Burkholderia cenocepacia Lipopolysaccharide Modification and Flagellin Glycosylation Affect Virulence but Not Innate Immune Recognition in Plants

Khodai-Kalaki, Maryam; Andrade, Ángel; Mohamed, Yasmine Fathy; Valvano, Miguel A.

doi:10.1128/mbio.00679-15

Cited by 17 publications

(20 citation statements)

References 61 publications

(90 reference statements)

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“…The flagellin of the plant pathogens Pseudomonas syringae pv tabaci and Burkholderia cenocepacia are also glycosylated, and the absence of this modification lowered the ability of these bacteria to cause disease on tobacco and Arabidopsis , respectively (Khodai‐Kalaki et al. , ; Taguchi et al. , ).…”

Section: Resultsmentioning

confidence: 99%

Identification by Tn‐seq of Dickeya dadantii genes required for survival in chicory plants

Royet

Parisot

Rodrigue

et al. 2018

Molecular Plant Pathology

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Summary The identification of the virulence factors of plant‐pathogenic bacteria has relied on the testing of individual mutants on plants, a time‐consuming process. Transposon sequencing (Tn‐seq) is a very powerful method for the identification of the genes required for bacterial growth in their host. We used this method in a soft‐rot pathogenic bacterium to identify the genes required for the multiplication of Dickeya dadantii in chicory. About 100 genes were identified showing decreased or increased fitness in the plant. Most had no previously attributed role in plant–bacterium interactions. Following our screening, in planta competition assays confirmed that the uridine monophosphate biosynthesis pathway and the purine biosynthesis pathway were essential to the survival of D. dadantii in the plant, as the mutants ∆ carA , ∆ purF , ∆ purL , ∆ guaB and ∆ pyrE were unable to survive in the plant in contrast with the wild‐type (WT) bacterium. This study also demonstrated that the biosynthetic pathways of leucine, cysteine and lysine were essential for bacterial survival in the plant and that RsmC and GcpA were important in the regulation of the infection process, as the mutants ∆ rsmC and ∆ gcpA were hypervirulent. Finally, our study showed that D. dadantii flagellin was glycosylated and that this modification conferred fitness to the bacterium during plant infection. Assay by this method of the large collections of environmental pathogenic strains now available will allow an easy and rapid identification of new virulence factors.

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Section: Resultsmentioning

confidence: 99%

Identification by Tn‐seq of Dickeya dadantii genes required for survival in chicory plants

Royet

Parisot

Rodrigue

et al. 2018

Molecular Plant Pathology

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“…Also, B. cenocepacia can be transmitted from patient to patient (Drevinek & Mahenthiralingam, 2010). B. cenocepacia is pathogenic in several plant and non-mammalian animal infection models (Khodai-Kalaki et al, 2015;Thomson & Dennis, 2013;Uehlinger et al, 2009;Vergunst et al, 2010) and can survive intracellularly within epithelial cells (Burns et al, 1996;Sajjan et al, 2006), macrophages (Lamothe et al, 2007;Martin & Mohr, 2000;Saini et al, 1999) and amoebae (Lamothe et al, 2004;Marolda et al, 1999).…”

Section: Introductionmentioning

confidence: 99%

Quantification of type VI secretion system activity in macrophages infected with Burkholderia cenocepacia

Aubert

Valvano

2015

Microbiology

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The Gram-negative bacterial type VI secretion system (T6SS) delivers toxins to kill or inhibit the growth of susceptible bacteria, while other secretion systems target eukaryotic cells. Deletion of atsR, a negative regulator of virulence factors in B. cenocepacia K56-2, increases T6SS activity. Macrophages infected with a K56-2 DatsR mutant display dramatic alterations in their actin cytoskeleton architecture that rely on the T6SS, which is responsible for the inactivation of multiple Rho-family GTPases by an unknown mechanism. We employed a strategy to standardize the bacterial infection of macrophages and densitometrically quantify the T6SS-associated cellular phenotype, which allowed us to characterize the phenotype of systematic deletions of each gene within the T6SS cluster and ten vgrG genes in K56-2 DatsR. None of the genes from the T6SS core cluster nor the individual vgrG genes were directly responsible for the cytoskeletal changes in infected cells. However, a mutant strain with all vgrG genes deleted was unable to cause macrophage alterations. Despite not being able to identify a specific effector protein responsible for the cytoskeletal defects in macrophages, our strategy resulted in the identification of the critical core components and accessory proteins of the T6SS assembly machinery and provides a screening method to detect T6SS effectors targeting the actin cytoskeleton in macrophages by random mutagenesis.

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“…). This is in contrast with the current view that flagellin glycosylation functions to evade the plant surveillance system (Hanuszkiewicz et al ., ; Khodai‐Kalaki et al ., ; Taguchi et al ., ). Second, the bacterial glycan composition itself, other than flagellin, which is generated through the GigX pathway, may act directly as a PAMP for PTI induction in rice.…”

Section: Discussionmentioning

confidence: 99%

“…Although flagellin glycosylation has been revealed in further pathogenic bacteria, in many cases, its biological function remains to be elucidated (Logan, 2006;Merino and Tomas, 2014). In general, flagellin glycosylation affects filament assembly, stability and flagellar motility (Asakura et al, 2010;Guerry et al, 2006;Taguchi et al, 2006Taguchi et al, , 2008Taguchi et al, , 2010, virulence (Khodai-Kalaki et al, 2015;Lithgow et al, 2014), host specificity, recognition and innate immune evasion (Logan, 2006;Nothaft and Szymanski, 2010). Flagellin glycosylation has been implicated in the regulation of bacterial virulence and interactions with the host in several pathogenic bacteria (Arora et al, 2005;Khodai-Kalaki et al, 2015;Taguchi et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

A ten gene‐containing genomic island determines flagellin glycosylation: implication for its regulatory role in motility and virulence of Xanthomonas oryzae pv. oryzae

Chen

Tian

et al. 2017

Molecular Plant Pathology

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Flagellin glycosylation plays a crucial role in flagellar assembly, motility and virulence in several pathogenic bacteria. However, little is known about the genetic determinants and biological functions of flagellin glycosylation in Xanthomonas oryzae pv. oryzae (Xoo), the causal pathogen of bacterial blight of rice. Here, the structure, regulation and functions of a ten-gene cluster gigX (glycosylation island genes of Xoo), which was embedded in a flagellar regulon, were characterized. gigX1 to gigX10 encoded putative enzymes or proteins involved in glycan biosynthesis and transfer, including a nucleotide sugar transaminase, an acyl-carrier protein (ACP), a 3-oxoacyl-ACP synthase, a 3-oxoacyl-ACP reductase, a dehydrogenase, an acetyltransferase, a ring hydroxylating dioxygenase, a hypothetical protein, a methyltransferanse and a glycosyltransferase, respectively. The gigX genes were co-transcribed in an operon and up-regulated by the upstream σ factor RpoN2 and transcriptional activator FleQ. In-frame deletion of each gigX gene affected flagellin glycosylation modification, meaning that the unglycosylated flagellin of the mutants was smaller than the glycosylated flagellin of the wild-type. No significant changes in flagellar filament and motility were observed in the ΔgigX mutants, among which only ΔgigX6 displayed increased swimming ability. Importantly, all mutants, except ΔgigX9, showed significantly increased virulence and bacterial growth in the susceptible rice cultivar IR24, and ΔgigX1 and ΔgigX10 showed enhanced type III secretion system (T3SS)-related gene expression. Moreover, the glycosylated flagellin of the wild-type induced higher H O levels in rice leaves than did the unglycosylated flagellins of ΔgigX1 or ΔgigX10. Taken together, this study reveals that the gigX cluster determines flagellin glycosylation, and implicates the regulatory role of post-translational modification with the glycosylation, acetylation and methylation of flagellin in the regulation of motility and virulence of Xoo.

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Burkholderia cenocepacia Lipopolysaccharide Modification and Flagellin Glycosylation Affect Virulence but Not Innate Immune Recognition in Plants

Cited by 17 publications

References 61 publications

Identification by Tn‐seq of Dickeya dadantii genes required for survival in chicory plants

Identification by Tn‐seq of Dickeya dadantii genes required for survival in chicory plants

Quantification of type VI secretion system activity in macrophages infected with Burkholderia cenocepacia

A ten gene‐containing genomic island determines flagellin glycosylation: implication for its regulatory role in motility and virulence of Xanthomonas oryzae pv. oryzae

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