Microbial Biofilms: Structural Plasticity and Emerging Properties

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

Deadline for manuscript submissions: closed (15 December 2022) | Viewed by 23073

Special Issue Editors


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Guest Editor
French National Research Institute for Agriculture, Food and Environment (INRAE), Paris, France
Interests: biofilm; 3D; spatial interactions; food borne-pathogens; persistence; biocide tolerance; protective biofilms; fluorescence imaging

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Guest Editor
ANSES, Fougères Laboratory, AB2R unit, Fougères, France
Interests: biofilms; biocides; antibioresistance; cross-resistance; stress adaptation; foodborne pathogen; microbial ecology; WGS; metagenomics

Special Issue Information

Dear Colleagues,

Microbial biofilms are found everywhere and can be either beneficial or detrimental, as they are involved in crucial ecological processes as well as in severe chronic infections. The functional properties of biofilms are intimately related to their three-dimensional (3D) structure and the ability of microorganisms to collectively and dynamically shape the community spatial organisation in response to stresses in such biological edifices. Numerous works have shown that the modulation of the spatial organization of biofilms and of species interactions under environmental fluctuations are related to emerging properties essential for nutrient cycling and bioremediation processes in natural environments. On the opposite, a large number of studies have emphasized the role of structural rearrangements and matrix production in the increased tolerance of bacteria in biofilms toward antimicrobials.

In these last years, the development of innovative approaches, relying on recent technological advances in imaging, sequencing and other analytical tools, has led to the production of original data that have improved our understanding of this close relationship. However, it has also highlighted the need to go further in the study of cell behavior in such complex and dynamic communities during biofilm structure development and maturation— from a single-cell to a multicellular scale—in order to better control or harness positive and negative impacts of biofilms.

For this Special Issue of Microorganisms, we invite you to send contributions concerning any aspects related to the interplay between biofilm emerging properties and their 3D spatial organisation considering different models, from single bacteria to complex environmental communities, and various environments, from natural ecosystems to industrial and medical settings.

Dr. Romain Briandet
Dr. Arnaud Bridier
Guest Editors

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Keywords

  • Biofilm
  • spatial organization
  • structural dynamics
  • microenvironments
  • ecological interactions
  • collective adaptation
  • single cell and local analysis
  • subpopulation and local response to the action of antimicrobials

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Published Papers (7 papers)

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Editorial

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5 pages, 209 KiB  
Editorial
Microbial Biofilms: Structural Plasticity and Emerging Properties
by Arnaud Bridier and Romain Briandet
Microorganisms 2022, 10(1), 138; https://doi.org/10.3390/microorganisms10010138 - 10 Jan 2022
Cited by 12 | Viewed by 2439
Abstract
Microbial biofilms are found everywhere and can be either beneficial or detrimental, as they are involved in crucial ecological processes and in severe chronic infections. The functional properties of biofilms are closely related to their three-dimensional (3D) structure, and the ability of microorganisms [...] Read more.
Microbial biofilms are found everywhere and can be either beneficial or detrimental, as they are involved in crucial ecological processes and in severe chronic infections. The functional properties of biofilms are closely related to their three-dimensional (3D) structure, and the ability of microorganisms to collectively and dynamically shape the community spatial organization in response to stresses in such biological edifices. A large number of works have shown a relationship between the modulation of the spatial organization and ecological interactions in biofilms in response to environmental fluctuations, as well as their emerging properties essential for nutrient cycling and bioremediation processes in natural environments. On the contrary, numerous studies have emphasized the role of structural rearrangements and matrix production in the increased tolerance of bacteria in biofilms toward antimicrobials. In these last few years, the development of innovative approaches, relying on recent technological advances in imaging, computing capacity, and other analytical tools, has led to the production of original data that have improved our understanding of this close relationship. However, it has also highlighted the need to delve deeper into the study of cell behavior in such complex communities during 3D structure development and maturation— from a single-cell to a multicellular scale— to better control or harness positive and negative impacts of biofilms. For this Special Issue, the interplay between biofilm emerging properties and their 3D spatial organization considering different models, from single bacteria to complex environmental communities, and various environments, from natural ecosystems to industrial and medical settings are addressed. Full article
(This article belongs to the Special Issue Microbial Biofilms: Structural Plasticity and Emerging Properties)

Research

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13 pages, 1988 KiB  
Article
Exploring the Diversity of Biofilm Formation by the Food Spoiler Brochothrix thermosphacta
by Antoine Gaillac, Romain Briandet, Elodie Delahaye, Julien Deschamps, Evelyne Vigneau, Philippe Courcoux, Emmanuel Jaffrès and Hervé Prévost
Microorganisms 2022, 10(12), 2474; https://doi.org/10.3390/microorganisms10122474 - 15 Dec 2022
Cited by 8 | Viewed by 2661
Abstract
Brochothrix thermosphacta is considered as a major spoiler of meat and seafood products. This study explores the biofilm formation ability and the biofilm structural diversity of 30 multi-origin B. thermosphacta strains using a set of complementary biofilm assays (biofilm ring test, crystal violet [...] Read more.
Brochothrix thermosphacta is considered as a major spoiler of meat and seafood products. This study explores the biofilm formation ability and the biofilm structural diversity of 30 multi-origin B. thermosphacta strains using a set of complementary biofilm assays (biofilm ring test, crystal violet staining, and confocal laser scanning microscopy). Two major groups corresponding to low and high biofilm producers were identified. High biofilm producers presented flat architectures characterized by high surface coverage, high cell biovolume, and high surface area. Full article
(This article belongs to the Special Issue Microbial Biofilms: Structural Plasticity and Emerging Properties)
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15 pages, 1833 KiB  
Article
Impact of Fe2+ and Shear Stress on the Development and Mesoscopic Structure of Biofilms—A Bacillus subtilis Case Study
by Luisa Gierl, Harald Horn and Michael Wagner
Microorganisms 2022, 10(11), 2234; https://doi.org/10.3390/microorganisms10112234 - 11 Nov 2022
Cited by 4 | Viewed by 1739
Abstract
Bivalent cations are known to affect the structural and mechanical properties of biofilms. In order to reveal the impact of Fe2+ ions within the cultivation medium on biofilm development, structure and stability, Bacillus subtilis biofilms were cultivated in mini-fluidic flow cells. Two [...] Read more.
Bivalent cations are known to affect the structural and mechanical properties of biofilms. In order to reveal the impact of Fe2+ ions within the cultivation medium on biofilm development, structure and stability, Bacillus subtilis biofilms were cultivated in mini-fluidic flow cells. Two different Fe2+ inflow concentrations (0.25 and 2.5 mg/L, respectively) and wall shear stress levels (0.05 and 0.27 Pa, respectively) were tested. Mesoscopic biofilm structure was determined daily in situ and non-invasively by means of optical coherence tomography. A set of ten structural parameters was used to quantify biofilm structure, its development and change. The study focused on characterizing biofilm structure and development at the mesoscale (mm-range). Therefore, biofilm replicates (n = 10) were cultivated and analyzed. Three hypotheses were defined in order to estimate the effect of Fe2+ inflow concentration and/or wall shear stress on biofilm development and structure, respectively. It was not the intention to investigate and describe the underlying mechanisms of iron incorporation as this would require a different set of tools applied at microscopic levels as well as the use of, i.e., omic approaches. Fe2+ addition influenced biofilm development (e.g., biofilm accumulation) and structure markedly. Experiments revealed the accumulation of FeO(OH) within the biofilm matrix and a positive correlation of Fe2+ inflow concentration and biofilm accumulation. In more detail, independent of the wall shear stress applied during cultivation, biofilms grew approximately four times thicker at 2.5 mg Fe2+/L (44.8 µmol/L; high inflow concentration) compared to the low Fe2+ inflow concentration of 0.25 mg Fe2+/L (4.48 µmol/L). This finding was statistically verified (Scheirer–Ray–Hare test, ANOVA) and hints at a higher stability of Bacillus subtilis biofilms (e.g., elevated cohesive and adhesive strength) when grown at elevated Fe2+ inflow concentrations. Full article
(This article belongs to the Special Issue Microbial Biofilms: Structural Plasticity and Emerging Properties)
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12 pages, 2463 KiB  
Article
Capture and Ex-Situ Analysis of Environmental Biofilms in Livestock Buildings
by Virgile Guéneau, Ana Rodiles, Jean-Christophe Piard, Bastien Frayssinet, Mathieu Castex, Julia Plateau-Gonthier and Romain Briandet
Microorganisms 2022, 10(1), 2; https://doi.org/10.3390/microorganisms10010002 - 21 Dec 2021
Cited by 6 | Viewed by 3894
Abstract
Little information about biofilm microbial communities on the surface of livestock buildings is available yet. While these spatially organized communities proliferate in close contact with animals and can harbor undesirable microorganisms, no standardized methods have been described to sample them non-destructively. We propose [...] Read more.
Little information about biofilm microbial communities on the surface of livestock buildings is available yet. While these spatially organized communities proliferate in close contact with animals and can harbor undesirable microorganisms, no standardized methods have been described to sample them non-destructively. We propose a reproducible coupon-based capture method associated with a set of complementary ex-situ analysis tools to describe the major features of those communities. To demonstrate the biofilm dynamics in a pig farm building, we analyzed the coupons on polymeric and metallic materials, as representative of these environments, over 4 weeks. Confocal laser scanning microscopy (CLSM) revealed a rapid coverage of the coupons with a thick layer of biological material and the existence of dispersed clusters of active metabolic microorganisms. After detaching the cells from the coupons, counts to quantify the CFU/cm2 were done with high reproducibility. High-throughput sequencing of the 16S rRNA V3-V4 region shows bacterial diversity profiles in accordance with reported bacteria diversity in pig intestinal ecosystems and reveals differences between materials. The coupon-based methodology allows us to deepen our knowledge on biofilm structure and composition on the surface of a pig farm and opens the door for application in different types of livestock buildings. Full article
(This article belongs to the Special Issue Microbial Biofilms: Structural Plasticity and Emerging Properties)
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14 pages, 1481 KiB  
Article
Insights into the Development of Phototrophic Biofilms in a Bioreactor by a Combination of X-ray Microtomography and Optical Coherence Tomography
by Susanne Schaefer, Jakob Walther, Dorina Strieth, Roland Ulber and Ulrich Bröckel
Microorganisms 2021, 9(8), 1743; https://doi.org/10.3390/microorganisms9081743 - 16 Aug 2021
Cited by 7 | Viewed by 2708
Abstract
As productive biofilms are increasingly gaining interest in research, the quantitative monitoring of biofilm formation on- or offline for the process remains a challenge. Optical coherence tomography (OCT) is a fast and often used method for scanning biofilms, but it has difficulty scanning [...] Read more.
As productive biofilms are increasingly gaining interest in research, the quantitative monitoring of biofilm formation on- or offline for the process remains a challenge. Optical coherence tomography (OCT) is a fast and often used method for scanning biofilms, but it has difficulty scanning through more dense optical materials. X-ray microtomography (μCT) can measure biofilms in most geometries but is very time-consuming. By combining both methods for the first time, the weaknesses of both methods could be compensated. The phototrophic cyanobacterium Tolypothrix distorta was cultured in a moving bed photobioreactor inside a biocarrier with a semi-enclosed geometry. An automated workflow was developed to process µCT scans of the biocarriers. This allowed quantification of biomass volume and biofilm-coverage on the biocarrier, both globally and spatially resolved. At the beginning of the cultivation, a growth limitation was detected in the outer region of the carrier, presumably due to shear stress. In the later phase, light limitations could be found inside the biocarrier. µCT data and biofilm thicknesses measured by OCT displayed good correlation. The latter could therefore be used to rapidly measure the biofilm formation in a process. The methods presented here can help gain a deeper understanding of biofilms inside a process and detect any limitations. Full article
(This article belongs to the Special Issue Microbial Biofilms: Structural Plasticity and Emerging Properties)
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10 pages, 1922 KiB  
Article
Massive Integration of Planktonic Cells within a Developing Biofilm
by Nay El-Khoury, Imene Bennaceur, Emilie Verplaetse, Stéphane Aymerich, Didier Lereclus, Mireille Kallassy and Michel Gohar
Microorganisms 2021, 9(2), 298; https://doi.org/10.3390/microorganisms9020298 - 2 Feb 2021
Cited by 2 | Viewed by 3536
Abstract
During biofilm growth, the coexistence of planktonic and sessile cells can lead to dynamic exchanges between the two populations. We have monitored the fate of these populations in glass tube assays, where the Bacillus thuringiensis 407 strain produces a floating pellicle. Time-lapse spectrophotometric [...] Read more.
During biofilm growth, the coexistence of planktonic and sessile cells can lead to dynamic exchanges between the two populations. We have monitored the fate of these populations in glass tube assays, where the Bacillus thuringiensis 407 strain produces a floating pellicle. Time-lapse spectrophotometric measurement methods revealed that the planktonic population grew until the pellicle started to be produced. Thereafter, the planktonic population decreased rapidly down to a value close to zero while the biofilm was in continuous growth, showing no dispersal until 120 h of culture. We found that this decrease was induced by the presence of the pellicle, but did not occur when oxygen availability was limited, suggesting that it was independent of cell death or cell sedimentation and that the entire planktonic population has integrated the biofilm. To follow the distribution of recruited planktonic cells within the pellicle, we tagged planktonic cells with GFP and sessile cells with mCherry. Fluorescence binocular microscopy observations revealed that planktonic cells, injected through a 24-h-aged pellicle, were found only in specific areas of the biofilm, where the density of sessile cells was low, showing that spatial heterogeneity can occur between recruited cells and sessile cells in a monospecies biofilm. Full article
(This article belongs to the Special Issue Microbial Biofilms: Structural Plasticity and Emerging Properties)
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Review

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36 pages, 3359 KiB  
Review
Wolf in Sheep’s Clothing: Clostridioides difficile Biofilm as a Reservoir for Recurrent Infections
by Jazmin Meza-Torres, Emile Auria, Bruno Dupuy and Yannick D. N. Tremblay
Microorganisms 2021, 9(9), 1922; https://doi.org/10.3390/microorganisms9091922 - 10 Sep 2021
Cited by 18 | Viewed by 4616
Abstract
The microbiota inhabiting the intestinal tract provide several critical functions to its host. Microorganisms found at the mucosal layer form organized three-dimensional structures which are considered to be biofilms. Their development and functions are influenced by host factors, host-microbe interactions, and microbe-microbe interactions. [...] Read more.
The microbiota inhabiting the intestinal tract provide several critical functions to its host. Microorganisms found at the mucosal layer form organized three-dimensional structures which are considered to be biofilms. Their development and functions are influenced by host factors, host-microbe interactions, and microbe-microbe interactions. These structures can dictate the health of their host by strengthening the natural defenses of the gut epithelium or cause disease by exacerbating underlying conditions. Biofilm communities can also block the establishment of pathogens and prevent infectious diseases. Although these biofilms are important for colonization resistance, new data provide evidence that gut biofilms can act as a reservoir for pathogens such as Clostridioides difficile. In this review, we will look at the biofilms of the intestinal tract, their contribution to health and disease, and the factors influencing their formation. We will then focus on the factors contributing to biofilm formation in C. difficile, how these biofilms are formed, and their properties. In the last section, we will look at how the gut microbiota and the gut biofilm influence C. difficile biofilm formation, persistence, and transmission. Full article
(This article belongs to the Special Issue Microbial Biofilms: Structural Plasticity and Emerging Properties)
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