valérie Nicolas and Claire Janoir

Microorganisms 2022, 10(6), 1082; https://doi.org/10.3390/microorganisms10061082 - 24 May 2022

Cited by 12 | Viewed by 3203

Abstract

Clostridioides difficile is responsible for post-antibiotic diarrhea and most of the pseudomembranous colitis cases. Multiple recurrences, one of the major challenges faced in C. difficile infection (CDI) management, can be considered as chronic infections, and the role of biofilm formation in CDI recurrences is now widely considered. Therefore, we explored if the probiotic yeast Saccharomyces boulardii CNCM I-745 could impact the in vitro formation of C. difficile biofilm. Biomass staining and viable bacterial cell quantification showed that live S. boulardii exerts an antagonistic effect on the biofilm formation for the three C. difficile strains tested. Confocal laser scanning microscopy observation revealed a weakening and an average thickness reduction of the biofilm structure when C. difficile is co-incubated with S. boulardii, compared to the single-species bacterial biofilm structure. These effects, that were not detected with another genetically close yeast, S. cerevisiae, seemed to require direct contact between the probiotic yeast and the bacterium. Quantification of the extrapolymeric matrix components, as well as results obtained after DNase treatment, revealed a significant decrease of eDNA, an essential structural component of the C. difficile biofilm matrix, in the dual-species biofilm. This modification could explain the reduced cohesion and robustness of C. difficile biofilms formed in the presence of S. boulardii CNCM I-745 and be involved in S. boulardii clinical preventive effect against CDI recurrences. Full article

(This article belongs to the Special Issue Feature Papers in Microbial Biofilm Formation)

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Review

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21 pages, 3477 KiB

Open AccessReview

A Meta-Analysis of Bacterial Communities in Food Processing Facilities: Driving Forces for Assembly of Core and Accessory Microbiomes across Different Food Commodities

by Zhaohui S. Xu, Tingting Ju, Xianqin Yang and Michael Gänzle

Microorganisms 2023, 11(6), 1575; https://doi.org/10.3390/microorganisms11061575 - 14 Jun 2023

Cited by 14 | Viewed by 3301

Abstract

Microbial spoilage is a major cause of food waste. Microbial spoilage is dependent on the contamination of food from the raw materials or from microbial communities residing in food processing facilities, often as bacterial biofilms. However, limited research has been conducted on the persistence of non-pathogenic spoilage communities in food processing facilities, or whether the bacterial communities differ among food commodities and vary with nutrient availability. To address these gaps, this review re-analyzed data from 39 studies from various food facilities processing cheese (n = 8), fresh meat (n = 16), seafood (n = 7), fresh produce (n = 5) and ready-to-eat products (RTE; n = 3). A core surface-associated microbiome was identified across all food commodities, including Pseudomonas, Acinetobacter, Staphylococcus, Psychrobacter, Stenotrophomonas, Serratia and Microbacterium. Commodity-specific communities were additionally present in all food commodities except RTE foods. The nutrient level on food environment surfaces overall tended to impact the composition of the bacterial community, especially when comparing high-nutrient food contact surfaces to floors with an unknown nutrient level. In addition, the compositions of bacterial communities in biofilms residing in high-nutrient surfaces were significantly different from those of low-nutrient surfaces. Collectively, these findings contribute to a better understanding of the microbial ecology of food processing environments, the development of targeted antimicrobial interventions and ultimately the reduction of food waste and food insecurity and the promotion of food sustainability. Full article

(This article belongs to the Special Issue Feature Papers in Microbial Biofilm Formation)

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17 pages, 2716 KiB

Open AccessReview

Clinical Escherichia coli: From Biofilm Formation to New Antibiofilm Strategies

by Victoria Ballén, Virginio Cepas, Carlos Ratia, Yaiza Gabasa and Sara M. Soto

Microorganisms 2022, 10(6), 1103; https://doi.org/10.3390/microorganisms10061103 - 26 May 2022

Cited by 37 | Viewed by 8741

Abstract

Escherichia coli is one of the species most frequently involved in biofilm-related diseases, being especially important in urinary tract infections, causing relapses or chronic infections. Compared to their planktonic analogues, biofilms confer to the bacteria the capacity to be up to 1000-fold more resistant to antibiotics and to evade the action of the host’s immune system. For this reason, biofilm-related infections are very difficult to treat. To develop new strategies against biofilms, it is important to know the mechanisms involved in their formation. In this review, the different steps of biofilm formation in E. coli, the mechanisms of tolerance to antimicrobials and new compounds and strategies to combat biofilms are discussed. Full article

(This article belongs to the Special Issue Feature Papers in Microbial Biofilm Formation)

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