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Type III secretion system and virulence markers highlight similarities and differences between human- and plant-associated pseudomonads related to Pseudomonas fluorescens and P. putida.

ABSTRACT: Pseudomonas fluorescens is commonly considered a saprophytic rhizobacterium devoid of pathogenic potential. Nevertheless, the recurrent isolation of strains from clinical human cases could indicate the emergence of novel strains originating from the rhizosphere reservoir, which could be particularly resistant to the immune system and clinical treatment. The importance of type three secretion systems (T3SSs) in the related Pseudomonas aeruginosa nosocomial species and the occurrence of this secretion system in plant-associated P. fluorescens raise the question of whether clinical isolates may also harbor T3SSs. In this study, isolates associated with clinical infections and identified in hospitals as belonging to P. fluorescens were compared with fluorescent pseudomonads harboring T3SSs isolated from plants. Bacterial isolates were tested for (i) their genetic relationships based on their 16S rRNA phylogeny, (ii) the presence of T3SS genes by PCR, and (iii) their infectious potential on animals and plants under environmental or physiological temperature conditions. Two groups of bacteria were delineated among the clinical isolates. The first group encompassed thermotolerant (41°C) isolates from patients suffering from blood infections; these isolates were finally found to not belong to P. fluorescens but were closely related and harbored highly conserved T3SS genes belonging to the Ysc-T3SS family, like the T3SSs from P. aeruginosa. The second group encompassed isolates from patients suffering from cystic fibrosis; these isolates belonged to P. fluorescens and harbored T3SS genes belonging to the Hrp1-T3SS family found commonly in plant-associated P. fluorescens.

SUBMITTER: Mazurier S

PROVIDER: S-EPMC4357948 | biostudies-literature | 2015 Apr

REPOSITORIES: biostudies-literature

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Type III secretion system and virulence markers highlight similarities and differences between human- and plant-associated pseudomonads related to Pseudomonas fluorescens and P. putida.

Mazurier Sylvie S Merieau Annabelle A Bergeau Dorian D Decoin Victorien V Sperandio Daniel D Crépin Alexandre A Barbey Corinne C Jeannot Katy K Vicré-Gibouin Maïté M Plésiat Patrick P Lemanceau Philippe P Latour Xavier X

Applied and environmental microbiology 20150130 7

Pseudomonas fluorescens is commonly considered a saprophytic rhizobacterium devoid of pathogenic potential. Nevertheless, the recurrent isolation of strains from clinical human cases could indicate the emergence of novel strains originating from the rhizosphere reservoir, which could be particularly resistant to the immune system and clinical treatment. The importance of type three secretion systems (T3SSs) in the related Pseudomonas aeruginosa nosocomial species and the occurrence of this secre ...[more]

PMID: 25636837

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Project description:Mechanisms by which cells attach to a surface and form a biofilm are diverse and differ greatly among organisms. The Gram-negative gammaproteobacterium Pseudomonas fluorescens attaches to a surface through the localization of the large type 1-secreted RTX adhesin LapA to the outer surface of the cell. LapA localization to the cell surface is controlled by the activities of a periplasmic protease, LapG, and an inner membrane-spanning cyclic di-GMP-responsive effector protein, LapD. A previous study identified a second, LapA-like protein encoded in the P. fluorescens Pf0-1 genome: Pfl01_1463. Here, we identified specific growth conditions under which Pfl01_1463, here called MapA (medium adhesion protein A) is a functional adhesin contributing to biofilm formation. This adhesin, like LapA, appears to be secreted through a Lap-related type 1 secretion machinery, and its localization is controlled by LapD and LapG. However, differing roles of LapA and MapA in biofilm formation are achieved, at least in part, through the differences in the sequences of the two adhesins and different distributions of the expression of the lapA and mapA genes within a biofilm. LapA-like proteins are broadly distributed throughout the Proteobacteria, and furthermore, LapA and MapA are well conserved among other Pseudomonas species. Together, our data indicate that the mechanisms by which a cell forms a biofilm and the components of a biofilm matrix can differ depending on growth conditions and the matrix protein(s) expressed.IMPORTANCE Adhesins are critical for the formation and maturation of bacterial biofilms. We identify a second adhesin in P. fluorescens, called MapA, which appears to play a role in biofilm maturation and whose regulation is distinct from the previously reported LapA adhesin, which is critical for biofilm initiation. Analysis of bacterial adhesins shows that LapA-like and MapA-like adhesins are found broadly in pseudomonads and related organisms, indicating that the utilization of different suites of adhesins may be broadly important in the Gammaproteobacteria.

Project description:Protein secretion systems are crucial mediators of bacterial interactions with other organisms. Among them, the type VI secretion system (T6SS) is widespread in Gram-negative bacteria and appears to inject toxins into competitor bacteria and/or eukaryotic cells. Major human pathogens, such as Vibrio cholerae, Burkholderia and Pseudomonas aeruginosa, express T6SSs. Bacteria prevent self-intoxication by their own T6SS toxins by producing immunity proteins, which interact with the cognate toxins. We describe here an environmental P. fluorescens strain, MFE01, displaying an uncommon oversecretion of Hcp (hemolysin-coregulated protein) and VgrG (valine-glycine repeat protein G) into the culture medium. These proteins are characteristic components of a functional T6SS. The aim of this study was to attribute a role to this energy-consuming overexpression of the T6SS. The genome of MFE01 contains at least two hcp genes (hcp1 and hcp2), suggesting that there may be two putative T6SS clusters. Phenotypic studies have shown that MFE01 is avirulent against various eukaryotic cell models (amebas, plant or animal cell models), but has antibacterial activity against a wide range of competitor bacteria, including rhizobacteria and clinical bacteria. Depending on the prey cell, mutagenesis of the hcp2 gene in MFE01 abolishes or reduces this antibacterial killing activity. Moreover, the introduction of T6SS immunity proteins from S. marcescens, which is not killed by MFE01, protects E. coli against MFE01 killing. These findings suggest that the protein encoded by hcp2 is involved in the killing activity of MFE01 mediated by effectors of the T6SS targeting the peptidoglycan of Gram-negative bacteria. Our results indicate that MFE01 can protect potato tubers against Pectobacterium atrosepticum, which causes tuber soft rot. Pseudomonas fluorescens is often described as a major PGPR (plant growth-promoting rhizobacterium), and our results suggest that there may be a connection between the T6SS and the PGPR properties of this bacterium.

Dataset Information

Type III secretion system and virulence markers highlight similarities and differences between human- and plant-associated pseudomonads related to Pseudomonas fluorescens and P. putida.

Publications

Type III secretion system and virulence markers highlight similarities and differences between human- and plant-associated pseudomonads related to Pseudomonas fluorescens and P. putida.

Similar Datasets

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