Flavobacterium gliding motility and the type IX secretion system

McBride, Mark J.; Nakane, Daisuke

doi:10.1016/j.mib.2015.07.016

Cited by 112 publications

(121 citation statements)

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“…Bioinformatic analyses revealed that the genomes of F. columnare strain IA-S-4 (genomovar I) and F. columnare strain C#2 (genomovar II) had orthologs of the F. johnsoniae T9SS genes gldK, gldL, gldM, gldN, sprA, sprE, sprT, porU, and porV (see Table S1 in the supplemental material). The proteins encoded by these genes are thought to be components of the T9SS (19,21,24). Proteins secreted by T9SSs can often be identified by their conserved C-terminal domains that target them for secretion (24,(28)(29)(30)(31)(32)(33)(34)37).…”

Section: Resultsmentioning

confidence: 99%

“…The T9SS (previously called the Por secretion system) was originally described in the human periodontal pathogen Porphyromonas gingivalis and in the environmental bacterium Flavobacterium johnsoniae (18). T9SSs are common in, but confined to, the phylum Bacteroidetes (19,20). In F. johnsoniae, they are involved in the secretion of cell surface components of the gliding motility apparatus, and thus, the T9SS is required for gliding motility (18,21,22).…”

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confidence: 99%

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The Type IX Secretion System Is Required for Virulence of the Fish Pathogen Flavobacterium columnare

Zhu

LaFrentz

et al. 2017

Appl Environ Microbiol

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Flavobacterium columnare, a member of the phylum Bacteroidetes, causes columnaris disease in wild and aquaculture-reared freshwater fish. The mechanisms responsible for columnaris disease are not known. Many members of the phylum Bacteroidetes use type IX secretion systems (T9SSs) to secrete enzymes, adhesins, and proteins involved in gliding motility. The F. columnare genome has all of the genes needed to encode a T9SS. gldN, which encodes a core component of the T9SS, was deleted in wild-type strains of F. columnare. The F. columnare ΔgldN mutants were deficient in the secretion of several extracellular proteins and lacked gliding motility. The ΔgldN mutants exhibited reduced virulence in zebrafish, channel catfish, and rainbow trout, and complementation restored virulence. PorV is required for the secretion of a subset of proteins targeted to the T9SS. An F. columnare ΔporV mutant retained gliding motility but exhibited reduced virulence. Cell-free spent media from exponentially growing cultures of wild-type and complemented strains caused rapid mortality, but spent media from ΔgldN and ΔporV mutants did not, suggesting that soluble toxins are secreted by the T9SS.IMPORTANCE Columnaris disease, caused by F. columnare, is a major problem for freshwater aquaculture. Little is known regarding the virulence factors produced by F. columnare, and control measures are limited. Analysis of targeted gene deletion mutants revealed the importance of the type IX protein secretion system (T9SS) and of secreted toxins in F. columnare virulence. T9SSs are common in members of the phylum Bacteroidetes and likely contribute to the virulence of other animal and human pathogens.KEYWORDS columnaris disease, gliding motility, type IX secretion system, virulence F lavobacterium columnare is a common fish pathogen that causes columnaris disease (1-3). F. columnare causes epidemics in wild and cultured fish and is a major problem in freshwater aquaculture worldwide, resulting in significant mortality. Many species of freshwater fish are susceptible to columnaris disease (4, 5). The virulence mechanisms of F. columnare are incompletely understood, and current control strategies are inadequate. F. columnare isolates are genetically diverse and have been assigned to multiple genomovars (6, 7). F. columnare genomovars I and II exhibit significant differences, including host ranges (8-10). Described outbreaks in salmonid aquaculture systems have almost invariably been associated with genomovar I strains

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Section: Resultsmentioning

confidence: 99%

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confidence: 99%

The Type IX Secretion System Is Required for Virulence of the Fish Pathogen Flavobacterium columnare

Zhu

LaFrentz

et al. 2017

Appl Environ Microbiol

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“…The external part of the bacterial flagellum is composed of a short proximal hook and a long helical filament made up of flagellin (Fla) sub-units [14]. Seven different TSSs have been described in Gram-negative bacteria: type I to VI and IX (T1SS to T9SS), which are responsible for the export of ‘effector’ proteins into the extracellular milieu or into target host cells [15,16] . T1SS, T2SS, T3SS, T5SS and T6SS can be found in P. aeruginosa .…”

Section: Introductionmentioning

confidence: 99%

Pseudomonas aeruginosa flagellum is critical for invasion, cutaneous persistence and induction of inflammatory response of skin epidermis

Garcia

Morello

Garnier³

et al. 2018

Virulence

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Pseudomonas aeruginosa, an opportunistic pathogen involved in skin and lung diseases, possesses numerous virulence factors, including type 2 and 3 secretion systems (T2SS and T3SS) and its flagellum, whose functions remain poorly known during cutaneous infection. Using isogenic mutants deleted from genes encoding each or all of these three virulence factors, we investigated their role in induction of inflammatory response and in tissue invasiveness in human primary keratinocytes and reconstructed epidermis. Our results showed that flagellum, but not T2SS and T3SS, is involved in induction of a large panel of cytokine, chemokine, and antimicrobial peptide (AMP) mRNA in the infected keratinocytes. Chemokine secretion and AMP tissular production were also dependent on the presence of the bacterial flagellum. This pro-inflammatory effect was significantly reduced in keratinocytes infected in presence of anti-toll-like receptor 5 (TLR5) neutralizing antibody. Bacterial invasion of human epidermis and persistence in a mouse model of sub-cutaneous infection were dependent on the P. aeruginosa flagellum. We demonstrated that flagellum constitutes the main virulence factor of P. aeruginosa involved not only in early induction of the epidermis inflammatory response but also in bacterial invasion and cutaneous persistence. P. aeruginosa is mainly sensed by TLR5 during the early innate immune response of human primary keratinocytes.

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“…The F. johnsoniae genome encodes other SprB-like proteins, such as RemA, which explains why sprB mutants exhibit some residual motility (17). Seven proteins (GldK, GldL, GldM, GldN, SprA, SprE, and SprT) comprise the type IX secretion system (T9SS) that is required for the delivery of SprB to the cell surface and for the secretion of dozens of other cell surface and extracellular proteins (14,15,18,19). SprF is also needed for the secretion of SprB but not for the secretion of other proteins targeted to the T9SS (13).…”

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Comparative Analysis of Cellulophaga algicola and Flavobacterium johnsoniae Gliding Motility

Zhu

McBride

2016

J Bacteriol

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Gliding motility is common in members of the phylum Bacteroidetes, including Flavobacterium johnsoniae and Cellulophaga algicola. F. johnsoniae gliding has been extensively studied and involves rapid movement of the cell surface adhesin SprB. Genetic analysis of C. algicola allowed a comparative analysis of gliding. Sixty-three HimarEm1-induced mutants that formed nonspreading colonies were characterized. Each had an insertion in an ortholog of an F. johnsoniae motility gene, highlighting similarities between the motility systems. Differences were also observed. C. algicola lacks orthologs of the F. johnsoniae motility genes gldA, gldF, and gldG that are thought to encode the components of an ATP-binding cassette (ABC) transporter. In addition, mutations in any of 12 F. johnsoniae gld genes result in complete loss of motility, whereas all C. algicola gld mutants retained slight residual motility. This may indicate that C. algicola has multiple motility systems, that the motility proteins exhibit partial redundancy of function, or that essential components of the motility machinery of both C. algicola and F. johnsoniae remain to be discovered. IMPORTANCEThe development of genetic tools for C. algicola and comparative analysis of F. johnsoniae and C. algicola motility mutants identified similarities and differences between their gliding motility machineries. Gliding motility is common in the phylum Bacteroidetes. Proteins that are important for gliding in both C. algicola and F. johnsoniae are potential core components of the Bacteroidetes gliding motility machinery. Many bacteria belonging to the phylum Bacteroidetes exhibit rapid gliding motility over surfaces (1). Gliding has been most well studied in Flavobacterium johnsoniae, in which the disruption of any of 11 gld genes (gldA, gldB, gldD, gldF, gldG, gldH, gldI, gldJ, gldK, gldL, and gldM) or deletion of gldN and its paralog gldO results in a complete loss of motility (2-10). These gld mutants form nonspreading colonies on agar, and individual cells exhibit no movement on glass or agar. Mutations in other F. johnsoniae genes (sprA, sprB, sprC, sprD, sprE, sprF, and sprT) result in partial motility defects (11-15). These spr mutants form nonspreading colonies composed of cells that exhibit some limited ability to glide on glass surfaces.sprB encodes an adhesin that is propelled rapidly along the cell surface and is thought to account for much of the gliding movement of F. johnsoniae (11, 16). The F. johnsoniae genome encodes other SprB-like proteins, such as RemA, which explains why sprB mutants exhibit some residual motility (17). Seven proteins (GldK, GldL, GldM, GldN, SprA, SprE, and SprT) comprise the type IX secretion system (T9SS) that is required for the delivery of SprB to the cell surface and for the secretion of dozens of other cell surface and extracellular proteins (14,15,18,19). SprF is also needed for the secretion of SprB but not for the secretion of other proteins targeted to the T9SS (13). The motor that propels SprB along the cel...

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Flavobacterium gliding motility and the type IX secretion system

Cited by 112 publications

References 43 publications

The Type IX Secretion System Is Required for Virulence of the Fish Pathogen Flavobacterium columnare

The Type IX Secretion System Is Required for Virulence of the Fish Pathogen Flavobacterium columnare

Pseudomonas aeruginosa flagellum is critical for invasion, cutaneous persistence and induction of inflammatory response of skin epidermis

Comparative Analysis of Cellulophaga algicola and Flavobacterium johnsoniae Gliding Motility

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