Protein secretion systems of Pseudomonas aeruginosa and P. fluorescens

Ma, Qinhong; Zhai, Yufeng; Schneider, Jane C.; Ramseier, Tom M.; Saier, Milton H.

doi:10.1016/s0005-2736(03)00059-2

Cited by 92 publications

(72 citation statements)

References 93 publications

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“…Based on a scan of the recently published DC3000 genome sequence (9), we determined that the DC3000 chromosome possesses a complete tat gene operon comprised of a single copy each of tatA (PSPTO5155), tatB (PSPTO5156), and tatC (PSPTO5157). This was not entirely surprising given that several other pseudomonads were reported to possess Tat export systems (44,51,64). The DC3000 tatABC genes shared Ͼ83% identity to the same genes from P. aeruginosa (62) and P. putida (48) (data not shown).…”

Section: Resultsmentioning

confidence: 92%

Identification of a Twin-Arginine Translocation System in Pseudomonas syringae pv. tomato DC3000 and Its Contribution to Pathogenicity and Fitness

et al. 2005

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The bacterial plant pathogen Pseudomonas syringae pv. tomato DC3000 (DC3000) causes disease in Arabidopsis thaliana and tomato plants, and it elicits the hypersensitive response in nonhost plants such as Nicotiana tabacum and Nicotiana benthamiana. While these events chiefly depend upon the type III protein secretion system and the effector proteins that this system translocates into plant cells, additional factors have been shown to contribute to DC3000 virulence and still many others are likely to exist. Therefore, we explored the contribution of the twin-arginine translocation (Tat) system to the physiology of DC3000. We found that a tatC mutant strain of DC3000 displayed a number of phenotypes, including loss of motility on soft agar plates, deficiency in siderophore synthesis and iron acquisition, sensitivity to copper, loss of extracellular phospholipase activity, and attenuated virulence in host plant leaves. In the latter case, we provide evidence that decreased virulence of tatC mutants likely arises from a synergistic combination of (i) compromised fitness of bacteria in planta; (ii) decreased efficiency of type III translocation; and (iii) cytoplasmically retained virulence factors. Finally, we demonstrate a novel broad-host-range genetic reporter based on the green fluorescent protein for the identification of Tat-targeted secreted virulence factors that should be generally applicable to any gram-negative bacterium. Collectively, our evidence supports the notion that virulence of DC3000 is a multifactorial process and that the Tat system is an important virulence determinant of this phytopathogenic bacterium.The hallmark of the Pseudomonas syringae infection process is the injection of virulence effector proteins directly into host cells via the type III secretion mechanism (TTSS) (14). For efficient translocation of effector proteins, P. syringae must first establish productive contact with a target plant cell. This entails secretion of exopolysaccharides, cell wall-degrading enzymes, plant hormones, and several low-molecular-weight phytotoxins, such as coronatine and syringomycin (1, 30). Since many of these factors are secreted in a type III-independent manner and since deletion of many of these virulence factors often does not render P. syringae avirulent, it can be assumed that P. syringae virulence is multifactorial. Moreover, given the complexity of interactions that occur at the host-pathogen interface, there are likely many additional virulence determinants in P. syringae yet to be discovered.One possible contributor to P. syringae pathogenesis is the twin-arginine translocation (Tat) pathway that operates in the inner membrane of many gram-negative bacteria (4, 5, 56). Tat substrates are synthesized with cleavable N-terminal signal peptides that are characterized by a highly conserved twinarginine motif in the positively charged N-terminal region, a weakly hydrophobic core region, and a positively charged Sec pathway-avoidance signal in the C-terminal region (7,17). The most remarkable feat...

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Section: Resultsmentioning

confidence: 92%

Identification of a Twin-Arginine Translocation System in Pseudomonas syringae pv. tomato DC3000 and Its Contribution to Pathogenicity and Fitness

et al. 2005

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“…Most of the TTSS genes are organized in a cluster of five operons on the P. aeruginosa chromosome. Genes encoding the effector proteins are located elsewhere on the chromosome (20,21,46,(79)(80)(81).…”

Section: Resultsmentioning

confidence: 99%

A Three-Component Regulatory System Regulates Biofilm Maturation and Type III Secretion inPseudomonas aeruginosa

2005

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Biofilms are structured communities found associated with a wide range of surfaces. Here we report the identification of a three-component regulatory system required for biofilm maturation by Pseudomonas aeruginosa strain PA14. A transposon mutation that altered biofilm formation in a 96-well dish assay originally defined this locus, which is comprised of genes for a putative sensor histidine kinase and two response regulators and has been designated sadARS. Nonpolar mutations in any of the sadARS genes result in biofilms with an altered mature structure but do not confer defects in growth or early biofilm formation, swimming, or twitching motility. After 2 days of growth under flowing conditions, biofilms formed by the mutants are indistinguishable from those formed by the wild-type (WT) strain. However, by 5 days, mutant biofilms appear to be more homogeneous than the WT in that they fail to form large and distinct macrocolonies and show a drastic reduction in water channels. We propose that the sadARS three-component system is required for later events in biofilm formation on an abiotic surface. Semiquantitative reverse transcription-PCR analysis showed that there is no detectable change in expression of the sadARS genes when cells are grown in a planktonic culture versus a biofilm, indicating that this locus is not itself induced during or in response to biofilm formation. DNA microarray studies were used to identify downstream targets of the SadARS system. Among the genes regulated by the SadARS system are those required for type III secretion. Mutations in type III secretion genes result in strains with enhanced biofilm formation. We propose a possible mechanism for the role that the SadARS system plays in biofilm formation.

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“…In most cases, multiple genes encoding autotransporters are found throughout the genome sequence of the microorganism, e.g., E. coli (530), Bordetella spp. (382), Yersinia pestis (98), Helicobacter pylori (313), Pseudomonas aeruginosa (306) and Neisseria (91). It has been suggested through genome sequence analysis that the passenger domain is not always covalently linked to the ␤-domain, since some open reading frames (ORFs) code either only for a passenger domain or a ␤-domain.…”

Section: Evolution and Distribution Of Autotransporter Proteinsmentioning

confidence: 99%

Type V Protein Secretion Pathway: the Autotransporter Story

Henderson

Navarro-Garcı́a

Desvaux

et al. 2004

Microbiol Mol Biol Rev

713

795

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Gram-negative bacteria possess an outer membrane layer which constrains uptake and secretion of solutes and polypeptides. To overcome this barrier, bacteria have developed several systems for protein secretion. The type V secretion pathway encompasses the autotransporter proteins, the two-partner secretion system, and the recently described type Vc or AT-2 family of proteins. Since its discovery in the late 1980s, this family of secreted proteins has expanded continuously, due largely to the advent of the genomic age, to become the largest group of secreted proteins in gram-negative bacteria. Several of these proteins play essential roles in the pathogenesis of bacterial infections and have been characterized in detail, demonstrating a diverse array of function including the ability to condense host cell actin and to modulate apoptosis. However, most of the autotransporter proteins remain to be characterized. In light of new discoveries and controversies in this research field, this review considers the autotransporter secretion process in the context of the more general field of bacterial protein translocation and exoprotein function

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Protein secretion systems of Pseudomonas aeruginosa and P. fluorescens

Cited by 92 publications

References 93 publications

Identification of a Twin-Arginine Translocation System in Pseudomonas syringae pv. tomato DC3000 and Its Contribution to Pathogenicity and Fitness

Identification of a Twin-Arginine Translocation System in Pseudomonas syringae pv. tomato DC3000 and Its Contribution to Pathogenicity and Fitness

A Three-Component Regulatory System Regulates Biofilm Maturation and Type III Secretion inPseudomonas aeruginosa

Type V Protein Secretion Pathway: the Autotransporter Story

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