Conjugative Transfer of Acute Hepatopancreatic Necrosis Disease-Causing pVA1-Type Plasmid Is Mediated by a Novel Self-Encoded Type IV Secretion System

Wang, Dehao; Wang, Liying; Bi, Dexi; Song, Jipeng; Wang, Guohao; Gao, Ye; Tang, Kathy F.J.; Meng, Fanzeng; Xie, Jingmei; Zhang, Fan; Huang, Jie; Li, Jianliang; Dong, Xuan

doi:10.1128/spectrum.01702-22

Cited by 5 publications

(4 citation statements)

References 55 publications

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“…It can, however, not be excluded that substrate recognition is mediated by TraG which is encoded next to the virB T4S gene cluster on plasmid pXCV38 and shares 23% amino acid identity with VirD4 ( Figure 1 and Figure S2 ). Since TraG-like proteins were shown to contribute to T4S ( Schröder et al., 2002 ; Khara et al., 2021 ; Wang et al., 2022 ), we analyzed a possible interaction of TraG with components and putative T4S substrates of the VirB-like T4S system. When analyzed by BACTH assays, TraG interacted with itself, with the predicted ATPase VirB11 and the structural component VirB10 but not with the potential T4S substrate TraI ( Figure S2 ).…”

Section: Resultsmentioning

confidence: 99%

Functional characterization of VirB/VirD4 and Icm/Dot type IV secretion systems from the plant-pathogenic bacterium Xanthomonas euvesicatoria

Drehkopf,

Scheibner,

Büttner

2023

Front. Cell. Infect. Microbiol.

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IntroductionMany Gram-negative plant- and animal-pathogenic bacteria employ type IV secretion (T4S) systems to transport proteins or DNA/protein complexes into eukaryotic or bacterial target cells. T4S systems have been divided into minimized and expanded T4S systems and resemble the VirB/VirD4 T4S system from the plant pathogen Agrobacterium tumefaciens and the Icm/Dot T4S system from the human pathogen Legionella pneumophila, respectively. The only known plant pathogen with both types of T4S systems is Xanthomonas euvesicatoria which is the causal agent of bacterial spot disease on pepper and tomato plants.Results and discussionIn the present study, we show that virB/virD4 and icm/dot T4S genes are expressed and encode components of oligomeric complexes corresponding to known assemblies of VirB/VirD4 and Icm/Dot proteins. Both T4S systems are dispensable for the interaction of X. euvesicatoria with its host plants and do not seem to confer contact-dependent lysis of other bacteria, which was previously shown for the chromosomally encoded VirB/VirD4 T4S system from Xanthomonas axonopodis pv. citri. The corresponding chromosomal T4S gene cluster from X. euvesicatoria is incomplete, however, the second plasmid-localized vir gene cluster encodes a functional VirB/VirD4 T4S system which contributes to plasmid transfer. In agreement with this finding, we identified the predicted relaxase TraI as substrate of the T4S systems from X. euvesicatoria. TraI and additional candidate T4S substrates with homology to T4S effectors from X. axonopodis pv. citri interact with the T4S coupling protein VirD4. Interestingly, however, the predicted C-terminal VirD4-binding sites are not sufficient for T4S, suggesting the contribution of additional yet unknown mechanisms to the targeting of T4S substrates from X. euvesicatoria to both VirB/VirD4 and Icm/Dot T4S systems.

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Section: Resultsmentioning

confidence: 99%

Functional characterization of VirB/VirD4 and Icm/Dot type IV secretion systems from the plant-pathogenic bacterium Xanthomonas euvesicatoria

Drehkopf,

Scheibner,

Büttner

2023

Front. Cell. Infect. Microbiol.

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“…For example, a draft genome sequence showed that a V. harveyi isolate could cause AHPND in shrimp in northern Vietnam ( 16 ) . Studies showed that plasmid-mediated interspecies transfer of the hazard genes could have occurred in different Vibrio species, including V. parahaemolyticus , V. campbellii , and V. owensii ( 17 , 18 ) and that conjugative transfer of the AHPND-causing pVA1-type plasmid carrying the hazard genes is mediated by a novel self-encoded type IV secretion system ( 19 ). Such methodologies provide direct guidelines for uncovering the virulence factors and pathogenic mechanism of Vp TPD .…”

Section: Discussionmentioning

confidence: 99%

Vibrio parahaemolyticus becomes lethal to post-larvae shrimp via acquiring novel virulence factors

Liu,

Wang,

Jia

et al. 2023

Microbiol Spectr

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Translucent post-larvae disease (TPD), caused by Vibrio parahaemolyticus ( Vp TPD ), has become an emerging shrimp disease, affecting more than 70%–80% of coastal shrimp nurseries in China in spring 2020. Here, we investigated the key virulence factors of Vp TPD by analyzing protein fragments, related genomic information, as well as experimental challenge tests. After investigating the toxic effects of purified protein fragments with different molecular weights (MWs) from Vp TPD, we found that only the protein fragments with MW >100 kDa showed similar lethality to live Vp TPD in the experimental challenge test using post-larvae shrimp. Meanwhile, similar histopathological changes exhibiting in the hepatopancreas and midgut of the diseased individuals were observed in the post-larvae shrimp challenged with either bacterial protein fragments (MW >100 kDa) or live Vp TPD . Based on sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) and mass spectrometry analyses, two novel proteins, Vibrio high virulent protein (VHVP)-1 and VHVP-2, were identified as the candidates of key virulence factors to cause TPD. Moreover, VHVP-1 and VHVP-2 were found to be encoded by two genes ( vhvp-1 and vhvp-2 ) tandemly located on a 187,791-bp plasmid and were predicted to depend on the same promoter following a comparative genomic analysis. Further epidemiological investigation and challenge test indicated that the V. parahaemolyticus isolate carrying only the vhvp-1 gene and lacking vhvp-2 gene could not cause mortality of experimental Penaeus vannamei post-larvae. The mutant (Δvhvp-2) by deleting vhvp-2 gene could only cause 4.92% of accumulative mortality of post-larvae that is similar to the non- Vp TPD Vibrio strain. Additionally, the complemented strains, Δvhvp-2/pBT3-vhvp-2 and Δvhvp-2/pwtCas9-vhvp-2, showed similar virulence to the wild-type Vp TPD . The results demonstrated that V. parahaemolyticus becomes lethal to post-larval shrimp by acquiring the VHVP-2 virulence factor. This study sheds light on further investigations of the pathogenic mechanism of Vp TPD and the development of strategies for early diagnosis of TPD in shrimp hatcheries. As a severe emerging shrimp disease, TPD has heavily impacted the shrimp aquaculture industry and resulted in serious economic losses in China since spring 2020. This study aimed to identify the key virulent factors and related genes of the Vp TPD , for a better understanding of its pathogenicity of the novel highly lethal infectious pathogen, as well as its molecular epidemiological characteristics in China. The present study revealed that a novel protein, Vibrio high virulent protein-2 (MW >100 kDa), is responsible to the lethal virulence of V. parahaemolyticus to shrimp post-larvae. The results are essential for effectively diagnosing and monitoring novel pathogenic bacteria, like Vp TPD , in aquaculture shrimps and would be beneficial to the fisheries department in early warning of Vp TPD emergence and developing prevention strategies to reduce economic losses due to severe outbreaks of TPD. Elucidation of the key virulence genes and genomics of Vp TPD could also provide valuable information on the evolution and ecology of this emerging pathogen in aquaculture environments.

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“…As shown in Table 1 , 5 different Vibrio species have so far been confirmed to contain pirA/pirB genes in their plasmids. Several studies have revealed that different Vibrio species may transfer pVA1-like plasmid from an AHPND-causative strain to a non-AHPND-causative strain through horizontal transfer [ 31 – 34 ] . It should also be noted that transposase genes are usually found around the Vibrio pirA/pirB genes [ 3 , 9 , 22 , 35 – 36 ] .…”

Section: Ahpnd-causing Pira Vp /Pirb ...mentioning

confidence: 99%

A bacterial binary toxin system that kills both insects and aquatic crustaceans: Photorhabdus insect-related toxins A and B

et al. 2023

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Photorhabdus insect-related toxins A and B (PirA and PirB) were first recognized as insecticidal toxins from Photorhabdus luminescens. However, subsequent studies showed that their homologs from Vibrio parahaemolyticus also play critical roles in the pathogenesis of acute hepatopancreatic necrosis disease (AHPND) in shrimps. Based on the structural features of the PirA/PirB toxins, it was suggested that they might function in the same way as a Bacillus thuringiensis Cry pore-forming toxin. However, unlike Cry toxins, studies on the PirA/PirB toxins are still scarce, and their cytotoxic mechanism remains to be clarified. In this review, based on our studies of V. parahaemolyticus PirAvp/PirBvp, we summarize the current understanding of the gene locations, expression control, activation, and cytotoxic mechanism of this type of toxin. Given the important role these toxins play in aquatic disease and their potential use in pest control applications, we also suggest further topics for research. We hope the information presented here will be helpful for future PirA/PirB studies.

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Conjugative Transfer of Acute Hepatopancreatic Necrosis Disease-Causing pVA1-Type Plasmid Is Mediated by a Novel Self-Encoded Type IV Secretion System

Cited by 5 publications

References 55 publications

Functional characterization of VirB/VirD4 and Icm/Dot type IV secretion systems from the plant-pathogenic bacterium Xanthomonas euvesicatoria

Functional characterization of VirB/VirD4 and Icm/Dot type IV secretion systems from the plant-pathogenic bacterium Xanthomonas euvesicatoria

Vibrio parahaemolyticus becomes lethal to post-larvae shrimp via acquiring novel virulence factors

A bacterial binary toxin system that kills both insects and aquatic crustaceans: Photorhabdus insect-related toxins A and B

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