The involvement of the PilQ secretin of type IV pili in phage infection in Ralstonia solanacearum

Narulita, Erlia; Addy, Hardian Susilo; Kawasaki, Takeru; Fujie, Makoto; Yamada, Takashi

doi:10.1016/j.bbrc.2015.12.071

Cited by 14 publications

(14 citation statements)

References 41 publications

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“…Besides their roles in natural transformation and biofilm formation, TFP are also key for bacterial virulence (7). In R. solanacearum, virulence processes during plant colonization have been investigated in some TFP-related genes such as pilA (8) and pilQ (30), highlighting the relationship between twitching motility and virulence (31)(32)(33). Our data demonstrate that PilI and ChpA proteins are required for early pathogenic stages that result in effective plant colonization and wilting.…”

Section: Discussionmentioning

confidence: 79%

Twitching and Swimming Motility Play a Role in Ralstonia solanacearum Pathogenicity

Corral

Sebastià

Coll

et al. 2020

mSphere

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Ralstonia solanacearum is a bacterial plant pathogen causing important economic losses worldwide. In addition to the polar flagella responsible for swimming motility, this pathogen produces type IV pili (TFP) that govern twitching motility, a flagellum-independent movement on solid surfaces. The implication of chemotaxis in plant colonization, through the control flagellar rotation by the proteins CheW and CheA, has been previously reported in R. solanacearum. In this work, we have identified in this bacterium homologues of the Pseudomonas aeruginosa pilI and chpA genes, suggested to play roles in TFP-associated motility analogous to those played by the cheW and cheA genes, respectively. We demonstrate that R. solanacearum strains with a deletion of the pilI or the chpA coding region show normal swimming and chemotaxis but altered biofilm formation and reduced twitching motility, transformation efficiency, and root attachment. Furthermore, these mutants displayed wild-type growth in planta and impaired virulence on tomato plants after soil-drench inoculations but not when directly applied to the xylem. Comparison with deletion mutants for pilA and fliC-encoding the major pilin and flagellin subunits, respectively-showed that both twitching and swimming are required for plant colonization and full virulence. This work proves for the first time the functionality of a pilus-mediated pathway encoded by pil-chp genes in R. solanacearum, demonstrating that pilI and chpA genes are bona fide motility regulators controlling twitching motility and its three related phenotypes: virulence, natural transformation, and biofilm formation. IMPORTANCE Twitching and swimming are two bacterial movements governed by pili and flagella. The present work identifies for the first time in the Gram-negative plant pathogen Ralstonia solanacearum a pilus-mediated chemotaxis pathway analogous to that governing flagellum-mediated chemotaxis. We show that regulatory genes in this pathway control all of the phenotypes related to pili, including twitching motility, natural transformation, and biofilm formation, and are also directly implicated in virulence, mainly during the first steps of the plant infection. Our results show that pili have a higher impact than flagella on the interaction of R. solanacearum with tomato plants and reveal new types of cross-talk between the swimming and twitching motility phenotypes: enhanced swimming in bacteria lacking pili and a role for the flagellum in root attachment.

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Section: Discussionmentioning

confidence: 79%

Twitching and Swimming Motility Play a Role in Ralstonia solanacearum Pathogenicity

Corral

Sebastià

Coll

et al. 2020

mSphere

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“…The RSM1‐like phages (including RSM3, and Rs551) have been implicated in cooperatively trading away virulence to acquire drug resistance in a plant disease model. This the phage does by reducing Ralstonia 's production of extracellular polysaccharide, reducing twitching motility, increasing cell aggregation and reducing the expression of key virulence genes . Given the phage modifies the host to ameliorate virulence, they have been proposed as biocontrol agents .…”

Section: Escherichia Coli Ff: the Archetypal Filamentous Phagementioning

confidence: 99%

Filamentous phages: masters of a microbial sharing economy

2019

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Bacteriophage (“bacteria eaters”) or phage is the collective term for viruses that infect bacteria. While most phages are pathogens that kill their bacterial hosts, the filamentous phages of the sub‐class Inoviridae live in cooperative relationships with their bacterial hosts, akin to the principal behaviours found in the modern‐day sharing economy: peer‐to‐peer support, to offset any burden. Filamentous phages impose very little burden on bacteria and offset this by providing service to help build better biofilms, or provision of toxins and other factors that increase virulence, or modified behaviours that provide novel motile activity to their bacterial hosts. Past, present and future biotechnology applications have been built on this phage–host cooperativity, including DNA sequencing technology, tools for genetic engineering and molecular analysis of gene expression and protein production, and phage‐display technologies for screening protein–ligand and protein–protein interactions. With the explosion of genome and metagenome sequencing surveys around the world, we are coming to realize that our knowledge of filamentous phage diversity remains at a tip‐of‐the‐iceberg stage, promising that new biology and biotechnology are soon to come.

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“…In the case of Gram-negative bacteria, phages are known to recognize different structures on the outer membrane such as sugar moieties and membrane proteins [16]. Indeed, different sites on the outer surface of bacterial phytopathogens such as exopolysaccharides, colanic acid residues, lipopolysaccharides, and type IV pili are described as crucial for phage attachment and infection [17][18][19][20].…”

Section: Introductionmentioning

confidence: 99%

Preparing for the KIL: Receptor Analysis of Pseudomonas syringae pv. porri Phages and Their Impact on Bacterial Virulence

Holtappels

Kerremans

Busschots

et al. 2020

IJMS

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The prevalence of Pseudomonas syringae pv. porri (Pspo) in Belgium continues to increase and sustainable treatments for this pathogen remain unavailable. A potentially attractive biocontrol strategy would be the application of bacteriophages. The ideal application strategy of phages in an agricultural setting remains unclear, especially in a field-based production such as for leek plants in Flanders. Therefore, more insight in bacteria–phage interaction is required, along with the evaluation of different application strategies. In this study, we further characterized the infection strategy of two Pspo phages, KIL3b and KIL5. We found that both phages recognize lipopolysaccharide (LPS) moieties on the surface of the bacterium. LPS is an important pathogenicity factor of Pspo. Our data also suggest that KIL5 requires an additional protein in the bacterial cytoplasmatic membrane to efficiently infect its host. Virulence tests showed that this protein also contributes to Pspo virulence. Furthermore, a cocktail of both phages was applied in a seed bioassay. A combination of KIL3b and KIL5 reduced the bacterial concentration 100-fold. However, in vitro Pspo resistance against phage infection developed quite rapidly. However, the impact of this phage resistance might be mitigated as is suggested by the fact that those resistance mutations preferably occur in genes involved in LPS metabolism, and that the virulence of those mutants is possibly reduced. Our data suggest that the phage cocktail has promising potential to lower the prevalence of Pspo and to be integrated in a pest management strategy. Targeted research is needed to further explore the applicability of the phages in combination with other disease control strategies.

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The involvement of the PilQ secretin of type IV pili in phage infection in Ralstonia solanacearum

Cited by 14 publications

References 41 publications

Twitching and Swimming Motility Play a Role in Ralstonia solanacearum Pathogenicity

Twitching and Swimming Motility Play a Role in Ralstonia solanacearum Pathogenicity

Filamentous phages: masters of a microbial sharing economy

Preparing for the KIL: Receptor Analysis of Pseudomonas syringae pv. porri Phages and Their Impact on Bacterial Virulence

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