Interdependence between iron acquisition and biofilm formation in Pseudomonas aeruginosa

Kang, Donghoon; Kirienko, Natalia V.

doi:10.1007/s12275-018-8114-3

Cited by 94 publications

(79 citation statements)

References 122 publications

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“…Among the proteins downregulated in 72 h biofilms, three are associated with the iron acquisition; isochorismate synthase (MPAO1_03800), a rate-limiting enzyme involved in the production of salicylate (precursor of the siderophore pyochelin) 53 , the siderophore receptor MPAO1_23930 (PuiA), and the siderophore-interacting protein MPAO1_15475. Iron acquisition is deemed necessary for P. aeruginosa biofilm formation 54 so their down-regulation was unexpected, however, this response is likely circumvented by the utilization of alternative iron acquisition strategies including the high-affinity siderophore pyoverdine.…”

Section: Resultsmentioning

confidence: 99%

An integrated model system to gain mechanistic insights into biofilm-associated antimicrobial resistance in Pseudomonas aeruginosa MPAO1

Varadarajan

Allan

Valentin

et al. 2020

npj Biofilms Microbiomes

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Pseudomonas aeruginosa MPAO1 is the parental strain of the widely utilized transposon mutant collection for this important clinical pathogen. Here, we validate a model system to identify genes involved in biofilm growth and biofilm-associated antibiotic resistance. Our model employs a genomics-driven workflow to assemble the complete MPAO1 genome, identify unique and conserved genes by comparative genomics with the PAO1 reference strain and genes missed within existing assemblies by proteogenomics. Among over 200 unique MPAO1 genes, we identified six general essential genes that were overlooked when mapping public Tn-seq data sets against PAO1, including an antitoxin. Genomic data were integrated with phenotypic data from an experimental workflow using a user-friendly, soft lithography-based microfluidic flow chamber for biofilm growth and a screen with the Tn-mutant library in microtiter plates. The screen identified hitherto unknown genes involved in biofilm growth and antibiotic resistance. Experiments conducted with the flow chamber across three laboratories delivered reproducible data on P. aeruginosa biofilms and validated the function of both known genes and genes identified in the Tn-mutant screens. Differential protein abundance data from planktonic cells versus biofilm confirmed the upregulation of candidates known to affect biofilm formation, of structural and secreted proteins of type VI secretion systems, and provided proteogenomic evidence for some missed MPAO1 genes. This integrated, broadly applicable model promises to improve the mechanistic understanding of biofilm formation, antimicrobial tolerance, and resistance evolution in biofilms.

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Section: Resultsmentioning

confidence: 99%

An integrated model system to gain mechanistic insights into biofilm-associated antimicrobial resistance in Pseudomonas aeruginosa MPAO1

Varadarajan

Allan

Valentin

et al. 2020

npj Biofilms Microbiomes

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“…Iron availability has been shown to both positively and negatively regulate bio lm formation through complex network systems 55 . Although high Fe can lead to ROS production, Kang and Kirienko suggested that iron uptake and homeostasis is essential for successful bio lm formation in Pseudomonas aeruginosa 56 . Fe-storage proteins bacterioferritin (Bfr) and ferritin A (Ftn), required to prevent ROS generation via Fenton reaction and DNA damage, are functionally very large proteins with a core to accommodate 3000 Fe atoms.…”

Section: Discussionmentioning

confidence: 99%

Global transcriptional regulation by cell-free sup of S. Typhimurium peptide transporter mutant leads to inhibition of intraspecies biofilm initiation

Chandra

Muralidhara²,

Kamanna

et al. 2020

Preprint

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Salmonella is a genus of widely spread Gram negative, facultative anaerobic bacteria, which is known to cause ¼th of the diarrhoeal morbidity and mortality globally. It causes typhoid fever and gastroenteritis by gaining access to the host gut through contaminated food and water. Salmonella utilizes its biofilm lifestyle to strongly resist antibiotics and persist in the host. Although the biofilm removal or dispersal have been studied widely, the inhibition of initiation Salmonella biofilm has not been studied much. This study was conducted to determine the anti-biofilm property of the cell-free supernatant obtained from a carbon-starvation inducible proline peptide transporter mutant (ΔyjiY) strain. Our study shows that Salmonella ΔyjiY culture supernatant inhibits biofilm initiation by regulating biofilm associated transcriptional network. This work demonstrates that highly abundant proteases like ecotin, HslV and GrpE cleave the protein aggregates, whereas global transcription regulators H-NS, FlgM regulate expression of SPIs and flagellar genes. Relatively low abundance of flavoredoxin, glutaredoxin, thiol peroxidase etc. leads to accumulation of ROS within the biofilm, and subsequent toxicity. This work further suggests that targeting these oxidative stress relieving proteins might be a good druggable choice to reduce Salmonella biofilm.

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“…First, it has been observed that the availability of iron greatly influences the ability of UPEC to form biofilms on the abiotic surface in urine medium (a poor source of iron); interestingly, this phenomenon was also dependent on the yersiniabactin system (Hancock et al, 2008). Second, Pseudomonas aeruginosa uses exopolysaccharides to sequester and store iron and stimulate biofilm formation (Yu et al, 2016;Kang & Kirienko, 2018). Negatively charged exopolysaccharides chelate Fe 3+ and Fe 2+ in the vicinity of the bacteria and allow its capture.…”

Section: Iron Capture and Biofilm Formationmentioning

confidence: 99%

The Crohn’s disease-related AIEC strain LF82 assembles a biofilm-like matrix to protect intracellular microcolonies from phagolysosomal attack

Prudent

Demarre

Vazeille

et al. 2020

Preprint

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Patients with Crohn's disease exhibit abnormal colonization of the intestine by proteobacteria, and among these bacteria, the adherent invasive E. coli (AIEC) family. They are predominant in the mucus, adhere to epithelial cells, colonize them and survive inside macrophages. We recently demonstrated that the acclimation of the AIEC strain LF82 to phagolysosomal stress requires stringent and SOS responses. Such adaptation involves a long lag phase in which many LF82 cells become antibiotic tolerant. Later during infection, they proliferate in vacuoles and form colonies harboring dozens of LF82 bacteria. In the present work, we investigated the mechanism sustaining this phase of growth. We found that intracellular LF82 produced an extrabacterial matrix composed of exopolysaccharides and amyloid fibers that surrounded each individual LF82 cell. This matrix acts as a biofilm and controls the formation of LF82 intracellular bacterial communities (IBCs) inside phagolysosomes for several days post infection. Using genomics assays, we characterized the gene set involved in IBCs formation and revealed the crucial role played by a pathogenicity island presents in the genome of most AIEC strains in this process. Iron capture, by the yersiniabactin system encoded by this pathogenicity island, is essential to form IBC and LF82 survival within macrophages. These results demonstrate that AIEC have developed a sophisticated strategy to establish their replicative niche within macrophages, which might have implications for envisioning future antibacterial strategies for Crohn's disease. the members of the CIRB imaging facility. We are grateful to Ugo Szachnowski for his help with RNAseq data processing and Nicolas Lapaque and Eric Allemand for helpful suggestions.

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Interdependence between iron acquisition and biofilm formation in Pseudomonas aeruginosa

Cited by 94 publications

References 122 publications

An integrated model system to gain mechanistic insights into biofilm-associated antimicrobial resistance in Pseudomonas aeruginosa MPAO1

An integrated model system to gain mechanistic insights into biofilm-associated antimicrobial resistance in Pseudomonas aeruginosa MPAO1

Global transcriptional regulation by cell-free sup of S. Typhimurium peptide transporter mutant leads to inhibition of intraspecies biofilm initiation

The Crohn’s disease-related AIEC strain LF82 assembles a biofilm-like matrix to protect intracellular microcolonies from phagolysosomal attack

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