Brominated Furanones Inhibit Biofilm Formation by Salmonella enterica Serovar Typhimurium

ABSTRACT Salmonella enterica serovar Typhimurium is a main cause of bacterial food-borne diseases. As Salmonella can form biofilms in which it is better protected against antimicrobial agents on a wide diversity of surfaces, it is of interest to explore ways to inhibit biofilm formation. Brominated furanones, originally extracted from the marine alga Delisea pulchra, are known to interfere with biofilm formation in several pathogens. In this study, we have synthesized a small focused library of brominated furanones and tested their activity against S. enterica serovar Typhimurium biofilm formation. We show that several furanones inhibit Salmonella biofilm formation at non-growth-inhibiting concentrations. The most interesting compounds are (Z)-4-bromo-5-(bromomethylene)-3-alkyl-2(5H)-furanones with chain lengths of two to six carbon atoms. A microarray study was performed to analyze the gene expression profiles of Salmonella in the presence of (Z)-4-bromo-5-(bromomethylene)-3-ethyl-2(5H)-furanone. The induced genes include genes that are involved in metabolism, stress response, and drug sensitivity. Most of the repressed genes are involved in metabolism, the type III secretion system, and flagellar biosynthesis. Follow-up experiments confirmed that this furanone interferes with the synthesis of flagella by Salmonella. No evidence was found that furanones act on the currently known quorum-sensing systems in Salmonella. Interestingly, pretreatment with furanones rendered Salmonella biofilms more susceptible to antibiotic treatment. Conclusively, this work demonstrates that particular brominated furanones have potential in the prevention of biofilm formation by Salmonella serovar Typhimurium.

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Effects of P22 bacteriophage on salmonella Enterica subsp. enterica serovar Typhimurium DMC4 strain biofilm formation and eradication

Archives of Biological Sciences ◽

10.2298/abs141120114k ◽

2015 ◽

Vol 67 (4) ◽

pp. 1361-1367 ◽

Cited By ~ 5

Author(s):

Basar Karaca ◽

Nefise Akcelik ◽

Mustafa Akcelik

Keyword(s):

Salmonella Enterica ◽

Biofilm Formation ◽

Bacterial Infections ◽

Food Systems ◽

Antimicrobial Agents ◽

Biofilm Inhibition ◽

Serovar Typhimurium ◽

Potential Applications ◽

Steel Surfaces

Over the last decades, several antimicrobial agents have been made available. Due to increasing antimicrobial resistance, bacteriophages were rediscovered for their potential applications against bacterial infections. In the present study, biofilm inhibition and eradication of Salmonella enterica subsp. enterica serovar Typhimurium DMC4 strain (S. Typhimurium) was evaluated with respect to different incubation periods at different P22 phage titrations. The efficacy of P22 phage on biofilm formation and eradication of S. Typhimurium DMC4 strain was screened in vitro on polystyrene and stainless steel surfaces. The biofilm forming capacity of S. Typhimurium was significantly reduced at higher phage titrations (106 pfu/mL ?). All phage titers (104-108 pfu/mL) were found to be effective at the end of the 24 h-incubation period whereas higher phage titrations were found to be effective at the end of the 48 h and 72 h of incubation. P22 phage has less efficacy on already formed, especially mature biofilms (72 h-old biofilm). Notable results of P22 phage treatment on S. Typhimurium biofilm suggest that P22 phage has potential uses in food systems.

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Inhibition of Bacterial Biofilm Formation by Phytotherapeutics with Focus on Overcoming Antimicrobial Resistance

Current Pharmaceutical Design ◽

10.2174/1381612826666200212121710 ◽

2020 ◽

Vol 26 (24) ◽

pp. 2807-2816 ◽

Cited By ~ 1

Author(s):

Yun Su Jang ◽

Tímea Mosolygó

Keyword(s):

Antimicrobial Resistance ◽

Biofilm Formation ◽

Antimicrobial Agents ◽

Bacterial Biofilm ◽

Experimental Investigations ◽

Resistant Bacteria ◽

Salmonella Spp ◽

Food Borne ◽

High Prevalence ◽

Scientific Attention

: Bacteria within biofilms are more resistant to antibiotics and chemical agents than planktonic bacteria in suspension. Treatment of biofilm-associated infections inevitably involves high dosages and prolonged courses of antimicrobial agents; therefore, there is a potential risk of the development of antimicrobial resistance (AMR). Due to the high prevalence of AMR and its association with biofilm formation, investigation of more effective anti-biofilm agents is required. : From ancient times, herbs and spices have been used to preserve foods, and their antimicrobial, anti-biofilm and anti-quorum sensing properties are well known. Moreover, phytochemicals exert their anti-biofilm properties at sub-inhibitory concentrations without providing the opportunity for the emergence of resistant bacteria or harming the host microbiota. : With increasing scientific attention to natural phytotherapeutic agents, numerous experimental investigations have been conducted in recent years. The present paper aims to review the articles published in the last decade in order to summarize a) our current understanding of AMR in correlation with biofilm formation and b) the evidence of phytotherapeutic agents against bacterial biofilms and their mechanisms of action. The main focus has been put on herbal anti-biofilm compounds tested to date in association with Staphylococcus aureus, Pseudomonas aeruginosa and food-borne pathogens (Salmonella spp., Campylobacter spp., Listeria monocytogenes and Escherichia coli).

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Cystathionine β-Lyase Is Important for Virulence of Salmonella enterica Serovar Typhimurium

Infection and Immunity ◽

10.1128/iai.72.6.3310-3314.2004 ◽

2004 ◽

Vol 72 (6) ◽

pp. 3310-3314 ◽

Cited By ~ 43

Author(s):

Linda J. Ejim ◽

Vanessa M. D'Costa ◽

Nadine H. Elowe ◽

J. Concepción Loredo-Osti ◽

Danielle Malo ◽

...

Keyword(s):

Salmonella Enterica ◽

Biosynthetic Pathway ◽

Antibacterial Agents ◽

Antimicrobial Agents ◽

Salmonella Enterica Serovar Typhimurium ◽

Systemic Infection ◽

Bacterial Virulence ◽

Methionine Biosynthesis ◽

Insertional Inactivation ◽

Serovar Typhimurium

ABSTRACT The biosynthesis of methionine in bacteria requires the mobilization of sulfur from Cys by the formation and degradation of cystathionine. Cystathionine β-lyase, encoded by metC in bacteria and STR3 in Schizosaccharomyces pombe, catalyzes the breakdown of cystathionine to homocysteine, the penultimate step in methionine biosynthesis. This enzyme has been suggested to be the target for pyridinamine antimicrobial agents. We have demonstrated, by using purified enzymes from bacteria and yeast, that cystathionine β-lyase is not the likely target of these agents. Nonetheless, an insertional inactivation of metC in Salmonella enterica serovar Typhimurium resulted in the attenuation of virulence in a mouse model of systemic infection. This result confirms a previous chemical validation of the Met biosynthetic pathway as a target for the development of antibacterial agents and demonstrates that cystathionine β-lyase is important for bacterial virulence.

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DETERMINATION OF in vitro BIOFILM FORMATION ABILITIES OF FOOD BORNE Salmonella enterica ISOLATES

Trakya University Journal of Natural Sciences ◽

10.23902/trkjnat.471236 ◽

2019 ◽

Cited By ~ 1

Author(s):

Deniz Aksoy

Keyword(s):

Salmonella Enterica ◽

Biofilm Formation ◽

Food Borne

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Clarithromycin Exerts an Antibiofilm Effect against Salmonella enterica Serovar Typhimurium rdar Biofilm Formation and Transforms the Physiology towards an Apparent Oxygen-Depleted Energy and Carbon Metabolism

Infection and Immunity ◽

10.1128/iai.00510-20 ◽

2020 ◽

Vol 88 (11) ◽

Author(s):

Munirah Zafar ◽

Humera Jahan ◽

Sulman Shafeeq ◽

Manfred Nimtz ◽

Lothar Jänsch ◽

...

Keyword(s):

Antimicrobial Resistance ◽

Salmonella Enterica ◽

Biofilm Formation ◽

Antibiofilm Activity ◽

Bacterial Cells ◽

Content Type ◽

Regulatory Pathways ◽

Heat Shock Stress ◽

Extracellular Matrix Components ◽

Serovar Typhimurium

ABSTRACT Upon biofilm formation, production of extracellular matrix components and alteration in physiology and metabolism allows bacteria to build up multicellular communities which can facilitate nutrient acquisition during unfavorable conditions and provide protection toward various forms of environmental stresses to individual cells. Thus, bacterial cells within biofilms become tolerant against antimicrobials and the immune system. In the present study, we evaluated the antibiofilm activity of the macrolides clarithromycin and azithromycin. Clarithromycin showed antibiofilm activity against rdar (red, dry, and rough) biofilm formation of the gastrointestinal pathogen Salmonella enterica serovar Typhimurium ATCC 14028 (Nalr) at a 1.56 μM subinhibitory concentration in standing culture and dissolved cell aggregates at 15 μM in a microaerophilic environment, suggesting that the oxygen level affects the activity of the drug. Treatment with clarithromycin significantly decreased transcription and production of the rdar biofilm activator CsgD, with biofilm genes such as csgB and adrA to be concomitantly downregulated. Although fliA and other flagellar regulon genes were upregulated, apparent motility was downregulated. RNA sequencing showed a holistic cell response upon clarithromycin exposure, whereby not only genes involved in the biofilm-related regulatory pathways but also genes that likely contribute to intrinsic antimicrobial resistance, and the heat shock stress response were differentially regulated. Most significantly, clarithromycin exposure shifted the cells toward an apparent oxygen- and energy-depleted status, whereby the metabolism that channels into oxidative phosphorylation was downregulated, and energy gain by degradation of propane 1,2-diol, ethanolamine and l-arginine catabolism, potentially also to prevent cytosolic acidification, was upregulated. This analysis will allow the subsequent identification of novel intrinsic antimicrobial resistance determinants.

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Facultative Anaerobes Shape Multispecies Biofilms Composed of Meat Processing Surface Bacteria and Escherichia coli O157:H7 or Salmonella enterica Serovar Typhimurium

Applied and Environmental Microbiology ◽

10.1128/aem.01123-19 ◽

2019 ◽

Vol 85 (17) ◽

Author(s):

Jeyachchandran Visvalingam ◽

Hui Wang ◽

Tim C. Ells ◽

Xianqin Yang

Keyword(s):

Food Processing ◽

Salmonella Enterica ◽

Biofilm Formation ◽

Single Species ◽

Meat Processing ◽

Content Type ◽

E Coli ◽

Facultative Anaerobes ◽

Serovar Typhimurium ◽

Multispecies Biofilms

ABSTRACT This study investigated the microbial dynamics in multispecies biofilms of Escherichia coli O157:H7 strain 1934 (O157) or Salmonella enterica serovar Typhimurium ATCC 14028 (ST) and 40 strains of meat processing surface bacteria (MPB). Biofilms of O157 or ST with/without MPB were developed on stainless steel coupons at 15°C for up to 6 days. Bacteria in suspensions (inoculum, days 2 and 6) and biofilms (days 2 and 6) were enumerated by plating. The composition of multispecies cultures was determined by 16S rRNA gene sequencing. In suspensions, levels of O157 and ST were ∼2 log higher in single-species than in multispecies cultures on both sampling days. ST was 3 log higher in single-species than in multispecies biofilms. A similar trend, though to a lesser extent, was observed for O157 in biofilms on day 2 but not on day 6. No difference (P > 0.05) in bacterial counts was noted for the two MPB-pathogen cocultures at any time during incubation. Bacterial diversity in multispecies cultures decreased with incubation time, irrespective of the pathogen or culture type. The changes in the relative abundance of MPB were similar for the two MPB-pathogen cocultures, though different interbacterial interactions were noted. Respective fractions of ST and O157 were 2.1% and 0.97% initially and then 0.10% and 0.07% on day 2, and 0.60% and 0.04% on day 6. The relative proportions of facultative anaerobes in both multispecies cultures were greater in both suspensions and biofilms than in the inoculum. Citrobacter, Hafnia, Aeromonas, and Carnobacterium predominated in biofilms but not always in the planktonic cultures. IMPORTANCE Results of this study demonstrate that Salmonella enterica serovar Typhimurium and E. coli O157:H7 can integrate into biofilms when cocultured with bacteria from meat plant processing surfaces. However, the degree of biofilm formation for both pathogens was substantially reduced in the presence of the competing microbiota, with S. Typhimurium more greatly affected than E. coli O157:H7. The expression of extracellular determinants such as curli and cellulose appears to be less important for biofilm formation of the pathogens in multispecies cultures than in monoculture. In contrast to previous reports regarding food processing surface bacteria, data collected here also demonstrate that facultative anaerobes may have a competitive edge over strict aerobes in establishing multispecies biofilms. It would be important to take into account the presence of background bacteria when evaluating the potential persistence of a pathogen in food processing facilities.

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Mucoid Pseudomonas aeruginosa isolates maintain the biofilm formation capacity and the gene expression profiles during the chronic lung infection of CF patients

Apmis ◽

10.1111/j.1600-0463.2011.02726.x ◽

2011 ◽

Vol 119 (4-5) ◽

pp. 263-274 ◽

Cited By ~ 38

Author(s):

BAOLERI LEE ◽

CHARLOTTE K. SCHJERLING ◽

NIKOLAI KIRKBY ◽

NADINE HOFFMANN ◽

REHANNAH BORUP ◽

...

Keyword(s):

Gene Expression ◽

Pseudomonas Aeruginosa ◽

Biofilm Formation ◽

Expression Profiles ◽

Gene Expression Profiles ◽

Lung Infection ◽

Chronic Lung Infection

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Genomic Profiling of Iron-Responsive Genes in Salmonella enterica Serovar Typhimurium by High-Throughput Screening of a Random Promoter Library

Journal of Bacteriology ◽

10.1128/jb.185.16.4973-4982.2003 ◽

2003 ◽

Vol 185 (16) ◽

pp. 4973-4982 ◽

Cited By ~ 124

Author(s):

Jaime Bjarnason ◽

Carolyn M. Southward ◽

Michael G. Surette

Keyword(s):

Gene Expression ◽

High Throughput ◽

Salmonella Enterica ◽

High Throughput Screening ◽

Expression Profiles ◽

Transport Systems ◽

Iron Availability ◽

Iron Storage ◽

Promoter Library ◽

Serovar Typhimurium

ABSTRACT The importance of iron to bacteria is shown by the presence of numerous iron-scavenging and transport systems and by many genes whose expression is tightly regulated by iron availability. We have taken a global approach to gene expression analysis of Salmonella enterica serovar Typhimurium in response to iron by combining efficient, high-throughput methods with sensitive, luminescent reporting of gene expression using a random promoter library. Real-time expression profiles of the library were generated under low- and high-iron conditions to identify iron-regulated promoters, including a number of previously identified genes. Our results indicate that approximately 7% of the genome may be regulated directly or indirectly by iron. Further analysis of these clones using a Fur titration assay revealed three separate classes of genes; two of these classes consist of Fur-regulated genes. A third class was Fur independent and included both negatively and positively iron-responsive genes. These may reflect new iron-dependent regulons. Iron-responsive genes included iron transporters, iron storage and mobility proteins, iron-containing proteins (redox proteins, oxidoreductases, and cytochromes), transcriptional regulators, and the energy transducer tonB. By identifying a wide variety of iron-responsive genes, we extend our understanding of the global effect of iron availability on gene expression in the bacterial cell.

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