Penetration barrier contributes to bacterial biofilm-associated resistance against only select antibiotics, and exhibits genus-, strain- and antibiotic-specific differences

Singh, R. P.; Sahore, Simmi; Kaur, Preetinder; Rani, Alka; Ray, Pallab

doi:10.1093/femspd/ftw056

Cited by 112 publications

(82 citation statements)

References 22 publications

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“…4D). Since the biofilm matrix of E. coli is known to impede ␤-lactam penetration significantly (48), this change correlates well with the significant decrease in Amp susceptibility in 0.85% NaCl among attached cells (77.4% decrease between 3-and 4-h biofilms; P Ͻ 0.0001, two-way ANOVA adjusted by Tukey test) (Fig. 1A).…”

Section: Resultssupporting

confidence: 53%

“…Collectively, these results indicate that cellulose and curli may influence the antibiotic susceptibility of surfaceattached E. coli cells. Unlike ␤-lactam, the E. coli biofilm matrix cannot prevent fluoroquinolone penetration effectively (48), which explains why the susceptibility of biofilm cells to Ofx (fluoroquinolone family) did not show significant change at the same time point (P ϭ 0.9257, two-way ANOVA adjusted by Tukey test) (Fig. 1B).…”

Section: Resultsmentioning

confidence: 99%

“…With the production of EPS started at 3 h after inoculation, the susceptibility of biofilm to Amp decreased presumably due to the decrease in antibiotic penetration. As for Ofx, an antibiotic that has better permeability through E. coli biofilm matrix and killing effects on cells with lower metabolic activities than Amp (28,48), the decrease in Ofx susceptibility of biofilm cells occurred later (16 h after inoculation) when the cellular activities started decreasing. Consistently, we demonstrate that without the protection of EPS, antibiotic susceptibility of dispersed early-stage biofilm cells was higher than planktonic cells due to active cellular activities and cell-cell interactions.…”

Section: Discussionmentioning

confidence: 99%

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Antibiotic Susceptibility of Escherichia coli Cells during Early-Stage Biofilm Formation

Lee

Carnicelli

et al. 2019

J Bacteriol

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Bacteria form complex multicellular structures on solid surfaces known as biofilms, which allow them to survive in harsh environments. A hallmark characteristic of mature biofilms is the high-level antibiotic tolerance (up to 1,000 times) compared with that of planktonic cells. Here, we report our new findings that biofilm cells are not always more tolerant to antibiotics than planktonic cells in the same culture. Specifically, Escherichia coli RP437 exhibited a dynamic change in antibiotic susceptibility during its early-stage biofilm formation. This phenomenon was not strain specific. Upon initial attachment, surface-associated cells became more sensitive to antibiotics than planktonic cells. By controlling the cell adhesion and cluster size using patterned E. coli biofilms, cells involved in the interaction between cell clusters during microcolony formation were found to be more susceptible to ampicillin than cells within clusters, suggesting a role of cell-cell interactions in biofilm-associated antibiotic tolerance. After this stage, biofilm cells became less susceptible to ampicillin and ofloxacin than planktonic cells. However, when the cells were detached by sonication, both antibiotics were more effective in killing the detached biofilm cells than the planktonic cells. Collectively, these results indicate that biofilm formation involves active cellular activities in adaption to the attached life form and interactions between cell clusters to build the complex structure of a biofilm, which can render these cells more susceptible to antibiotics. These findings shed new light on bacterial antibiotic susceptibility during biofilm formation and can guide the design of better antifouling surfaces, e.g., those with micron-scale topographic structures to interrupt cell-cell interactions. IMPORTANCE Mature biofilms are known for their high-level tolerance to antibiotics; however, antibiotic susceptibility of sessile cells during early-stage biofilm formation is not well understood. In this study, we aim to fill this knowledge gap by following bacterial antibiotic susceptibility during early-stage biofilm formation. We found that the attached cells have a dynamic change in antibiotic susceptibility, and during certain phases, they can be more sensitive to antibiotics than planktonic counterparts in the same culture. Using surface chemistry-controlled patterned biofilm formation, cell-surface and cell-cell interactions were found to affect the antibiotic susceptibility of attached cells. Collectively, these findings provide new insights into biofilm physiology and reveal how adaptation to the attached life form may influence antibiotic susceptibility of bacterial cells.

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Section: Resultssupporting

confidence: 53%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Antibiotic Susceptibility of Escherichia coli Cells during Early-Stage Biofilm Formation

Lee

Carnicelli

et al. 2019

J Bacteriol

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“…This antibiotic acts by binding to the D-Ala-D-ala residues of the membrane bound cell wall precursor, lipid II, preventing its incorporation and stalling active peptidoglycan synthesis 27 . Importantly, some studies have indicated that vancomycin penetration is impeded into biofilms 17 . US-PCCA potentiated vancomycin killing of biofilm-associated cells by 93% (Fig.…”

Section: Resultsmentioning

confidence: 99%

Harnessing Ultrasound-Stimulated Phase Change Contrast Agents to Improve Antibiotic Efficacy Against Methicillin-ResistantStaphylococcus aureusBiofilms

Durham

Sidders

Dayton

et al. 2020

Preprint

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17Bacterial biofilms, often associated with chronic infections, respond poorly to antibiotic 18 therapy and frequently require surgical intervention. Biofilms harbor persister cells, metabolically 19 indolent cells, which are tolerant to most conventional antibiotics. In addition, the biofilm matrix 20 can act as a physical barrier, impeding diffusion of antibiotics. Novel therapeutic approaches 21 frequently improve biofilm killing, but usually fail to achieve eradication. Failure to eradicate the 22 biofilm leads to chronic and relapsing infection, associated with major financial healthcare costs 23 and significant morbidity and mortality. We address this problem with a two-pronged strategy 24 using 1) antibiotics that target persister cells and 2) ultrasound-stimulated phase-change 25 contrast agents (US-PCCA) , which improve antibiotic penetration. 26We previously demonstrated that rhamnolipids, produced by Pseudomonas aeruginosa, 27 could induce aminoglycoside uptake in gram-positive organisms, leading to persister cell death. 28We have also shown that US-PCCA can transiently disrupt biological barriers to improve 29 penetration of therapeutic macromolecules. We hypothesized that combining antibiotics which 30 target persister cells with US-PCCA to improve drug penetration could eradicate methicillin 31 resistant S. aureus (MRSA) biofilms. Aminoglycosides alone or in combination with US-PCCA 32 displayed limited efficacy against MRSA biofilms. In contrast, the anti-persister combination of 33 rhamnolipids and aminoglycosides combined with US-PCCA dramatically reduced biofilm 34 viability, frequently culminating in complete eradication of the biofilm. These data demonstrate 35 that biofilm eradication can be achieved using a combined approach of improving drug 36 penetration of therapeutics that target persister cells.37 38 42 osteomyelitis, endocarditis and pneumonia 2,3. In addition to the high degree of mortality, chronic 43 and relapsing S. aureus infections are common and associated with significant morbidity. This is 44 2 due to frequent treatment failure of S. aureus infections. This is best illustrated by SSTIs, with 45 some studies suggesting treatment failure rates as high as 45% and a recurrence rate of 70% 4. 46Importantly the failure of antibiotic therapy cannot be adequately explained by antibiotic 47 resistance 1. Failure to clear the infection leads to a need for prolonged antibiotic therapies, 48 increased morbidity and mortality, increased likelihood of antibiotic resistance development as 49 well as an enormous financial healthcare burden. 50 S. aureus forms biofilms, bacterial cells embedded in a self-produced extracellular 51 matrix, which act as a protective barrier from the host immune response and other 52 environmental assaults. Biofilms expand up to 1200μm in thickness when attached to indwelling 53 devices such as catheters 5. Non-surface attached biofilms, in chronic wounds and chronic lung 54 infections, harbor smaller non-surface attached cell aggregates ranging from 2-200μm in 5...

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“…Remarkably, cells within the biofilm are far more resistant to a wide range of stressors, including cleaning chemicals and sanitizers, than their free‐living counterparts . This resistance results from a number of factors associated with living within a biofilm, including physical and chemical binding of antimicrobial compounds by EPS, modifications in EPS composition and quantity, imposition of biofilm‐specific mode of growth, or physical protection / engulfment of the sensitive species by the tolerant ones in multispecies biofilm . Moreover, the resistance of cells within a biofilm can also depend on the hydrophobic protective layer of EPS structures, for instance, specified by a small hydrophobic protein called BslA in B. subtilis …”

Section: Biofilm‐forming Bacteria Contaminate Dairy Food and Deteriormentioning

confidence: 99%

Role of Bacillus species in biofilm persistence and emerging antibiofilm strategies in the dairy industry

Shemesh

Ostrov

2020

J Sci Food Agric

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Biofilm‐forming Bacillus species are often involved in persistent contamination and spoilage of dairy products. They therefore present a major microbiological challenge in the field of dairy food quality and safety. Due to their substantial physiological versatility, Bacillus species can survive in various parts of dairy manufacturing plants, leading to a high risk of product spoilage and potential dissemination of foodborne diseases. Furthermore, biofilm and heat‐resistant spore formation make these bacteria challenging to eliminate. Thus, some strategies have been employed to remove, prevent, or delay the formation of Bacillus biofilms in the dairy industry, but with limited success. Lack of understanding of the Bacillus biofilm structure and behavior in conditions relevant to dairy‐associated environments could partially account for this situation. The current paper reviews dairy‐associated biofilm formation by Bacillus species, with particular attention to the role of biofilm in Bacillus species adaptation and survival in a dairy processing environment. Relevant model systems are discussed for the development of novel antimicrobial approaches to improve the quality of dairy food. © 2020 Society of Chemical Industry

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Penetration barrier contributes to bacterial biofilm-associated resistance against only select antibiotics, and exhibits genus-, strain- and antibiotic-specific differences

Cited by 112 publications

References 22 publications

Antibiotic Susceptibility of Escherichia coli Cells during Early-Stage Biofilm Formation

Antibiotic Susceptibility of Escherichia coli Cells during Early-Stage Biofilm Formation

Harnessing Ultrasound-Stimulated Phase Change Contrast Agents to Improve Antibiotic Efficacy Against Methicillin-ResistantStaphylococcus aureusBiofilms

Role of Bacillus species in biofilm persistence and emerging antibiofilm strategies in the dairy industry

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