Effect of Micro- and Nanoscale Topography on the Adhesion of Bacterial Cells to Solid Surfaces

ABSTRACTAttachment and biofilm formation by bacterial pathogens on surfaces in natural, industrial, and hospital settings lead to infections and illnesses and even death. Minimizing bacterial attachment to surfaces using controlled topography could reduce the spreading of pathogens and, thus, the incidence of illnesses and subsequent human and financial losses. In this context, the attachment of key microorganisms, includingEscherichia coli,Listeria innocua, andPseudomonas fluorescens, to silica and alumina surfaces with micron and nanoscale topography was investigated. The results suggest that orientation of the attached cells occurs preferentially such as to maximize their contact area with the surface. Moreover, the bacterial cells exhibited different morphologies, including different number and size of cellular appendages, depending on the topographical details of the surface to which they attached. This suggests that bacteria may utilize different mechanisms of attachment in response to surface topography. These results are important for the design of novel microbe-repellant materials.

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PBP4 and PBP5 are involved in regulating exopolysaccharide synthesis during Escherichia coli biofilm formation

Microbiology ◽

10.1099/mic.0.001031 ◽

2021 ◽

Vol 167 (3) ◽

Author(s):

Sathi Mallick ◽

Shanti Kiran ◽

Tapas Kumar Maiti ◽

Anindya S. Ghosh

Keyword(s):

Escherichia Coli ◽

Biofilm Formation ◽

Type Species ◽

Pentose Phosphate ◽

Bacterial Cells ◽

Surface Adhesion ◽

Content Type ◽

Penicillin Binding Proteins ◽

E Coli ◽

Link Type

Escherichia coli low-molecular-mass (LMM) Penicillin-binding proteins (PBPs) help in hydrolysing the peptidoglycan fragments from their cell wall and recycling them back into the growing peptidoglycan matrix, in addition to their reported involvement in biofilm formation. Biofilms are external slime layers of extra-polymeric substances that sessile bacterial cells secrete to form a habitable niche for themselves. Here, we hypothesize the involvement of Escherichia coli LMM PBPs in regulating the nature of exopolysaccharides (EPS) prevailing in its extra-polymeric substances during biofilm formation. Therefore, this study includes the assessment of physiological characteristics of E. coli CS109 LMM PBP deletion mutants to address biofilm formation abilities, viability and surface adhesion. Finally, EPS from parent CS109 and its ΔPBP4 and ΔPBP5 mutants were purified and analysed for sugars present. Deletions of LMM PBP reduced biofilm formation, bacterial adhesion and their viability in biofilms. Deletions also diminished EPS production by ΔPBP4 and ΔPBP5 mutants, purification of which suggested an increased overall negative charge compared with their parent. Also, EPS analyses from both mutants revealed the appearance of an unusual sugar, xylose, that was absent in CS109. Accordingly, the reason for reduced biofilm formation in LMM PBP mutants may be speculated as the subsequent production of xylitol and a hindrance in the standard flow of the pentose phosphate pathway.

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Multiple Drug-Induced Stress Responses Inhibit Formation of Escherichia coli Biofilms

Applied and Environmental Microbiology ◽

10.1128/aem.01113-20 ◽

2020 ◽

Vol 86 (21) ◽

Cited By ~ 1

Author(s):

Nataliya A. Teteneva ◽

Sergey V. Mart’yanov ◽

María Esteban-López ◽

Jörg Kahnt ◽

Timo Glatter ◽

...

Keyword(s):

Escherichia Coli ◽

Stress Responses ◽

Biofilm Formation ◽

Molecular Mechanisms ◽

Drug Repurposing ◽

Bacterial Attachment ◽

Bacterial Biofilm ◽

Multiple Drug ◽

Content Type ◽

Approved Drugs

ABSTRACT In most ecosystems, bacteria exist primarily as structured surface-associated biofilms that can be highly tolerant to antibiotics and thus represent an important health issue. Here, we explored drug repurposing as a strategy to identify new antibiofilm compounds, screening over 1,000 compounds from the Prestwick Chemical Library of approved drugs for specific activities that prevent biofilm formation by Escherichia coli. Most growth-inhibiting compounds, which include known antibacterial but also antiviral and other drugs, also reduced biofilm formation. However, we also identified several drugs that were biofilm inhibitory at doses where only a weak effect or no effect on planktonic growth could be observed. The activities of the most specific antibiofilm compounds were further characterized using gene expression analysis, proteomics, and microscopy. We observed that most of these drugs acted by repressing genes responsible for the production of curli, a major component of the E. coli biofilm matrix. This repression apparently occurred through the induction of several different stress responses, including DNA and cell wall damage, and homeostasis of divalent cations, demonstrating that biofilm formation can be inhibited through a variety of molecular mechanisms. One tested drug, tyloxapol, did not affect curli expression or cell growth but instead inhibited biofilm formation by suppressing bacterial attachment to the surface. IMPORTANCE The prevention of bacterial biofilm formation is one of the major current challenges in microbiology. Here, by systematically screening a large number of approved drugs for their ability to suppress biofilm formation by Escherichia coli, we identified a number of prospective antibiofilm compounds. We further demonstrated different mechanisms of action for individual compounds, from induction of replicative stress to disbalance of cation homeostasis to inhibition of bacterial attachment to the surface. Our work demonstrates the potential of drug repurposing for the prevention of bacterial biofilm formation and suggests that also for other bacteria, the activity spectrum of antibiofilm compounds is likely to be broad.

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BolA Is a Transcriptional Switch That Turns Off Motility and Turns On Biofilm Development

mBio ◽

10.1128/mbio.02352-14 ◽

2015 ◽

Vol 6 (1) ◽

Cited By ~ 46

Author(s):

Clémentine Dressaire ◽

Ricardo Neves Moreira ◽

Susana Barahona ◽

António Pedro Alves de Matos ◽

Cecília Maria Arraiano

Keyword(s):

Escherichia Coli ◽

Biofilm Formation ◽

Extracellular Polysaccharides ◽

Bacterial Cells ◽

Content Type ◽

Bacterial Transcription ◽

A Genome ◽

Exact Function ◽

Transcriptional Switch ◽

Biofilm Development

ABSTRACTBacteria are extremely versatile organisms that rapidly adapt to changing environments. When bacterial cells switch from planktonic growth to biofilm, flagellum formation is turned off and the production of fimbriae and extracellular polysaccharides is switched on. BolA is present in most Gram-negative bacteria, and homologues can be found from proteobacteria to eukaryotes. Here, we show that BolA is a new bacterial transcription factor that modulates the switch from a planktonic to a sessile lifestyle. It negatively modulates flagellar biosynthesis and swimming capacity inEscherichia coli. Furthermore, BolA overexpression favors biofilm formation, involving the production of fimbria-like adhesins and curli. Our results also demonstrate that BolA is a protein with high affinity to DNA and is able to regulate many genes on a genome-wide scale. Moreover, we show that the most significant targets of this protein involve a complex network of genes encoding proteins related to biofilm development. Herein, we propose that BolA is a motile/adhesive transcriptional switch, specifically involved in the transition between the planktonic and the attachment stage of biofilm formation.IMPORTANCEEscherichia colicells possess several mechanisms to cope with stresses. BolA has been described as a protein important for survival in late stages of bacterial growth and under harsh environmental conditions. BolA-like proteins are widely conserved from prokaryotes to eukaryotes. Although their exact function is not fully established at the molecular level, they seem to be involved in cell proliferation or cell cycle regulation. Here, we unraveled the role of BolA in biofilm development and bacterial motility. Our work suggests that BolA actively contributes to the decision of bacteria to arrest flagellar production and initiate the attachment to form structured communities, such as biofilms. The molecular studies of different lifestyles coupled with the comprehension of the BolA functions may be an important step for future perspectives, with health care and biotechnology applications.

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Evidence for Escherichia coli Diguanylate Cyclase DgcZ Interlinking Surface Sensing and Adhesion via Multiple Regulatory Routes

Journal of Bacteriology ◽

10.1128/jb.00320-16 ◽

2016 ◽

Vol 198 (18) ◽

pp. 2524-2535 ◽

Cited By ~ 13

Author(s):

Egidio Lacanna ◽

Colette Bigosch ◽

Volkhard Kaever ◽

Alex Boehm ◽

Anke Becker

Keyword(s):

Escherichia Coli ◽

Biofilm Formation ◽

Bacterial Infections ◽

Primary Role ◽

Bacterial Cells ◽

Diguanylate Cyclase ◽

Surface Attachment ◽

Content Type ◽

Surface Sensing

ABSTRACTDgcZ is the main cyclic dimeric GMP (c-di-GMP)-producing diguanylate cyclase (DGC) controlling biosynthesis of the exopolysaccharide poly-β-1,6-N-acetylglucosamine (poly-GlcNAc or PGA), which is essential for surface attachment ofEscherichia coli. Although the complex regulation of DgcZ has previously been investigated, its primary role and the physiological conditions under which the protein is active are not fully understood. Transcription ofdgcZis regulated by the two-component system CpxAR activated by the lipoprotein NlpE in response to surface sensing. Here, we show that the negative effect of acpxRmutation and the positive effect ofnlpEoverexpression on biofilm formation both depend on DgcZ. Coimmunoprecipitation data suggest several potential interaction partners of DgcZ. Interaction with FrdB, a subunit of the fumarate reductase complex (FRD) involved in anaerobic respiration and in control of flagellum assembly, was further supported by a bacterial-two-hybrid assay. Furthermore, the FRD complex was required for the increase in DgcZ-mediated biofilm formation upon induction of oxidative stress by addition of paraquat. A DgcZ-mVENUS fusion protein was found to localize at one bacterial cell pole in response to alkaline pH and carbon starvation. Based on our data and previous knowledge, an integrative role of DgcZ in regulation of surface attachment is proposed. We speculate that both DgcZ-stimulated PGA biosynthesis and interaction of DgcZ with the FRD complex contribute to impeding bacterial escape from the surface.IMPORTANCEBacterial cells can grow by clonal expansion to surface-associated biofilms that are ubiquitous in the environment but also constitute a pervasive problem related to bacterial infections. Cyclic dimeric GMP (c-di-GMP) is a widespread bacterial second messenger involved in regulation of motility and biofilm formation, and plays a primary role in bacterial surface attachment.E. colipossesses a plethora of c-di-GMP-producing diguanylate cyclases, including DgcZ. Our study expands the knowledge on the role of DgcZ in regulation of surface attachment and suggests that it interconnects surface sensing and adhesion via multiple routes.

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Conditional Function of Autoaggregative Protein Cah and Common cah Mutations in Shiga Toxin-Producing Escherichia coli

Applied and Environmental Microbiology ◽

10.1128/aem.01739-17 ◽

2017 ◽

Vol 84 (1) ◽

Cited By ~ 3

Author(s):

Michelle Qiu Carter ◽

Maria T. Brandl ◽

Indira T. Kudva ◽

Robab Katani ◽

Matthew R. Moreau ◽

...

Keyword(s):

Escherichia Coli ◽

Shiga Toxin ◽

Calcium Binding ◽

Biofilm Formation ◽

Bacterial Attachment ◽

Ecological Niches ◽

Loss Of Function ◽

Host Colonization ◽

Content Type ◽

E Coli

ABSTRACTCah is a calcium-binding autotransporter protein involved in autoaggregation and biofilm formation. Althoughcahis widespread in Shiga toxin-producingEscherichia coli(STEC), we detected mutations incahat a frequency of 31.3% in this pathogen. In STEC O157:H7 supershedder strain SS17, a large deletion results in a smaller coding sequence, encoding a protein lacking the C-terminal 71 amino acids compared with Cah in STEC O157:H7 strain EDL933. We examined the function of Cah in biofilm formation and host colonization to better understand the selective pressures forcahmutations. EDL933-Cah played a conditional role in biofilm formationin vitro: it enhancedE. coliDH5α biofilm formation on glass surfaces under agitated culture conditions that prevented autoaggregation but inhibited biofilm formation under hydrostatic conditions that facilitated autoaggregation. This function appeared to be strain dependent since Cah-mediated biofilm formation was diminished when an EDL933cahgene was expressed in SS17. Deletion ofcahin EDL933 enhanced bacterial attachment to spinach leaves and altered the adherence pattern of EDL933 to bovine recto-anal junction squamous epithelial (RSE) cells. In contrast, intransexpression of EDL933cahin SS17 increased its attachment to leaf surfaces, and in DH5α, it enhanced its adherence to RSE cells. Hence, the ecological function of Cah appears to be modulated by environmental conditions and other bacterial strain-specific properties. Considering the prevalence ofcahin STEC and its role in attachment and biofilm formation,cahmutations might be selected in ecological niches in which inactivation of Cah would result in an increased fitness in STEC during colonization of plants or animal hosts.IMPORTANCEShiga toxin-producingEscherichia coli(STEC) harbors genes encoding diverse adhesins, and many of these are known to play an important role in bacterial attachment and host colonization. We demonstrated here that the autotransporter protein Cah confers onE. coliDH5α cells a strong autoaggregative phenotype that is inversely correlated with its ability to form biofilms and plays a strain-specific role in plant and animal colonization by STEC. Althoughcahis widespread in the STEC population, we detected a mutation rate of 31.3% incah, which is similar to that reported forrpoSandfimH. The formation of cell aggregates due to increased bacterium-to-bacterium interactions may be disadvantageous to bacterial populations under conditions that favor a planktonic state in STEC. Therefore, a loss-of-function mutation incahis likely a selective trait in STEC when autoaggregative properties become detrimental to bacterial cells and may contribute to the adaptability of STEC to fluctuating environments.

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Bacterial Secretions of Nonpathogenic Escherichia coli Elicit Inflammatory Pathways: a Closer Investigation of Interkingdom Signaling

mBio ◽

10.1128/mbio.00025-15 ◽

2015 ◽

Vol 6 (2) ◽

Cited By ~ 33

Author(s):

Amin Zargar ◽

David N. Quan ◽

Karen K. Carter ◽

Min Guo ◽

Herman O. Sintim ◽

...

Keyword(s):

Escherichia Coli ◽

Epithelial Cells ◽

Negative Feedback ◽

Cell Contact ◽

Bacterial Cells ◽

Content Type ◽

Phenotypic Differences ◽

E Coli ◽

Autoinducer 2 ◽

Human Epithelial Cells

ABSTRACTThere have been many studies on the relationship between nonpathogenic bacteria and human epithelial cells; however, the bidirectional effects of the secretomes (secreted substances in which there is no direct bacterium-cell contact) have yet to be fully investigated. In this study, we use a transwell model to explore the transcriptomic effects of bacterial secretions from two different nonpathogenicEscherichia colistrains on the human colonic cell line HCT-8 using next-generation transcriptome sequencing (RNA-Seq).E. coliBL21 and W3110, while genetically very similar (99.1% homology), exhibit key phenotypic differences, including differences in their production of macromolecular structures (e.g., flagella and lipopolysaccharide) and in their secretion of metabolic byproducts (e.g., acetate) and signaling molecules (e.g., quorum-sensing autoinducer 2 [AI-2]). After analysis of differential epithelial responses to the respective secretomes, this study shows for the first time that a nonpathogenic bacterial secretome activates the NF-κB-mediated cytokine-cytokine receptor pathways while also upregulating negative-feedback components, including the NOD-like signaling pathway. Because of AI-2's relevance as a bacterium-bacterium signaling molecule and the differences in its secretion rates between these strains, we investigated its role in HCT-8 cells. We found that the expression of the inflammatory cytokine interleukin 8 (IL-8) responded to AI-2 with a pattern of rapid upregulation before subsequent downregulation after 24 h. Collectively, these data demonstrate that secreted products from nonpathogenic bacteria stimulate the transcription of immune-related biological pathways, followed by the upregulation of negative-feedback elements that may serve to temper the inflammatory response.IMPORTANCEThe symbiotic relationship between the microbiome and the host is important in the maintenance of human health. There is a growing need to further understand the nature of these relationships to aid in the development of homeostatic probiotics and also in the design of novel antimicrobial therapeutics. To our knowledge, this is the first global-transcriptome study of bacteria cocultured with human epithelial cells in a model to determine the transcriptional effects of epithelial cells in which epithelial and bacterial cells are allowed to “communicate” with each other only through diffusible small molecules and proteins. By beginning to demarcate the direct and indirect effects of bacteria on the gastrointestinal (GI) tract, two-way interkingdom communication can potentially be mediated between host and microbe.

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Application of Bacteriophages on Shiga Toxin-Producing Escherichia coli (STEC) Biofilm

Antibiotics ◽

10.3390/antibiotics10111423 ◽

2021 ◽

Vol 10 (11) ◽

pp. 1423

Author(s):

Nicola Mangieri ◽

Roberto Foschino ◽

Claudia Picozzi

Keyword(s):

Escherichia Coli ◽

Shiga Toxin ◽

Biofilm Formation ◽

Pathogenic Bacteria ◽

Antimicrobial Agents ◽

Bacterial Cells ◽

Abiotic Surfaces ◽

Continuous Presence ◽

Different Strains ◽

Better Than

Shiga toxin-producing Escherichia coli are pathogenic bacteria able to form biofilms both on abiotic surfaces and on food, thus increasing risks for food consumers. Moreover, biofilms are difficult to remove and more resistant to antimicrobial agents compared to planktonic cells. Bacteriophages, natural predators of bacteria, can be used as an alternative to prevent biofilm formation or to remove pre-formed biofilm. In this work, four STEC able to produce biofilm were selected among 31 different strains and tested against single bacteriophages and two-phage cocktails. Results showed that our phages were able to reduce biofilm formation by 43.46% both when used as single phage preparation and as a cocktail formulation. Since one of the two cocktails had a slightly better performance, it was used to remove pre-existing biofilms. In this case, the phages were unable to destroy the biofilms and reduce the number of bacterial cells. Our data confirm that preventing biofilm formation in a food plant is better than trying to remove a preformed biofilm and the continuous presence of bacteriophages in the process environment could reduce the number of bacteria able to form biofilms and therefore improve the food safety.

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Novel regulators of the csgD gene encoding the master regulator of biofilm formation in Escherichia coli K-12

Microbiology ◽

10.1099/mic.0.000947 ◽

2020 ◽

Vol 166 (9) ◽

pp. 880-890 ◽

Cited By ~ 1

Author(s):

Hiroshi Ogasawara ◽

Toshiyuki Ishizuka ◽

Shuhei Hotta ◽

Michiko Aoki ◽

Tomohiro Shimada ◽

...

Keyword(s):

Escherichia Coli ◽

Biofilm Formation ◽

Cell Aggregation ◽

Master Regulator ◽

Gene Encoding ◽

Content Type ◽

Promoter Probe ◽

K 12 ◽

Specific Environmental Condition

Under stressful conditions, Escherichia coli forms biofilm for survival by sensing a variety of environmental conditions. CsgD, the master regulator of biofilm formation, controls cell aggregation by directly regulating the synthesis of Curli fimbriae. In agreement of its regulatory role, as many as 14 transcription factors (TFs) have so far been identified to participate in regulation of the csgD promoter, each monitoring a specific environmental condition or factor. In order to identify the whole set of TFs involved in this typical multi-factor promoter, we performed in this study ‘promoter-specific transcription-factor’ (PS-TF) screening in vitro using a set of 198 purified TFs (145 TFs with known functions and 53 hitherto uncharacterized TFs). A total of 48 TFs with strong binding to the csgD promoter probe were identified, including 35 known TFs and 13 uncharacterized TFs, referred to as Y-TFs. As an attempt to search for novel regulators, in this study we first analysed a total of seven Y-TFs, including YbiH, YdcI, YhjC, YiaJ, YiaU, YjgJ and YjiR. After analysis of curli fimbriae formation, LacZ-reporter assay, Northern-blot analysis and biofilm formation assay, we identified at least two novel regulators, repressor YiaJ (renamed PlaR) and activator YhjC (renamed RcdB), of the csgD promoter.

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Evaluation of Changes Induced in the Probiotic Escherichia coli M17 Following Recurrent Exposure to Antimicrobials

Journal of Pharmaceutical Research International ◽

10.9734/jpri/2021/v33i29b31601 ◽

2021 ◽

pp. 158-167

Author(s):

M. J. A. Mbarga ◽

I. V. Podoprigora ◽

E. G. Volina ◽

A. V. Ermolaev ◽

L. A. Smolyakova

Keyword(s):

Escherichia Coli ◽

Growth Rate ◽

Silver Nanoparticles ◽

Biofilm Formation ◽

Fold Increase ◽

Bacterial Attachment ◽

Diffusion Method ◽

Cross Resistance ◽

Microdilution Method ◽

Similar Work

Introduction: It is already well known that the exposure of certain bacteria, pathogenic or not, to antimicrobials is likely to increase their virulence and induce the development of direct or cross resistance to antimicrobials, but there is almost no information available regarding probiotics. Aim: To assess the changes induced in susceptibility to antibiotics, biofilm formation, growth rate and relative pathogenicity in the probiotic Escherichia coli M17 (EC-M17) after long exposure to antimicrobials namely ampicillin, kanamycin, cefazolin and silver nanoparticles (AgNPs). Methods: After determining the minimum inhibitory concentrations (MIC) and minimum bactericidal concentrations (MBC) of the 4 antimicrobials above-mentioned by the microdilution method, EC-M17 was exposed to increasing subinhibitory doses ranging from MIC/8 to MIC for 8 days. The susceptibility to antibiotics of the mutants obtained was assessed by the Kirby Bauer disc diffusion method, biofilm formation by the Congo red agar method and with crystal violet bacterial attachment assay, and relative pathogenicity was assessed using a Galleria melonella waxworm model. Results: Exposure to antimicrobials induces noticeable changes in EC-M17. The highest adaptation to antimicrobials was observed on AgNPs with 8-fold increase in MIC and 16-fold increase in MBC of AgNPs. EC-M17 exposed to ampicillin, kanamycin and silver nanoparticles became resistant to ampicillin, ceftazidime, ceftazidime/clavulanate and tetracycline while exposure to cefazolin induced a significant decrease in sensitivity to tetracycline and ampicillin and resistance to ceftazidime/clavulanate and ceftazidime. The strain exposed to ampicillin was the only one to produce more biofilm than the control strain and except the EC-M17 exposed to cefazolin, all other EC-M17 strains were more pathogenic on G. melonella model than the control. Conclusion: Data in this investigation suggest that repeated exposure of the probiotic EC-M17 to antimicrobials may induce changes in antimicrobials susceptibility, biofilm formation, growth rate, and relative pathogenicity. Therefore, as far as possible, the probiotic E. coli M17 should not be used in combination with antibiotics and further investigations are required to expand similar work on more probiotics in order to avoid resistance build-up which might be transmitted by horizontal transfer.

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Influence of Type I Fimbriae and Fluid Shear Stress on Bacterial Behavior and Multicellular Architecture of Early Escherichia coli Biofilms at Single-Cell Resolution

Applied and Environmental Microbiology ◽

10.1128/aem.02343-17 ◽

2018 ◽

Vol 84 (6) ◽

Cited By ~ 8

Author(s):

Liyun Wang ◽

Robert Keatch ◽

Qi Zhao ◽

John A. Wright ◽

Clare E. Bryant ◽

...

Keyword(s):

Escherichia Coli ◽

Shear Stress ◽

Single Cell ◽

Biofilm Formation ◽

Fluid Shear Stress ◽

Cell Membrane Permeability ◽

Type I ◽

Fluid Shear ◽

Content Type ◽

Type I Fimbriae

ABSTRACT Biofilm formation on abiotic surfaces in the food and medical industry can cause severe contamination and infection, yet how biological and physical factors determine the cellular architecture of early biofilms and the bacterial behavior of the constituent cells remains largely unknown. In this study, we examined the specific role of type I fimbriae in nascent stages of biofilm formation and the response of microcolonies to environmental flow shear at the single-cell resolution. The results show that type I fimbriae are not required for reversible adhesion from plankton, but they are critical for the irreversible adhesion of Escherichia coli strain MG1655 cells that form biofilms on polyethylene terephthalate (PET) surfaces. Besides establishing firm cell surface contact, the irreversible adhesion seems necessary to initiate the proliferation of E. coli on the surface. After the application of shear stress, bacterial retention is dominated by the three-dimensional architecture of colonies, independent of the population size, and the multilayered structure could protect the embedded cells from being insulted by fluid shear, while the cell membrane permeability mainly depends on the biofilm population size and the duration of the shear stress. IMPORTANCE Bacterial biofilms could lead to severe contamination problems in medical devices and food processing equipment. However, biofilms are usually studied at a rough macroscopic level; thus, little is known about how individual bacterium behavior within biofilms and the multicellular architecture are influenced by bacterial appendages (e.g., pili/fimbriae) and environmental factors during early biofilm formation. We applied confocal laser scanning microscopy (CLSM) to visualize Escherichia coli microcolonies at a single-cell resolution. Our findings suggest that type I fimbriae are vital to the initiation of bacterial proliferation on surfaces. We also found that the fluid shear stress affects the biofilm architecture and cell membrane permeability of the constituent bacteria in a different way: the onset of the biofilm is linked with the three-dimensional morphology, while membranes are regulated by the overall population of microcolonies.

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