Diversification of the Type VI Secretion System in Agrobacteria

Wu, Chih-Feng; Weisberg, Alexandra J.; Davis, Edward W.; Chou, Li-Dek; Khan, Surtaz; Lai, Erh‐Min; Kuo, Chih-Horng; Chang, Jeff H.

doi:10.1128/mbio.01927-21

Cited by 19 publications

(22 citation statements)

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“…tumefaciens , activation of the T6SS results in the production of a contractile nanomachine which delivers effector proteins to antagonize and compete with other bacteria [ 28 ]. Among agrobacteria, T6SS is activated by different signals, is important during different stages of the lifecycle, and may be used to acquire nutrients [ 29 ]. To determine if the T6SS contributes to the spreading response observed during PBP1a depletion we deleted the intergenic gap between the hcp and imp operons (ΔT6SSpro).…”

Section: Resultsmentioning

confidence: 99%

Activation of ChvG-ChvI regulon by cell wall stress confers resistance to β-lactam antibiotics and initiates surface spreading in Agrobacterium tumefaciens

et al. 2022

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A core component of nearly all bacteria, the cell wall is an ideal target for broad spectrum antibiotics. Many bacteria have evolved strategies to sense and respond to antibiotics targeting cell wall synthesis, especially in the soil where antibiotic-producing bacteria compete with one another. Here we show that cell wall stress caused by both chemical and genetic inhibition of the essential, bifunctional penicillin-binding protein PBP1a prevents microcolony formation and activates the canonical host-invasion two-component system ChvG-ChvI in Agrobacterium tumefaciens. Using RNA-seq, we show that depletion of PBP1a for 6 hours results in a downregulation in transcription of flagellum-dependent motility genes and an upregulation in transcription of type VI secretion and succinoglycan biosynthesis genes, a hallmark of the ChvG-ChvI regulon. Depletion of PBP1a for 16 hours, results in differential expression of many additional genes and may promote a stress response, resembling those of sigma factors in other bacteria. Remarkably, the overproduction of succinoglycan causes cell spreading and deletion of the succinoglycan biosynthesis gene exoA restores microcolony formation. Treatment with cefsulodin phenocopies depletion of PBP1a and we correspondingly find that chvG and chvI mutants are hypersensitive to cefsulodin. This hypersensitivity only occurs in response to treatment with β-lactam antibiotics, suggesting that the ChvG-ChvI pathway may play a key role in resistance to antibiotics targeting cell wall synthesis. Finally, we provide evidence that ChvG-ChvI likely has a conserved role in conferring resistance to cell wall stress within the Alphaproteobacteria that is independent of the ChvG-ChvI repressor ExoR.

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Section: Resultsmentioning

confidence: 99%

Activation of ChvG-ChvI regulon by cell wall stress confers resistance to β-lactam antibiotics and initiates surface spreading in Agrobacterium tumefaciens

et al. 2022

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“…In A. tumefaciens , activation of the T6SS results in the production of a contractile nanomachine which delivers effector proteins to antagonize and compete with other bacteria [27]. Among agrobacteria, T6SS is activated by different signals, is important during different stages of the lifecycle, and may be used to acquire nutrients [28]. To determine if the T6SS contributes to the spreading response observed during PBP1a depletion we deleted the intergenic gap between the hcp and imp operons (ΔT6SSpro).…”

Section: Resultsmentioning

confidence: 99%

Activation of ChvG-ChvI regulon by cell wall stress confers resistance to β-lactam antibiotics and initiates surface spreading inAgrobacterium tumefaciens

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et al. 2022

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A core component of nearly all bacteria, the cell wall is an ideal target for broad spectrum antibiotics. Many bacteria have evolved strategies to sense and respond to antibiotics targeting cell wall synthesis, especially in the soil where antibiotic-producing bacteria compete with one another. Here we show that cell wall stress caused by both chemical and genetic inhibition of the essential, bifunctional penicillin-binding protein PBP1a prevents microcolony formation and activates the canonical host-invasion two-component system ChvG-ChvI in Agrobacterium tumefaciens. Using RNA-seq, we show that depletion of PBP1a for 6 hours results in a downregulation in transcription of flagellum-dependent motility genes and an upregulation in transcription of type VI secretion and succinoglycan biosynthesis genes, a hallmark of the ChvG-ChvI regulon. Depletion of PBP1a for 16 hours, results in differential expression of many additional genes and may promote a general stress response. Remarkably, the overproduction of succinoglycan causes cell spreading and deletion of the succinoglycan biosynthesis gene exoA restores microcolony formation. Treatment with cefsulodin phenocopies depletion of PBP1a and we correspondingly find that chvG and chvI mutants are hypersensitive to cefsulodin. This hypersensitivity only occurs in response to treatment β-lactam antibiotics and moenomycin, suggesting that the ChvG-ChvI pathway may play a key role in resistance to antibiotics targeting cell wall synthesis. Finally, we provide evidence that ChvG-ChvI likely has a conserved role in conferring resistance to cell wall stress within the Alphaproteobacteria.

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“…In addition to core genes, we also observed reticulations in phylogenetic network, indicating frequent exchange of Hcp and VgrG among Xanthomonas species. Such events of reshuffling of VgrG and Hcp have been observed as a strong force in diversification of effector-immunity proteins in many genera, such as Agrobacterium and Vibrio ( Salomon et al, 2015 ; Thomas et al, 2017 ; Wu et al, 2021 ). Although it is true that poorly resolved phylogenies or phylogenies of closely related strains with low branch support could appear as reticulations in the network, reticulations observed specifically for distantly related species suggest that recombination could be a highly likely explanation in those cases.…”

Section: Discussionmentioning

confidence: 99%

Phylogenetic Distribution and Evolution of Type VI Secretion System in the Genus Xanthomonas

et al. 2022

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The type VI secretion system (T6SS) present in many Gram-negative bacteria is a contact-dependent apparatus that can directly deliver secreted effectors or toxins into diverse neighboring cellular targets including both prokaryotic and eukaryotic organisms. Recent reverse genetics studies with T6 core gene loci have indicated the importance of functional T6SS toward overall competitive fitness in various pathogenic Xanthomonas spp. To understand the contribution of T6SS toward ecology and evolution of Xanthomonas spp., we explored the distribution of the three distinguishable T6SS clusters, i3*, i3***, and i4, in approximately 1,740 Xanthomonas genomes, along with their conservation, genetic organization, and their evolutionary patterns in this genus. Screening genomes for core genes of each T6 cluster indicated that 40% of the sequenced strains possess two T6 clusters, with combinations of i3*** and i3* or i3*** and i4. A few strains of Xanthomonas citri, Xanthomonas phaseoli, and Xanthomonas cissicola were the exception, possessing a unique combination of i3* and i4. The findings also indicated clade-specific distribution of T6SS clusters. Phylogenetic analysis demonstrated that T6SS clusters i3* and i3*** were probably acquired by the ancestor of the genus Xanthomonas, followed by gain or loss of individual clusters upon diversification into subsequent clades. T6 i4 cluster has been acquired in recent independent events by group 2 xanthomonads followed by its spread via horizontal dissemination across distinct clades across groups 1 and 2 xanthomonads. We also noted reshuffling of the entire core T6 loci, as well as T6SS spike complex components, hcp and vgrG, among different species. Our findings indicate that gain or loss events of specific T6SS clusters across Xanthomonas phylogeny have not been random.

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Diversification of the Type VI Secretion System in Agrobacteria

Abstract: The T6SS is used by several taxa of Gram-negative bacteria to secrete toxic effector proteins to attack others. Diversification of effector collections shapes bacterial interactions and impacts the health of hosts and ecosystems in which bacteria reside.

Cited by 19 publications

References 75 publications

Activation of ChvG-ChvI regulon by cell wall stress confers resistance to β-lactam antibiotics and initiates surface spreading in Agrobacterium tumefaciens

Activation of ChvG-ChvI regulon by cell wall stress confers resistance to β-lactam antibiotics and initiates surface spreading in Agrobacterium tumefaciens

Activation of ChvG-ChvI regulon by cell wall stress confers resistance to β-lactam antibiotics and initiates surface spreading inAgrobacterium tumefaciens

Phylogenetic Distribution and Evolution of Type VI Secretion System in the Genus Xanthomonas

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