Coinfection of Two Rickettsia Species in a Single Tick Species Provides New Insight into Rickettsia-Rickettsia and Rickettsia-Vector Interactions
ABSTRACT Rickettsiae are obligate intracellular bacteria that can cause life-threatening illnesses. There is an ongoing debate as to whether established infections by one Rickettsia species preclude the maintenance of the second species in ticks. Here, we identified two Rickettsia species in inoculu...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2022-10-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02323-22 |
| _version_ | 1811257664282296320 |
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| author | Yu-Sheng Pan Xiao-Ming Cui Li-Feng Du Luo-Yuan Xia Chun-Hong Du Lesley Bell-Sakyi Ming-Zhu Zhang Dai-Yun Zhu Yi Dong Wei Wei Lin Zhao Yi Sun Qing-Yu Lv Run-Ze Ye Zhi-Hai He Qian Wang Liang-Jing Li Ming-Guo Yao Tao Xiong Jia-Fu Jiang Wu-Chun Cao Na Jia |
| author_facet | Yu-Sheng Pan Xiao-Ming Cui Li-Feng Du Luo-Yuan Xia Chun-Hong Du Lesley Bell-Sakyi Ming-Zhu Zhang Dai-Yun Zhu Yi Dong Wei Wei Lin Zhao Yi Sun Qing-Yu Lv Run-Ze Ye Zhi-Hai He Qian Wang Liang-Jing Li Ming-Guo Yao Tao Xiong Jia-Fu Jiang Wu-Chun Cao Na Jia |
| author_sort | Yu-Sheng Pan |
| collection | DOAJ |
| description | ABSTRACT Rickettsiae are obligate intracellular bacteria that can cause life-threatening illnesses. There is an ongoing debate as to whether established infections by one Rickettsia species preclude the maintenance of the second species in ticks. Here, we identified two Rickettsia species in inoculum from Haemaphysalis montgomeryi ticks and subsequently obtained pure isolates of each species by plaque selection. The two isolates were classified as a transitional group and spotted fever group rickettsiae and named Rickettsia hoogstraalii str CS and Rickettsia rhipicephalii str EH, respectively. The coinfection of these two Rickettsia species was detected in 25.6% of individual field-collected H. montgomeryi. In cell culture infection models, R. hoogstraalii str CS overwhelmed R. rhipicephalii str EH with more obvious cytopathic effects, faster plaque formation, and increased cellular growth when cocultured, and R. hoogstraalii str CS seemed to polymerize actin tails differently from R. rhipicephalii str EH in vitro. This work provides a model to investigate the mechanisms of both Rickettsia-Rickettsia and Rickettsia-vector interactions. IMPORTANCE The rickettsiae are a group of obligate intracellular Gram-negative bacteria that include human pathogens causing an array of clinical symptoms and even death. There is an important question in the field, that is whether one infection can block the superinfection of other rickettsiae. This work demonstrated the coinfection of two Rickettsia species in individual ticks and further highlighted that testing the rickettsial competitive exclusion hypothesis will undoubtedly be a promising area as methods for bioengineering and pathogen biocontrol become amenable for rickettsiae. |
| first_indexed | 2024-04-12T18:01:57Z |
| format | Article |
| id | doaj.art-0bc7f2aadea643ff8ab53633988f7676 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-12T18:01:57Z |
| publishDate | 2022-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-0bc7f2aadea643ff8ab53633988f76762022-12-22T03:22:08ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-10-0110510.1128/spectrum.02323-22Coinfection of Two Rickettsia Species in a Single Tick Species Provides New Insight into Rickettsia-Rickettsia and Rickettsia-Vector InteractionsYu-Sheng Pan0Xiao-Ming Cui1Li-Feng Du2Luo-Yuan Xia3Chun-Hong Du4Lesley Bell-Sakyi5Ming-Zhu Zhang6Dai-Yun Zhu7Yi Dong8Wei Wei9Lin Zhao10Yi Sun11Qing-Yu Lv12Run-Ze Ye13Zhi-Hai He14Qian Wang15Liang-Jing Li16Ming-Guo Yao17Tao Xiong18Jia-Fu Jiang19Wu-Chun Cao20Na Jia21State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaYunnan Institute for Endemic Diseases Control and Prevention, Dali, Yunnan, People’s Republic of ChinaDepartment of Infection Biology and Microbiomes, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool, United KingdomState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaYunnan Institute for Endemic Diseases Control and Prevention, Dali, Yunnan, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaInstitute of EcoHealth, School of Public Health, Shandong University, Jinan, Shandong, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaYunnan Institute for Endemic Diseases Control and Prevention, Dali, Yunnan, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaYunnan Institute for Endemic Diseases Control and Prevention, Dali, Yunnan, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing, People’s Republic of ChinaABSTRACT Rickettsiae are obligate intracellular bacteria that can cause life-threatening illnesses. There is an ongoing debate as to whether established infections by one Rickettsia species preclude the maintenance of the second species in ticks. Here, we identified two Rickettsia species in inoculum from Haemaphysalis montgomeryi ticks and subsequently obtained pure isolates of each species by plaque selection. The two isolates were classified as a transitional group and spotted fever group rickettsiae and named Rickettsia hoogstraalii str CS and Rickettsia rhipicephalii str EH, respectively. The coinfection of these two Rickettsia species was detected in 25.6% of individual field-collected H. montgomeryi. In cell culture infection models, R. hoogstraalii str CS overwhelmed R. rhipicephalii str EH with more obvious cytopathic effects, faster plaque formation, and increased cellular growth when cocultured, and R. hoogstraalii str CS seemed to polymerize actin tails differently from R. rhipicephalii str EH in vitro. This work provides a model to investigate the mechanisms of both Rickettsia-Rickettsia and Rickettsia-vector interactions. IMPORTANCE The rickettsiae are a group of obligate intracellular Gram-negative bacteria that include human pathogens causing an array of clinical symptoms and even death. There is an important question in the field, that is whether one infection can block the superinfection of other rickettsiae. This work demonstrated the coinfection of two Rickettsia species in individual ticks and further highlighted that testing the rickettsial competitive exclusion hypothesis will undoubtedly be a promising area as methods for bioengineering and pathogen biocontrol become amenable for rickettsiae.https://journals.asm.org/doi/10.1128/spectrum.02323-22rickettsiaecoinfectionHaemaphysalis montgomeryitickinterferencecompetition |
| spellingShingle | Yu-Sheng Pan Xiao-Ming Cui Li-Feng Du Luo-Yuan Xia Chun-Hong Du Lesley Bell-Sakyi Ming-Zhu Zhang Dai-Yun Zhu Yi Dong Wei Wei Lin Zhao Yi Sun Qing-Yu Lv Run-Ze Ye Zhi-Hai He Qian Wang Liang-Jing Li Ming-Guo Yao Tao Xiong Jia-Fu Jiang Wu-Chun Cao Na Jia Coinfection of Two Rickettsia Species in a Single Tick Species Provides New Insight into Rickettsia-Rickettsia and Rickettsia-Vector Interactions Microbiology Spectrum rickettsiae coinfection Haemaphysalis montgomeryi tick interference competition |
| title | Coinfection of Two Rickettsia Species in a Single Tick Species Provides New Insight into Rickettsia-Rickettsia and Rickettsia-Vector Interactions |
| title_full | Coinfection of Two Rickettsia Species in a Single Tick Species Provides New Insight into Rickettsia-Rickettsia and Rickettsia-Vector Interactions |
| title_fullStr | Coinfection of Two Rickettsia Species in a Single Tick Species Provides New Insight into Rickettsia-Rickettsia and Rickettsia-Vector Interactions |
| title_full_unstemmed | Coinfection of Two Rickettsia Species in a Single Tick Species Provides New Insight into Rickettsia-Rickettsia and Rickettsia-Vector Interactions |
| title_short | Coinfection of Two Rickettsia Species in a Single Tick Species Provides New Insight into Rickettsia-Rickettsia and Rickettsia-Vector Interactions |
| title_sort | coinfection of two rickettsia species in a single tick species provides new insight into rickettsia rickettsia and rickettsia vector interactions |
| topic | rickettsiae coinfection Haemaphysalis montgomeryi tick interference competition |
| url | https://journals.asm.org/doi/10.1128/spectrum.02323-22 |
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