Identification of a new effector-immunity pair of Aeromonas hydrophila type VI secretion system

Abstract The type VI secretion system (T6SS) is a multiprotein weapon that kills eukaryotic predators or prokaryotic competitors by delivering toxic effectors. Despite the importance of T6SS in bacterial environmental adaptation, it is still challenging to systematically identify T6SS effectors beca...

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Main Authors: Shuiyan Ma, Yuhao Dong, Nannan Wang, Jin Liu, Chengping Lu, Yongjie Liu
Format: Article
Language:English
Published: BMC 2020-05-01
Series:Veterinary Research
Online Access:http://link.springer.com/article/10.1186/s13567-020-00794-w
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spelling doaj-184c9f695ed048d08e9d10d483b9642f2020-11-25T03:21:55ZengBMCVeterinary Research1297-97162020-05-0151111410.1186/s13567-020-00794-wIdentification of a new effector-immunity pair of Aeromonas hydrophila type VI secretion systemShuiyan Ma0Yuhao Dong1Nannan Wang2Jin Liu3Chengping Lu4Yongjie Liu5Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural UniversityJoint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural UniversityCollege of Animal Science and Technology, Jinling Institute of TechnologyJoint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural UniversityJoint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural UniversityJoint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural UniversityAbstract The type VI secretion system (T6SS) is a multiprotein weapon that kills eukaryotic predators or prokaryotic competitors by delivering toxic effectors. Despite the importance of T6SS in bacterial environmental adaptation, it is still challenging to systematically identify T6SS effectors because of their high diversity and lack of conserved domains. In this report, we discovered a putative effector gene, U876-17730, in the whole genome of Aeromonas hydrophila NJ-35 based on the reported conservative domain DUF4123 (domain of unknown function), with two cognate immunity proteins encoded downstream. Phylogenetic tree analysis of amino acids indicates that AH17730 belongs to the Tle1 (type VI lipase effector) family, and therefore was named Tle1AH. The deletion of tle1 AH resulted in significantly decreased biofilm formation, antibacterial competition ability and virulence in zebrafish (Danio rerio) when compared to the wild-type strain. Only when the two immunity proteins coexist can bacteria protect themselves from the toxicity of Tle1AH. Further study shows that Tle1AH is a kind of phospholipase that possesses a conserved lipase motif, Gly-X-Ser-X-Gly (X is for any amino acid). Tle1AH is secreted by T6SS, and this secretion requires its interaction with an associated VgrG (valine-glycine repeat protein G). In conclusion, we identified a T6SS effector-immunity pair and verified its function, which lays the foundation for future research on the role of T6SS in the pathogenic mechanism of A. hydrophila.http://link.springer.com/article/10.1186/s13567-020-00794-w
collection DOAJ
language English
format Article
sources DOAJ
author Shuiyan Ma
Yuhao Dong
Nannan Wang
Jin Liu
Chengping Lu
Yongjie Liu
spellingShingle Shuiyan Ma
Yuhao Dong
Nannan Wang
Jin Liu
Chengping Lu
Yongjie Liu
Identification of a new effector-immunity pair of Aeromonas hydrophila type VI secretion system
Veterinary Research
author_facet Shuiyan Ma
Yuhao Dong
Nannan Wang
Jin Liu
Chengping Lu
Yongjie Liu
author_sort Shuiyan Ma
title Identification of a new effector-immunity pair of Aeromonas hydrophila type VI secretion system
title_short Identification of a new effector-immunity pair of Aeromonas hydrophila type VI secretion system
title_full Identification of a new effector-immunity pair of Aeromonas hydrophila type VI secretion system
title_fullStr Identification of a new effector-immunity pair of Aeromonas hydrophila type VI secretion system
title_full_unstemmed Identification of a new effector-immunity pair of Aeromonas hydrophila type VI secretion system
title_sort identification of a new effector-immunity pair of aeromonas hydrophila type vi secretion system
publisher BMC
series Veterinary Research
issn 1297-9716
publishDate 2020-05-01
description Abstract The type VI secretion system (T6SS) is a multiprotein weapon that kills eukaryotic predators or prokaryotic competitors by delivering toxic effectors. Despite the importance of T6SS in bacterial environmental adaptation, it is still challenging to systematically identify T6SS effectors because of their high diversity and lack of conserved domains. In this report, we discovered a putative effector gene, U876-17730, in the whole genome of Aeromonas hydrophila NJ-35 based on the reported conservative domain DUF4123 (domain of unknown function), with two cognate immunity proteins encoded downstream. Phylogenetic tree analysis of amino acids indicates that AH17730 belongs to the Tle1 (type VI lipase effector) family, and therefore was named Tle1AH. The deletion of tle1 AH resulted in significantly decreased biofilm formation, antibacterial competition ability and virulence in zebrafish (Danio rerio) when compared to the wild-type strain. Only when the two immunity proteins coexist can bacteria protect themselves from the toxicity of Tle1AH. Further study shows that Tle1AH is a kind of phospholipase that possesses a conserved lipase motif, Gly-X-Ser-X-Gly (X is for any amino acid). Tle1AH is secreted by T6SS, and this secretion requires its interaction with an associated VgrG (valine-glycine repeat protein G). In conclusion, we identified a T6SS effector-immunity pair and verified its function, which lays the foundation for future research on the role of T6SS in the pathogenic mechanism of A. hydrophila.
url http://link.springer.com/article/10.1186/s13567-020-00794-w
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