Acinetobacter baumannii Kills Fungi via a Type VI DNase Effector
ABSTRACT Many Gram-negative bacteria deploy a type VI secretion system (T6SS) to inject toxins into target cells to promote their survival and replication in complex environments. Here, we report that Acinetobacter baumannii uses its T6SS to kill fungi and that the effector TafE (ACX60_15365) is res...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-02-01
|
| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mbio.03420-22 |
| _version_ | 1811163387465302016 |
|---|---|
| author | Jingjing Luo Xiao Chu Jing Jie Yu Sun Qingtian Guan Dan Li Zhao-Qing Luo Lei Song |
| author_facet | Jingjing Luo Xiao Chu Jing Jie Yu Sun Qingtian Guan Dan Li Zhao-Qing Luo Lei Song |
| author_sort | Jingjing Luo |
| collection | DOAJ |
| description | ABSTRACT Many Gram-negative bacteria deploy a type VI secretion system (T6SS) to inject toxins into target cells to promote their survival and replication in complex environments. Here, we report that Acinetobacter baumannii uses its T6SS to kill fungi and that the effector TafE (ACX60_15365) is responsible for such killing. Although ectopically expressed TafE is toxic to both Escherichia coli and Saccharomyces cerevisiae, deletion of tafE only affects the antifungal activity of A. baumannii. We demonstrate that TafE is a DNase capable of targeting the nuclei of yeast cells and that an Ntox15 domain is essential for its ability to degrade DNA. Furthermore, our findings show that A. baumannii is protected from the toxicity of TafE by elaborating the immunity protein TaeI (ACX60_15360), which antagonizes the activity of the effector by direct binding. The discovery of A. baumannii T6SS effectors capable of killing multiple taxonomically distinct microbes has shed light on a mechanism of the high-level fitness of this pathogen in environments characterized by scarce nutrients and the potential presence of diverse microorganisms. IMPORTANCE Acinetobacter baumannii is an increasing important nosocomial pathogen that is difficult to combat due to its ability to survive in harsh environments and the emergence of isolates that are resistant to multiple antibiotics. A better understanding of the mechanism underlying the toughness of A. baumannii may identify its Achilles’ heel, which will facilitate the development of novel preventive and treatment measures. In this study, our findings show that A. baumannii kills fungi with the DNase effector TafE injected into competitor cells by its type VI secretion system. A. baumannii is protected from the activity of TafE by the immunity protein TaeI, which inactivates the effector by direct binding. Our results suggest that inactivation of its T6SS or effectors may reduce the fitness of A. baumannii and increase the effectiveness of treatment by means such as antibiotics. Furthermore, our finding suggests that targeted degradation of TaeI may be an effective strategy to kill A. baumannii. |
| first_indexed | 2024-04-10T06:44:20Z |
| format | Article |
| id | doaj.art-b58dd343246d489b974d28cc21a6b732 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-04-10T06:44:20Z |
| publishDate | 2023-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-b58dd343246d489b974d28cc21a6b7322023-02-28T14:06:25ZengAmerican Society for MicrobiologymBio2150-75112023-02-0114110.1128/mbio.03420-22Acinetobacter baumannii Kills Fungi via a Type VI DNase EffectorJingjing Luo0Xiao Chu1Jing Jie2Yu Sun3Qingtian Guan4Dan Li5Zhao-Qing Luo6Lei Song7Department of Respiratory Medicine, Center for Infectious Diseases and Pathogen Biology, Key Laboratory of Organ Regeneration and Transplantation of the Ministry of Education, State Key Laboratory for Zoonotic Diseases, The First Hospital of Jilin University, Changchun, ChinaDepartment of Respiratory Medicine, Center for Infectious Diseases and Pathogen Biology, Key Laboratory of Organ Regeneration and Transplantation of the Ministry of Education, State Key Laboratory for Zoonotic Diseases, The First Hospital of Jilin University, Changchun, ChinaDepartment of Respiratory Medicine, Center for Infectious Diseases and Pathogen Biology, Key Laboratory of Organ Regeneration and Transplantation of the Ministry of Education, State Key Laboratory for Zoonotic Diseases, The First Hospital of Jilin University, Changchun, ChinaThe First Hospital of Jilin University, Changchun, ChinaThe First Hospital of Jilin University, Changchun, ChinaDepartment of Respiratory Medicine, Center for Infectious Diseases and Pathogen Biology, Key Laboratory of Organ Regeneration and Transplantation of the Ministry of Education, State Key Laboratory for Zoonotic Diseases, The First Hospital of Jilin University, Changchun, ChinaDepartment of Biological Sciences, Purdue University, West Lafayette, Indiana, USADepartment of Respiratory Medicine, Center for Infectious Diseases and Pathogen Biology, Key Laboratory of Organ Regeneration and Transplantation of the Ministry of Education, State Key Laboratory for Zoonotic Diseases, The First Hospital of Jilin University, Changchun, ChinaABSTRACT Many Gram-negative bacteria deploy a type VI secretion system (T6SS) to inject toxins into target cells to promote their survival and replication in complex environments. Here, we report that Acinetobacter baumannii uses its T6SS to kill fungi and that the effector TafE (ACX60_15365) is responsible for such killing. Although ectopically expressed TafE is toxic to both Escherichia coli and Saccharomyces cerevisiae, deletion of tafE only affects the antifungal activity of A. baumannii. We demonstrate that TafE is a DNase capable of targeting the nuclei of yeast cells and that an Ntox15 domain is essential for its ability to degrade DNA. Furthermore, our findings show that A. baumannii is protected from the toxicity of TafE by elaborating the immunity protein TaeI (ACX60_15360), which antagonizes the activity of the effector by direct binding. The discovery of A. baumannii T6SS effectors capable of killing multiple taxonomically distinct microbes has shed light on a mechanism of the high-level fitness of this pathogen in environments characterized by scarce nutrients and the potential presence of diverse microorganisms. IMPORTANCE Acinetobacter baumannii is an increasing important nosocomial pathogen that is difficult to combat due to its ability to survive in harsh environments and the emergence of isolates that are resistant to multiple antibiotics. A better understanding of the mechanism underlying the toughness of A. baumannii may identify its Achilles’ heel, which will facilitate the development of novel preventive and treatment measures. In this study, our findings show that A. baumannii kills fungi with the DNase effector TafE injected into competitor cells by its type VI secretion system. A. baumannii is protected from the activity of TafE by the immunity protein TaeI, which inactivates the effector by direct binding. Our results suggest that inactivation of its T6SS or effectors may reduce the fitness of A. baumannii and increase the effectiveness of treatment by means such as antibiotics. Furthermore, our finding suggests that targeted degradation of TaeI may be an effective strategy to kill A. baumannii.https://journals.asm.org/doi/10.1128/mbio.03420-22type VI secretion systemanti-fungal effectorinterkingdom competitionpolymicrobial niches |
| spellingShingle | Jingjing Luo Xiao Chu Jing Jie Yu Sun Qingtian Guan Dan Li Zhao-Qing Luo Lei Song Acinetobacter baumannii Kills Fungi via a Type VI DNase Effector mBio type VI secretion system anti-fungal effector interkingdom competition polymicrobial niches |
| title | Acinetobacter baumannii Kills Fungi via a Type VI DNase Effector |
| title_full | Acinetobacter baumannii Kills Fungi via a Type VI DNase Effector |
| title_fullStr | Acinetobacter baumannii Kills Fungi via a Type VI DNase Effector |
| title_full_unstemmed | Acinetobacter baumannii Kills Fungi via a Type VI DNase Effector |
| title_short | Acinetobacter baumannii Kills Fungi via a Type VI DNase Effector |
| title_sort | acinetobacter baumannii kills fungi via a type vi dnase effector |
| topic | type VI secretion system anti-fungal effector interkingdom competition polymicrobial niches |
| url | https://journals.asm.org/doi/10.1128/mbio.03420-22 |
| work_keys_str_mv | AT jingjingluo acinetobacterbaumanniikillsfungiviaatypevidnaseeffector AT xiaochu acinetobacterbaumanniikillsfungiviaatypevidnaseeffector AT jingjie acinetobacterbaumanniikillsfungiviaatypevidnaseeffector AT yusun acinetobacterbaumanniikillsfungiviaatypevidnaseeffector AT qingtianguan acinetobacterbaumanniikillsfungiviaatypevidnaseeffector AT danli acinetobacterbaumanniikillsfungiviaatypevidnaseeffector AT zhaoqingluo acinetobacterbaumanniikillsfungiviaatypevidnaseeffector AT leisong acinetobacterbaumanniikillsfungiviaatypevidnaseeffector |