Identification and Characterization of EvpQ, a Novel T6SS Effector Encoded on a Mobile Genetic Element in

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2021 Mar 29

PMID 33776977

Citations 6

Authors

Duan You Li

Ying Li Liu

Xiao Jian Liao

Tian Tian He

Shan Shan Sun

Pin Nie

Hai Xia Xie

Affiliations

Soon will be listed here.

Abstract

In this study, a hypothetical protein (ORF02740) secreted by was identified. We renamed the ORF02740 protein as EvpQ, which is encoded by a mobile genetic element (MGE) in genome. The gene is spaced by 513 genes from type VI secretion system (T6SS) gene cluster. Low GC content, three tRNA, and three transposase genes nearby define this MGE that localizes as a genomic island. Sequence analysis reveals that EvpQ shares a conserved domain of C70 family cysteine protease and shares 23.91% identity with T3SS effector AvrRpt2 of phytopathogenic Instead, EvpQ of is proved to be secreted at a T6SS-dependent manner, and it can be translocated into host cells. EvpQ is thereof a novel T6SS effector. Significantly decreased competitive index of Δ strain in blue gourami fish (0.53 ± 0.27 in head kidney and 0.44 ± 0.19 in spleen) indicates that EvpQ contributes to the pathogenesis of . At 8-, 18-, and 24-h post-subculture into DMEM, the transcription of was found to be negatively regulated by Fur and positively regulated by EsrC, and the steady-state protein levels of EvpQ are negatively controlled by RpoS. Our study lays a foundation for further understanding the pathogenic role of T6SS in edwardsiellosis.

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References

Uzzau S, Rubino S, Bossi L . Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci U S A. 2001; 98(26):15264-9. PMC: 65018. DOI: 10.1073/pnas.261348198. View

Mackey D, Belkhadir Y, Alonso J, Ecker J, Dangl J . Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell. 2003; 112(3):379-89. DOI: 10.1016/s0092-8674(03)00040-0. View

Sory M, Cornelis G . Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol. 1994; 14(3):583-94. DOI: 10.1111/j.1365-2958.1994.tb02191.x. View

Mohanty B, Sahoo P . Edwardsiellosis in fish: a brief review. J Biosci. 2008; 32(7):1331-44. DOI: 10.1007/s12038-007-0143-8. View

Escolar L, Perez-Martin J, de Lorenzo V . Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol. 1999; 181(20):6223-9. PMC: 103753. DOI: 10.1128/JB.181.20.6223-6229.1999. View

Abayneh T, Colquhoun D, Sorum H . Edwardsiella piscicida sp. nov., a novel species pathogenic to fish. J Appl Microbiol. 2012; 114(3):644-54. DOI: 10.1111/jam.12080. View

Axtell M, Chisholm S, Dahlbeck D, Staskawicz B . Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol Microbiol. 2003; 49(6):1537-46. DOI: 10.1046/j.1365-2958.2003.03666.x. View

Casper-Lindley C, Dahlbeck D, Clark E, Staskawicz B . Direct biochemical evidence for type III secretion-dependent translocation of the AvrBs2 effector protein into plant cells. Proc Natl Acad Sci U S A. 2002; 99(12):8336-41. PMC: 123068. DOI: 10.1073/pnas.122220299. View

Ma A, McAuley S, Pukatzki S, Mekalanos J . Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe. 2009; 5(3):234-43. PMC: 3142922. DOI: 10.1016/j.chom.2009.02.005. View

10.

Shao S, Lai Q, Liu Q, Wu H, Xiao J, Shao Z . Phylogenomics characterization of a highly virulent Edwardsiella strain ET080813(T) encoding two distinct T3SS and three T6SS gene clusters: Propose a novel species as Edwardsiella anguillarum sp. nov. Syst Appl Microbiol. 2014; 38(1):36-47. DOI: 10.1016/j.syapm.2014.10.008. View

11.

Spano S, Galan J . A Rab32-dependent pathway contributes to Salmonella typhi host restriction. Science. 2012; 338(6109):960-3. PMC: 3693731. DOI: 10.1126/science.1229224. View

12.

Liu L, Nie P, Yu H, Xie H . Regulation of Type III Secretion of Translocon and Effector Proteins by the EsaB/EsaL/EsaM Complex in Edwardsiella tarda. Infect Immun. 2017; 85(9). PMC: 5563572. DOI: 10.1128/IAI.00322-17. View

13.

Coombes B, Lowden M, Bishop J, Wickham M, Brown N, Duong N . SseL is a salmonella-specific translocated effector integrated into the SsrB-controlled salmonella pathogenicity island 2 type III secretion system. Infect Immun. 2006; 75(2):574-80. PMC: 1828504. DOI: 10.1128/IAI.00985-06. View

14.

Dix S, Owen H, Sun R, Ahmad A, Shastri S, Spiewak H . Structural insights into the function of type VI secretion system TssA subunits. Nat Commun. 2018; 9(1):4765. PMC: 6232143. DOI: 10.1038/s41467-018-07247-1. View

15.

Mudgett M, Staskawicz B . Characterization of the Pseudomonas syringae pv. tomato AvrRpt2 protein: demonstration of secretion and processing during bacterial pathogenesis. Mol Microbiol. 1999; 32(5):927-41. DOI: 10.1046/j.1365-2958.1999.01403.x. View

16.

Cui F, Wu S, Sun W, Coaker G, Kunkel B, He P . The Pseudomonas syringae type III effector AvrRpt2 promotes pathogen virulence via stimulating Arabidopsis auxin/indole acetic acid protein turnover. Plant Physiol. 2013; 162(2):1018-29. PMC: 3668037. DOI: 10.1104/pp.113.219659. View

17.

Chakraborty S, Li M, Chatterjee C, Sivaraman J, Leung K, Mok Y . Temperature and Mg2+ sensing by a novel PhoP-PhoQ two-component system for regulation of virulence in Edwardsiella tarda. J Biol Chem. 2010; 285(50):38876-88. PMC: 2998078. DOI: 10.1074/jbc.M110.179150. View

18.

Silverman J, Agnello D, Zheng H, Andrews B, Li M, Catalano C . Haemolysin coregulated protein is an exported receptor and chaperone of type VI secretion substrates. Mol Cell. 2013; 51(5):584-93. PMC: 3844553. DOI: 10.1016/j.molcel.2013.07.025. View

19.

Leung K, Wang Q, Yang Z, Siame B . : A versatile emerging pathogen of fish. Virulence. 2019; 10(1):555-567. PMC: 6592360. DOI: 10.1080/21505594.2019.1621648. View

20.

Wolf K, Mann J . Poikilotherm vertebrate cell lines and viruses: a current listing for fishes. In Vitro. 1980; 16(2):168-79. DOI: 10.1007/BF02831507. View