Contribution of the type III secretion system (TTSS) to virulence of Aeromonas salmonicida subsp. salmonicida

Dacanay, Andrew; Knickle, Leah C.; Solanky, Kirty S.; Boyd, Jessica M.; Walter, John A.; Brown, Laura L.; Johnson, Stewart C.; Reith, Michael

doi:10.1099/mic.0.28768-0

Cited by 85 publications

(96 citation statements)

References 36 publications

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“…Invasion of the epithelial layer by Gram-negative bacteria is often mediated by Type III secretion systems (T3SS). Aeromonas salmonicida has a functioning T3SS (Burr et al 2002(Burr et al , 2003 and we have shown it to be critical for virulence in Atlantic salmon (Dacanay et al 2006). The results of the present study suggest that the Fim pili allow A. salmonicida to come into close contact with the gut epithelium.…”

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confidence: 56%

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Aeromonas salmonicida Type I pilus system contributes to host colonization but not invasion

Dacanay¹,

Boyd²,

Fast³

et al. 2010

Dis. Aquat. Org.

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The host-adherence strategies employed by Aeromonas salmonicida subsp. salmonicida, the etiological agent of an infectious bacteremia of salmonids, are poorly understood. In addition to the outer protein coat or S-layer, A. salmonicida has both Type I and Type IV pili loci. The A. salmonicida Type I or Fim pilus is encoded by an operon with genes for a chaperone, an usher, and 3 pilus subunits and is predicted to be similar to the Pap fimbriae of uropathogenic Escherichia coli, which are considered significant virulence factors. A Fim-deficient strain of A. salmonicida strain A449, Δfim, was created by deleting this operon. Virulence of Δfim was unchanged in direct live challenges of Atlantic salmon Salmo salar L., a natural host for A. salmonicida. A measure of clinically inapparent (covert) infections suggested Fim was required to establish or maintain a covert infection. This was confirmed by an ex vivo adherence and invasion assay using freshly excised salmon gastrointestinal (GI) tract, which showed that, compared to the parental strain, the ability of the isogenic Δfim mutant strain to adhere to the salmon GI tract was reduced but, once adhered, its ability to invade was unchanged. Thus the Fim pilus functions as an adhesin in A. salmonicida and the presence of a functional Fim improved the efficiency of A. salmonicida infection of Atlantic salmon. KEY WORDS: Pilin · Adhesin · Furunculosis · VirulenceResale or republication not permitted without written consent of the publisher Dis Aquat Org 88: 199-206, 2010 epithelium by a trans-cellular route and that this translocation requires bacteria with intact and functional surface structures. Our continued interest in A. salmonicida adhesins leads us to ask if we could identify factors important for adherence to salmon intestinal tissue.The most well studied Aeromonas salmonicida adhesin is its outer protein coat, the S-layer, the major protein constituent of which is VapA. While the S-layer has long been demonstrated to be both an important virulence factor and an adhesin (Ishiguro et al. 1981, Trust et al. 1983, Garduño et al. 1992, Kay & Trust 1997, Garduño et al. 2000, VapA-deficient strains may still be infectious (Ellis et al. 1988, Olivier 1990. In addition to the S-layer, A. salmonicida strain A449 also has genes for at least 4 specific adhesion systems: Tap, Flp, MSHA, and Fim (Reith et al. 2008). The first 3 are Type IV pili and have been characterized elsewhere (Masada et al. 2002). The latter system, Fim, is predicted to encode a Type I pilus, similar to the fimbriae of pathogenic Escherichia coli that are considered to be important virulence factors in that organism. The present study reports on the contribution of Fim to A. salmonicida strain A449 virulence as assessed by a Fim-deficient isogenic laboratory strain. MATERIALS AND METHODSBacterial strains and growth conditions. Bacteria and plasmids used in the present study are listed in Table 1. The parental strain for all knockouts was Aeromonas salmonicida subsp. salmonicida strain ...

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confidence: 56%

“…The virulence of the mutant strain Δfim and its parental strain A449 were tested by intraperitoneal (i.p.) and immersion challenges conducted as per Dacanay et al (2006). Briefly, for the immersion challenge there were 2 tanks group -1 with ca.…”

Section: Methodsmentioning

confidence: 99%

Aeromonas salmonicida Type I pilus system contributes to host colonization but not invasion

Dacanay¹,

Boyd²,

Fast³

et al. 2010

Dis. Aquat. Org.

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“…Both intraperitoneal injection and immersion bacterial challenges of Atlantic salmon were conducted as described elsewhere (11). The parental, tapA::KO, and flp::Km strains were tested by immersion challenge in Saint John River Atlantic salmon.…”

Section: Vol 76 2008mentioning

confidence: 99%

“…salmonicida remains poorly understood, and no single characteristic or phenotype was found only in virulent strains (16,17,30,42) until the recent description of an A. salmonicida subsp. salmonicida type III secretion system (6,11).…”

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confidence: 99%

Contribution of Type IV Pili to the Virulence of Aeromonas salmonicida subsp. salmonicida in Atlantic Salmon ( Salmo salar L.)

et al. 2008

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Aeromonas salmonicida subsp. salmonicida, a bacterial pathogen of Atlantic salmon, has no visible pili, yet its genome contains genes for three type IV pilus systems. One system, Tap, is similar to the Pseudomonas aeruginosa Pil system, and a second, Flp, resembles the Actinobacillus actinomycetemcomitans Flp pilus, while the third has homology to the mannose-sensitive hemagglutinin pilus of Vibrio cholerae. The latter system is likely nonfunctional since eight genes, including the gene encoding the main pilin subunit, are deleted compared with the orthologous V. cholerae locus. The first two systems were characterized to investigate their expression and role in pathogenesis. The pili of A. salmonicida subsp. salmonicida were imaged using atomic force microscopy and Tap-and Flp-overexpressing strains. The Tap pili appeared to be polar, while the Flp pili appeared to be peritrichous. Strains deficient in tap and/or flp were used in live bacterial challenges of Atlantic salmon, which showed that the Tap pilus made a moderate contribution to virulence, while the Flp pilus made little or no contribution. Delivery of the tap mutant by immersion resulted in reduced cumulative morbidity compared with the cumulative morbidity observed with the wild-type strain; however, delivery by intraperitoneal injection resulted in cumulative morbidity similar to that of the wild type. Unlike the pili of other piliated bacterial pathogens, A. salmonicida subsp. salmonicida type IV pili are not absolutely required for virulence in Atlantic salmon. Significant differences in the behavior of the two mutant strains indicated that the two pilus systems are not redundant.Aeromonas salmonicida subsp. salmonicida is a gram-negative, nonmotile, rod-shaped bacterium that is the etiologic agent of an infectious bacteremia-septicemia of salmonids known as furunculosis. Furunculosis is a complex disease that exists in different forms depending on the health, age, and species of fish. Many cell-associated and secreted factors have been implicated as virulence determinants in this bacterium (for reviews, see references 5 and 7). Despite this, much of the pathogenesis of A. salmonicida subsp. salmonicida remains poorly understood, and no single characteristic or phenotype was found only in virulent strains (16,17,30,42) until the recent description of an A. salmonicida subsp. salmonicida type III secretion system (6, 11).In order to better understand the virulence strategies employed by A. salmonicida subsp. salmonicida, we have focused on the initial stages of infection: adherence and invasion. Bacteria use complex intercellular mechanisms and specific and nonspecific adhesins to achieve these aims (34). The most well-studied A. salmonicida subsp. salmonicida adhesin is the surface layer or S-layer, sometimes referred to as the A-layer (additional layer) (33). This layer is a nonspecific but important factor for adherence due to its hydrophobic nature.Pili allow bacteria to attach to solid surfaces, including host tissues, and are considered impor...

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“…All these A. salmonicida subsp. salmonicida isolates were grown on furunculosis agar (H€ anninen & Hirvel€ aKoski, 1997) at 18 C for 24 to 72 h since it is at this temperature that this psychrophilic bacterium is usually most efficient at infecting fish (Beaz-Hidalgo & Figueras, 2012;Dacanay et al, 2006;Dautremepuits et al, 2006).…”

Section: Methodsmentioning

confidence: 99%

Antibiotic resistance due to an unusual ColE1-type replicon plasmid in Aeromonas salmonicida

et al. 2016

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Aeromonas salmonicida subsp. salmonicida is a fish pathogen known to have a rich plasmidome. In the present study, we discovered an isolate of this bacterium bearing an additional unidentified small plasmid. After having sequenced the DNA of that isolate by nextgeneration sequencing, it appeared that the new small plasmid is a ColE1-type replicon plasmid, named here pAsa7. This plasmid bears a functional chloramphenicol-acetyltransferase-encoding gene (cat-pAsa7) previously unknown in A. salmonicida and responsible for resistance to chloramphenicol. A comparison of pAsa7 with pAsa2, the only known ColE1-type replicon plasmid usually found in A. salmonicida subsp. salmonicida, revealed that even if both plasmids share a high structural similarity, it is still unclear if pAsa7 is a derivative of pAsa2 since they showed several mutations at the nucleotide level. Transcriptomic analysis revealed that the catpAsa4 gene, another chloramphenicol-acetyltransferase-encoding gene, found on the large plasmid pAsa4, was significantly more transcribed than cat-pAsa7. This was correlated with a higher chloramphenicol resistance for isolates bearing pAsa4 compared with the one having pAsa7. Finally, a phylogenetic analysis showed that both CAT-pAsa4 and CAT-pAsa7 proteins were in different clusters. The clustering was supported by the identity of residues involved in the catalytic site. In addition, to give a better understanding of the large drug-resistance panel of A.salmonicida, this study reinforces the hypothesis that A. salmonicida subsp. salmonicida is a considerable reservoir for mobile genetic elements such as plasmids.

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Contribution of the type III secretion system (TTSS) to virulence of Aeromonas salmonicida subsp. salmonicida

Cited by 85 publications

References 36 publications

Aeromonas salmonicida Type I pilus system contributes to host colonization but not invasion

Aeromonas salmonicida Type I pilus system contributes to host colonization but not invasion

Contribution of Type IV Pili to the Virulence of Aeromonas salmonicida subsp. salmonicida in Atlantic Salmon ( Salmo salar L.)

Antibiotic resistance due to an unusual ColE1-type replicon plasmid in Aeromonas salmonicida

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