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Current and New Knowledge of Biofilm Formation by Staphylococci

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Microbiology".

Deadline for manuscript submissions: closed (30 October 2022) | Viewed by 16920

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Special Issue Editor

Dr. Catherine Dunyach-Remy

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Guest Editor

Bacterial Virulence and Chronic Infections, INSERM U1047, Department of Microbiology and Hospital Hygiene, Hospital of Nîmes, University of Montpellier, Nîmes, France
Interests: chronic wounds; bacterial interactions; bacterial biofilm

Special Issue Information

Dear Colleagues,

Biofilm formation is a multistep process whereby heterogeneous communities of microorganisms are embedded into a self-produced matrix of an extracellular polymeric substance. Biofilms are found in various clinical environments, including urinary catheters and indwelling medical devices; however, it is more frequently described in chronic infections (e.g., chronic wound infection, endocarditis osteomyelitis, cystic fibrosis, etc.). Thus, biofilms constitute a significant public health problem.

Among the different bacterial species, staphylococci are recognized as one of the most common causes of biofilm-associated infections. The molecular basis of biofilm formation in staphylococci is now well-established and this process plays an important role in the pathogenicity and persistence of these microorganisms. Recently, in some medical biofilms, staphylococci were mixed with other bacterial species within biofilm-associated infections, constituting a polymicrobial biofilm. The proximity of these bacterial species within the biofilm promotes bacterial interactions that play an important role in the chronicity of infections.

Finally, sessile cells involved in biofilms harbor a higher tolerance towards antimicrobial agents and are able to transfer resistance traits among all embedded bacteria, representing a cause of treatment failure and favoring the emergence and diffusion of antibiotic resistance.

This Special Issue aims to explore both the existing and latest knowledge on the pathogenesis and therapeutic management of Staphylococci biofilm-related infections. The presentation of innovative therapeutic strategies and methods to assess biofilm formation will form the analytical basis of this Special Issue.

This Special Issue is accepting research articles and review articles that focus on the following aspects of Staphylococci biofilms:

The existing and latest knowledge on biofilm formation by Staphylococci (bacterial interactions in biofilm, metabolism of released Staphylococci from biofilm, regulation of biofilm formation…);
The antibiotic resistance/tolerance in Staphylococci biofilm-related infections;
The contribution Staphylococci microbial biofilms in chronic infections;
The role of the host's immune system in Staphylococci biofilm-related infections;
New technologies to evaluate and analyze biofilm formation by Staphylococci
New therapeutic strategies against Staphylococci biofilm

Dr. Catherine Dunyach-Remy
Guest Editor

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. International Journal of Molecular Sciences is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. There is an Article Processing Charge (APC) for publication in this open access journal. For details about the APC please see here. 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

staphylococci
biofilm
bacterial interactions
chronic infections
medical devices-associated infections
biofilm management

Published Papers (7 papers)

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Research

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16 pages, 1849 KiB

Open AccessArticle

Effect of Antibiotic Exposure on Staphylococcus epidermidis Responsible for Catheter-Related Bacteremia

by Cassandra Pouget, Clotilde Chatre, Jean-Philippe Lavigne, Alix Pantel, Jacques Reynes and Catherine Dunyach-Remy

Int. J. Mol. Sci. 2023, 24(2), 1547; https://doi.org/10.3390/ijms24021547 - 12 Jan 2023

Cited by 6 | Viewed by 2149

Abstract

Coagulase-negative staphylococci (CoNS) and especially Staphylococcus epidermidis are responsible for health care infections, notably in the presence of foreign material (e.g., venous or central-line catheters). Catheter-related bacteremia (CRB) increases health care costs and mortality. The aim of our study was to evaluate the impact of 15 days of antibiotic exposure (ceftobiprole, daptomycin, linezolid and vancomycin) at sub-inhibitory concentration on the resistance, fitness and genome evolution of 36 clinical strains of S. epidermidis responsible for CRB. Resistance was evaluated by antibiogram, the ability to adapt metabolism by the Biofilm Ring test^® and the in vivo nematode virulence model. The impact of antibiotic exposure was determined by whole-genome sequencing (WGS) and biofilm formation experiments. We observed that S. epidermidis strains presented a wide variety of virulence potential and biofilm formation. After antibiotic exposure, S. epidermidis strains adapted their fitness with an increase in biofilm formation. Antibiotic exposure also affected genes involved in resistance and was responsible for cross-resistance between vancomycin, daptomycin and ceftobiprole. Our data confirmed that antibiotic exposure modified bacterial pathogenicity and the emergence of resistant bacteria. Full article

(This article belongs to the Special Issue Current and New Knowledge of Biofilm Formation by Staphylococci)

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20 pages, 2441 KiB

Open AccessArticle

Phenotypic and Genotypic Virulence Characterisation of Staphylococcus pettenkoferi Strains Isolated from Human Bloodstream and Diabetic Foot Infections

by Chloé Magnan, Nour Ahmad-Mansour, Cassandra Pouget, Madjid Morsli, Sylvaine Huc-Brandt, Alix Pantel, Catherine Dunyach-Remy, Albert Sotto, Virginie Molle and Jean-Philippe Lavigne

Int. J. Mol. Sci. 2022, 23(24), 15476; https://doi.org/10.3390/ijms232415476 - 7 Dec 2022

Cited by 2 | Viewed by 1516

Abstract

Staphylococcus pettenkoferi is a recently described coagulase-negative Staphylococcus identified in human diseases, especially in infections of foot ulcers in patients living with diabetes mellitus. To date, its pathogenicity remains underexplored. In this study, whole-genome analysis was performed on a collection of 29 S. pettenkoferi clinical strains isolated from bloodstream and diabetic foot infections with regard to their phylogenetic relationships and comprehensive analysis of their resistome and virulome. Their virulence was explored by their ability to form biofilm, their growth kinetics and in an in vivo zebrafish embryo infection model. Our results identified two distinct clades (I and II) and two subclades (I-a and I-b) with notable genomic differences. All strains had a slow bacterial growth. Three profiles of biofilm formation were noted, with 89.7% of isolates able to produce biofilm and harbouring a high content of biofilm-encoding genes. Two virulence profiles were also observed in the zebrafish model irrespective of the strains’ origin or biofilm profile. Therefore, this study brings new insights in S. pettenkoferi pathogenicity. Full article

(This article belongs to the Special Issue Current and New Knowledge of Biofilm Formation by Staphylococci)

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14 pages, 2462 KiB

Open AccessArticle

Polymicrobial Biofilm Organization of Staphylococcus aureus and Pseudomonas aeruginosa in a Chronic Wound Environment

by Cassandra Pouget, Catherine Dunyach-Remy, Chloé Magnan, Alix Pantel, Albert Sotto and Jean-Philippe Lavigne

Int. J. Mol. Sci. 2022, 23(18), 10761; https://doi.org/10.3390/ijms231810761 - 15 Sep 2022

Cited by 9 | Viewed by 2016

Abstract

Biofilm on the skin surface of chronic wounds is an important step that involves difficulties in wound healing. The polymicrobial nature inside this pathogenic biofilm is key to understanding the chronicity of the lesion. Few in vitro models have been developed to study bacterial interactions inside this chronic wound. We evaluated the biofilm formation and the evolution of bacteria released from this biofilm on the two main bacteria isolated in this condition, Staphylococcus aureus and Pseudomonas aeruginosa, using a dynamic system (BioFlux™ 200) and a chronic wound-like medium (CWM) that mimics the chronic wound environment. We observed that all species constituted a faster biofilm in the CWM compared to a traditional culture medium (p < 0.01). The percentages of biofilm formation were significantly higher in the mixed biofilm compared to those determined for the bacterial species alone (p < 0.01). Biofilm organization was a non-random structure where S. aureus aggregates were located close to the wound surface, whereas P. aeruginosa was located deeper in the wound bed. Planktonic biofilm-detached bacteria showed decreased growth, overexpression of genes encoding biofilm formation, and an increase in the mature biofilm biomass formed. Our data confirmed the impact of the chronic wound environment on biofilm formation and on bacterial lifecycle inside the biofilm. Full article

(This article belongs to the Special Issue Current and New Knowledge of Biofilm Formation by Staphylococci)

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13 pages, 2335 KiB

Open AccessArticle

A Combination of the Natural Molecules Gallic Acid and Carvacrol Eradicates P. aeruginosa and S. aureus Mature Biofilms

by Maxime Gobin, Richard Proust, Stéphane Lack, Laura Duciel, Céline Des Courtils, Emmanuel Pauthe, Adeline Gand and Damien Seyer

Int. J. Mol. Sci. 2022, 23(13), 7118; https://doi.org/10.3390/ijms23137118 - 27 Jun 2022

Cited by 8 | Viewed by 2096

Abstract

Wound infection, especially the development of bacterial biofilms, delays wound healing and is a major public health concern. Bacteria in biofilms are more tolerant to antimicrobial agents, and new treatments to eradicate mature biofilms are needed. Combining antimicrobial molecules with different mechanisms of action is an attractive strategy to tackle the heterogeneous nature of microbial communities in biofilms. This study focused on three molecules of natural origin: gallic acid (G), carvacrol (K) and curcumin (Q). Their abilities, individually or in combination, to eradicate biofilms were quantified on mono- and dual-species mature biofilms of Pseudomonas aeruginosa and Staphylococcus aureus, the strains most commonly found in infected wounds. G presented biofilm eradicating activity on P. aeruginosa, whereas K had biofilm eradicating activity on S. aureus and P. aeruginosa. Q had no potent biofilm eradicating activity. The combination of G and K increased the effects previously observed on P. aeruginosa biofilm and led to complete eradication of S. aureus biofilm. This combination was also efficient in eradicating a dual-species biofilm of S. aureus and P. aeruginosa. This work demonstrates that K and G used in combination have a strong and synergistic eradicating activity on both mono- and dual-species mature biofilms of S. aureus and P. aeruginosa and may therefore represent an efficient alternative for the treatment of biofilms in wounds. Full article

(This article belongs to the Special Issue Current and New Knowledge of Biofilm Formation by Staphylococci)

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12 pages, 1160 KiB

Open AccessArticle

May Staphylococcus lugdunensis Be an Etiological Factor of Chronic Maxillary Sinuses Infection?

by Maja Kosecka-Strojek, Mariola Wolska-Gębarzewska, Adrianna Podbielska-Kubera, Alfred Samet, Beata Krawczyk, Jacek Międzobrodzki and Michał Michalik

Int. J. Mol. Sci. 2022, 23(12), 6450; https://doi.org/10.3390/ijms23126450 - 9 Jun 2022

Cited by 2 | Viewed by 2351

Abstract

Staphylococcus lugdunensis is an opportunistic pathogen found in the healthy human skin microbiome bacterial community that is able to cause infections of diverse localization, manifestation, and course, including laryngological infections, such as necrotizing sinusitis. Chronic maxillary sinusitis is a disease present in up to one third of European and American populations, and its etiology is not fully described. Within this study, we aimed to characterize 18 S. lugdunensis strains recovered from maxillary sinuses and evaluate them as etiological agents of chronic disease. We performed MLST analysis, the complex analysis of both phenotypic and genetic virulence factors, antibiotic susceptibility profiles, and biofilm formation assay for the detection of biofilm-associated genes. Altogether, S. lugdunensis strains were clustered into eight different STs, and we demonstrated several virulence factors associated with the chronic disease. All tested strains were able to produce biofilm in vitro with numerous strains with a very strong ability, and overall, they were mostly susceptible to antibiotics, although we found resistance to fosfomycin, erythromycin, and clindamycin in several strains. We believe that further in-depth analysis of S. lugdunensis strains from different niches, including the nasal one, should be performed in the future in order to reduce infection rate and broaden the knowledge about this opportunistic pathogen that is gaining attention. Full article

(This article belongs to the Special Issue Current and New Knowledge of Biofilm Formation by Staphylococci)

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Review

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19 pages, 1928 KiB

Open AccessReview

Biology and Regulation of Staphylococcal Biofilm

by Patrice François, Jacques Schrenzel and Friedrich Götz

Int. J. Mol. Sci. 2023, 24(6), 5218; https://doi.org/10.3390/ijms24065218 - 9 Mar 2023

Cited by 5 | Viewed by 2376

Abstract

Despite continuing progress in medical and surgical procedures, staphylococci remain the major Gram-positive bacterial pathogens that cause a wide spectrum of diseases, especially in patients requiring the utilization of indwelling catheters and prosthetic devices implanted temporarily or for prolonged periods of time. Within the genus, if Staphylococcus aureus and S. epidermidis are prevalent species responsible for infections, several coagulase-negative species which are normal components of our microflora also constitute opportunistic pathogens that are able to infect patients. In such a clinical context, staphylococci producing biofilms show an increased resistance to antimicrobials and host immune defenses. Although the biochemical composition of the biofilm matrix has been extensively studied, the regulation of biofilm formation and the factors contributing to its stability and release are currently still being discovered. This review presents and discusses the composition and some regulation elements of biofilm development and describes its clinical importance. Finally, we summarize the numerous and various recent studies that address attempts to destroy an already-formed biofilm within the clinical context as a potential therapeutic strategy to avoid the removal of infected implant material, a critical event for patient convenience and health care costs. Full article

(This article belongs to the Special Issue Current and New Knowledge of Biofilm Formation by Staphylococci)

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28 pages, 3488 KiB

Open AccessReview

Biofilm Formation by Staphylococcus aureus in the Specific Context of Cystic Fibrosis

by Vincent Jean-Pierre, Agathe Boudet, Pauline Sorlin, Quentin Menetrey, Raphaël Chiron, Jean-Philippe Lavigne and Hélène Marchandin

Int. J. Mol. Sci. 2023, 24(1), 597; https://doi.org/10.3390/ijms24010597 - 29 Dec 2022

Cited by 10 | Viewed by 3567

Abstract

Staphylococcus aureus is a major human pathogen whose characteristics support its success in various clinical settings including Cystic Fibrosis (CF). In CF, S. aureus is indeed the most commonly identified opportunistic pathogen in children and the overall population. S. aureus colonization/infection, either by methicillin-susceptible or methicillin-resistant strains, will become chronic in about one third of CF patients. The persistence of S. aureus in CF patients’ lungs, despite various eradication strategies, is favored by several traits in both host and pathogen. Among the latter, living in biofilm is a highly protective way to survive despite deleterious environmental conditions, and is a common characteristic shared by the main pathogens identified in CF. This is why CF has earned the status of a biofilm-associated disease for several years now. Biofilm formation by S. aureus, and the molecular mechanisms governing and regulating it, have been extensively studied but have received less attention in the specific context of CF lungs. Here, we review the current knowledge on S. aureus biofilm in this very context, i.e., the importance, study methods, molecular data published on mono- and multi-species biofilm and anti-biofilm strategies. This focus on studies including clinical isolates from CF patients shows that they are still under-represented in the literature compared with studies based on reference strains, and underlines the need for such studies. Indeed, CF clinical strains display specific characteristics that may not be extrapolated from results obtained on laboratory strains. Full article

(This article belongs to the Special Issue Current and New Knowledge of Biofilm Formation by Staphylococci)

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