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

In this study, a hypothetical protein (ORF02740) secreted by Edwardsiella piscicida was identified. We renamed the ORF02740 protein as EvpQ, which is encoded by a mobile genetic element (MGE) in E. piscicida genome. The evpQ gene is spaced by 513 genes from type VI secretion system (T6SS) gene clust...

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Main Authors: Duan You Li, Ying Li Liu, Xiao Jian Liao, Tian Tian He, Shan Shan Sun, Pin Nie, Hai Xia Xie
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.643498/full
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author Duan You Li
Duan You Li
Ying Li Liu
Xiao Jian Liao
Xiao Jian Liao
Tian Tian He
Shan Shan Sun
Shan Shan Sun
Pin Nie
Pin Nie
Pin Nie
Hai Xia Xie
author_facet Duan You Li
Duan You Li
Ying Li Liu
Xiao Jian Liao
Xiao Jian Liao
Tian Tian He
Shan Shan Sun
Shan Shan Sun
Pin Nie
Pin Nie
Pin Nie
Hai Xia Xie
author_sort Duan You Li
collection DOAJ
description In this study, a hypothetical protein (ORF02740) secreted by Edwardsiella piscicida was identified. We renamed the ORF02740 protein as EvpQ, which is encoded by a mobile genetic element (MGE) in E. piscicida genome. The evpQ gene is spaced by 513 genes from type VI secretion system (T6SS) gene cluster. Low GC content, three tRNA, and three transposase genes nearby evpQ define this MGE that evpQ 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 Erwinia amylovora. Instead, EvpQ of E. piscicida 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 ΔevpQ 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 E. piscicida. At 8-, 18-, and 24-h post-subculture into DMEM, the transcription of evpQ 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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spelling doaj.art-785def579c974692827223ff65b786ce2022-12-21T18:27:34ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-03-011210.3389/fmicb.2021.643498643498Identification and Characterization of EvpQ, a Novel T6SS Effector Encoded on a Mobile Genetic Element in Edwardsiella piscicidaDuan You Li0Duan You Li1Ying Li Liu2Xiao Jian Liao3Xiao Jian Liao4Tian Tian He5Shan Shan Sun6Shan Shan Sun7Pin Nie8Pin Nie9Pin Nie10Hai Xia Xie11State Key Laboratory of Freshwater Ecology and Biotechnology, Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaLaboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology, Qingdao, ChinaSchool of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, ChinaState Key Laboratory of Freshwater Ecology and Biotechnology, Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaIn this study, a hypothetical protein (ORF02740) secreted by Edwardsiella piscicida was identified. We renamed the ORF02740 protein as EvpQ, which is encoded by a mobile genetic element (MGE) in E. piscicida genome. The evpQ gene is spaced by 513 genes from type VI secretion system (T6SS) gene cluster. Low GC content, three tRNA, and three transposase genes nearby evpQ define this MGE that evpQ 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 Erwinia amylovora. Instead, EvpQ of E. piscicida 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 ΔevpQ 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 E. piscicida. At 8-, 18-, and 24-h post-subculture into DMEM, the transcription of evpQ 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.https://www.frontiersin.org/articles/10.3389/fmicb.2021.643498/fulltype VI secretion systemeffectorEvpQregulationmobile genetic elementEdwardsiella piscicida
spellingShingle Duan You Li
Duan You Li
Ying Li Liu
Xiao Jian Liao
Xiao Jian Liao
Tian Tian He
Shan Shan Sun
Shan Shan Sun
Pin Nie
Pin Nie
Pin Nie
Hai Xia Xie
Identification and Characterization of EvpQ, a Novel T6SS Effector Encoded on a Mobile Genetic Element in Edwardsiella piscicida
Frontiers in Microbiology
type VI secretion system
effector
EvpQ
regulation
mobile genetic element
Edwardsiella piscicida
title Identification and Characterization of EvpQ, a Novel T6SS Effector Encoded on a Mobile Genetic Element in Edwardsiella piscicida
title_full Identification and Characterization of EvpQ, a Novel T6SS Effector Encoded on a Mobile Genetic Element in Edwardsiella piscicida
title_fullStr Identification and Characterization of EvpQ, a Novel T6SS Effector Encoded on a Mobile Genetic Element in Edwardsiella piscicida
title_full_unstemmed Identification and Characterization of EvpQ, a Novel T6SS Effector Encoded on a Mobile Genetic Element in Edwardsiella piscicida
title_short Identification and Characterization of EvpQ, a Novel T6SS Effector Encoded on a Mobile Genetic Element in Edwardsiella piscicida
title_sort identification and characterization of evpq a novel t6ss effector encoded on a mobile genetic element in edwardsiella piscicida
topic type VI secretion system
effector
EvpQ
regulation
mobile genetic element
Edwardsiella piscicida
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.643498/full
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