Delivery of an Rhs‐family nuclease effector reveals direct penetration of the gram‐positive cell envelope by a type VI secretion system in Acidovorax citrulli
Abstract The type VI secretion system (T6SS) is a double‐tubular nanomachine widely found in gram‐negative bacteria. Its spear‐like Hcp tube is capable of penetrating a neighboring cell for cytosol‐to‐cytosol protein delivery. However, gram‐positive bacteria have been considered impenetrable to such...
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| Format: | Article |
| Language: | English |
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Wiley
2022-03-01
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| Series: | mLife |
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| Online Access: | https://doi.org/10.1002/mlf2.12007 |
| _version_ | 1797857831765934080 |
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| author | Tong‐Tong Pei Yumin Kan Zeng‐Hang Wang Ming‐Xuan Tang Hao Li Shuangquan Yan Yang Cui Hao‐Yu Zheng Han Luo Xiaoye Liang Tao Dong |
| author_facet | Tong‐Tong Pei Yumin Kan Zeng‐Hang Wang Ming‐Xuan Tang Hao Li Shuangquan Yan Yang Cui Hao‐Yu Zheng Han Luo Xiaoye Liang Tao Dong |
| author_sort | Tong‐Tong Pei |
| collection | DOAJ |
| description | Abstract The type VI secretion system (T6SS) is a double‐tubular nanomachine widely found in gram‐negative bacteria. Its spear‐like Hcp tube is capable of penetrating a neighboring cell for cytosol‐to‐cytosol protein delivery. However, gram‐positive bacteria have been considered impenetrable to such T6SS action. Here we report that the T6SS of a plant pathogen, Acidovorax citrulli (AC), could deliver an Rhs‐family nuclease effector RhsB to kill not only gram‐negative but also gram‐positive bacteria. Using bioinformatic, biochemical, and genetic assays, we systematically identified T6SS‐secreted effectors and determined that RhsB is a crucial antibacterial effector. RhsB contains an N‐terminal PAAR domain, a middle Rhs domain, and an unknown C‐terminal domain. RhsB is subject to self‐cleavage at both its N‐ and C‐terminal domains and its secretion requires the upstream‐encoded chaperone EagT2 and VgrG3. The toxic C‐terminus of RhsB exhibits DNase activities and such toxicity is neutralized by either of the two downstream immunity proteins, RimB1 and RimB2. Deletion of rhsB significantly impairs the ability of killing Bacillus subtilis while ectopic expression of immunity proteins RimB1 or RimB2 confers protection. We demonstrate that the AC T6SS not only can effectively outcompete Escherichia coli and B. subtilis in planta but also is highly potent in killing other bacterial and fungal species. Collectively, these findings highlight the greatly expanded capabilities of T6SS in modulating microbiome compositions in complex environments. |
| first_indexed | 2024-04-09T21:03:11Z |
| format | Article |
| id | doaj.art-8a3774533a194d2a84af8298cd1b7724 |
| institution | Directory Open Access Journal |
| issn | 2770-100X |
| language | English |
| last_indexed | 2024-04-09T21:03:11Z |
| publishDate | 2022-03-01 |
| publisher | Wiley |
| record_format | Article |
| series | mLife |
| spelling | doaj.art-8a3774533a194d2a84af8298cd1b77242023-03-29T06:46:59ZengWileymLife2770-100X2022-03-0111667810.1002/mlf2.12007Delivery of an Rhs‐family nuclease effector reveals direct penetration of the gram‐positive cell envelope by a type VI secretion system in Acidovorax citrulliTong‐Tong Pei0Yumin Kan1Zeng‐Hang Wang2Ming‐Xuan Tang3Hao Li4Shuangquan Yan5Yang Cui6Hao‐Yu Zheng7Han Luo8Xiaoye Liang9Tao Dong10State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Developmental Sciences, School of Life Sciences and Biotechnology Shanghai Jiao Tong University Shanghai ChinaAbstract The type VI secretion system (T6SS) is a double‐tubular nanomachine widely found in gram‐negative bacteria. Its spear‐like Hcp tube is capable of penetrating a neighboring cell for cytosol‐to‐cytosol protein delivery. However, gram‐positive bacteria have been considered impenetrable to such T6SS action. Here we report that the T6SS of a plant pathogen, Acidovorax citrulli (AC), could deliver an Rhs‐family nuclease effector RhsB to kill not only gram‐negative but also gram‐positive bacteria. Using bioinformatic, biochemical, and genetic assays, we systematically identified T6SS‐secreted effectors and determined that RhsB is a crucial antibacterial effector. RhsB contains an N‐terminal PAAR domain, a middle Rhs domain, and an unknown C‐terminal domain. RhsB is subject to self‐cleavage at both its N‐ and C‐terminal domains and its secretion requires the upstream‐encoded chaperone EagT2 and VgrG3. The toxic C‐terminus of RhsB exhibits DNase activities and such toxicity is neutralized by either of the two downstream immunity proteins, RimB1 and RimB2. Deletion of rhsB significantly impairs the ability of killing Bacillus subtilis while ectopic expression of immunity proteins RimB1 or RimB2 confers protection. We demonstrate that the AC T6SS not only can effectively outcompete Escherichia coli and B. subtilis in planta but also is highly potent in killing other bacterial and fungal species. Collectively, these findings highlight the greatly expanded capabilities of T6SS in modulating microbiome compositions in complex environments.https://doi.org/10.1002/mlf2.12007cell envelopecell wallinterspecies interactionprotein secretion |
| spellingShingle | Tong‐Tong Pei Yumin Kan Zeng‐Hang Wang Ming‐Xuan Tang Hao Li Shuangquan Yan Yang Cui Hao‐Yu Zheng Han Luo Xiaoye Liang Tao Dong Delivery of an Rhs‐family nuclease effector reveals direct penetration of the gram‐positive cell envelope by a type VI secretion system in Acidovorax citrulli mLife cell envelope cell wall interspecies interaction protein secretion |
| title | Delivery of an Rhs‐family nuclease effector reveals direct penetration of the gram‐positive cell envelope by a type VI secretion system in Acidovorax citrulli |
| title_full | Delivery of an Rhs‐family nuclease effector reveals direct penetration of the gram‐positive cell envelope by a type VI secretion system in Acidovorax citrulli |
| title_fullStr | Delivery of an Rhs‐family nuclease effector reveals direct penetration of the gram‐positive cell envelope by a type VI secretion system in Acidovorax citrulli |
| title_full_unstemmed | Delivery of an Rhs‐family nuclease effector reveals direct penetration of the gram‐positive cell envelope by a type VI secretion system in Acidovorax citrulli |
| title_short | Delivery of an Rhs‐family nuclease effector reveals direct penetration of the gram‐positive cell envelope by a type VI secretion system in Acidovorax citrulli |
| title_sort | delivery of an rhs family nuclease effector reveals direct penetration of the gram positive cell envelope by a type vi secretion system in acidovorax citrulli |
| topic | cell envelope cell wall interspecies interaction protein secretion |
| url | https://doi.org/10.1002/mlf2.12007 |
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