Horizontally acquired antibacterial genes associated with adaptive radiation of ladybird beetles
Abstract Background Horizontal gene transfer (HGT) has been documented in many herbivorous insects, conferring the ability to digest plant material and promoting their remarkable ecological diversification. Previous reports suggest HGT of antibacterial enzymes may have contributed to the insect immu...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2021-01-01
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| Series: | BMC Biology |
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| Online Access: | https://doi.org/10.1186/s12915-020-00945-7 |
| _version_ | 1818383309300826112 |
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| author | Hao-Sen Li Xue-Fei Tang Yu-Hao Huang Ze-Yu Xu Mei-Lan Chen Xue-Yong Du Bo-Yuan Qiu Pei-Tao Chen Wei Zhang Adam Ślipiński Hermes E. Escalona Robert M. Waterhouse Andreas Zwick Hong Pang |
| author_facet | Hao-Sen Li Xue-Fei Tang Yu-Hao Huang Ze-Yu Xu Mei-Lan Chen Xue-Yong Du Bo-Yuan Qiu Pei-Tao Chen Wei Zhang Adam Ślipiński Hermes E. Escalona Robert M. Waterhouse Andreas Zwick Hong Pang |
| author_sort | Hao-Sen Li |
| collection | DOAJ |
| description | Abstract Background Horizontal gene transfer (HGT) has been documented in many herbivorous insects, conferring the ability to digest plant material and promoting their remarkable ecological diversification. Previous reports suggest HGT of antibacterial enzymes may have contributed to the insect immune response and limit bacterial growth. Carnivorous insects also display many evolutionary successful lineages, but in contrast to the plant feeders, the potential role of HGTs has been less well-studied. Results Using genomic and transcriptomic data from 38 species of ladybird beetles, we identified a set of bacterial cell wall hydrolase (cwh) genes acquired by this group of beetles. Infection with Bacillus subtilis led to upregulated expression of these ladybird cwh genes, and their recombinantly produced proteins limited bacterial proliferation. Moreover, RNAi-mediated cwh knockdown led to downregulation of other antibacterial genes, indicating a role in antibacterial immune defense. cwh genes are rare in eukaryotes, but have been maintained in all tested Coccinellinae species, suggesting that this putative immune-related HGT event played a role in the evolution of this speciose subfamily of predominant predatory ladybirds. Conclusion Our work demonstrates that, in a manner analogous to HGT-facilitated plant feeding, enhanced immunity through HGT might have played a key role in the prey adaptation and niche expansion that promoted the diversification of carnivorous beetle lineages. We believe that this represents the first example of immune-related HGT in carnivorous insects with an association with a subsequent successful species radiation. |
| first_indexed | 2024-12-14T03:04:19Z |
| format | Article |
| id | doaj.art-00c15286271540e88a21b1795816f32d |
| institution | Directory Open Access Journal |
| issn | 1741-7007 |
| language | English |
| last_indexed | 2024-12-14T03:04:19Z |
| publishDate | 2021-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj.art-00c15286271540e88a21b1795816f32d2022-12-21T23:19:26ZengBMCBMC Biology1741-70072021-01-0119111610.1186/s12915-020-00945-7Horizontally acquired antibacterial genes associated with adaptive radiation of ladybird beetlesHao-Sen Li0Xue-Fei Tang1Yu-Hao Huang2Ze-Yu Xu3Mei-Lan Chen4Xue-Yong Du5Bo-Yuan Qiu6Pei-Tao Chen7Wei Zhang8Adam Ślipiński9Hermes E. Escalona10Robert M. Waterhouse11Andreas Zwick12Hong Pang13State Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen UniversityState Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen UniversityState Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen UniversityState Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen UniversityState Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen UniversityState Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen UniversityState Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen UniversityState Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen UniversityState Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen UniversityAustralian National Insect Collection, CSIROAustralian National Insect Collection, CSIRODepartment of Ecology and Evolution, University of Lausanne and Swiss Institute of BioinformaticsAustralian National Insect Collection, CSIROState Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen UniversityAbstract Background Horizontal gene transfer (HGT) has been documented in many herbivorous insects, conferring the ability to digest plant material and promoting their remarkable ecological diversification. Previous reports suggest HGT of antibacterial enzymes may have contributed to the insect immune response and limit bacterial growth. Carnivorous insects also display many evolutionary successful lineages, but in contrast to the plant feeders, the potential role of HGTs has been less well-studied. Results Using genomic and transcriptomic data from 38 species of ladybird beetles, we identified a set of bacterial cell wall hydrolase (cwh) genes acquired by this group of beetles. Infection with Bacillus subtilis led to upregulated expression of these ladybird cwh genes, and their recombinantly produced proteins limited bacterial proliferation. Moreover, RNAi-mediated cwh knockdown led to downregulation of other antibacterial genes, indicating a role in antibacterial immune defense. cwh genes are rare in eukaryotes, but have been maintained in all tested Coccinellinae species, suggesting that this putative immune-related HGT event played a role in the evolution of this speciose subfamily of predominant predatory ladybirds. Conclusion Our work demonstrates that, in a manner analogous to HGT-facilitated plant feeding, enhanced immunity through HGT might have played a key role in the prey adaptation and niche expansion that promoted the diversification of carnivorous beetle lineages. We believe that this represents the first example of immune-related HGT in carnivorous insects with an association with a subsequent successful species radiation.https://doi.org/10.1186/s12915-020-00945-7Horizontal gene transferAntibacterial activityCell wall hydrolaseLadybirds |
| spellingShingle | Hao-Sen Li Xue-Fei Tang Yu-Hao Huang Ze-Yu Xu Mei-Lan Chen Xue-Yong Du Bo-Yuan Qiu Pei-Tao Chen Wei Zhang Adam Ślipiński Hermes E. Escalona Robert M. Waterhouse Andreas Zwick Hong Pang Horizontally acquired antibacterial genes associated with adaptive radiation of ladybird beetles BMC Biology Horizontal gene transfer Antibacterial activity Cell wall hydrolase Ladybirds |
| title | Horizontally acquired antibacterial genes associated with adaptive radiation of ladybird beetles |
| title_full | Horizontally acquired antibacterial genes associated with adaptive radiation of ladybird beetles |
| title_fullStr | Horizontally acquired antibacterial genes associated with adaptive radiation of ladybird beetles |
| title_full_unstemmed | Horizontally acquired antibacterial genes associated with adaptive radiation of ladybird beetles |
| title_short | Horizontally acquired antibacterial genes associated with adaptive radiation of ladybird beetles |
| title_sort | horizontally acquired antibacterial genes associated with adaptive radiation of ladybird beetles |
| topic | Horizontal gene transfer Antibacterial activity Cell wall hydrolase Ladybirds |
| url | https://doi.org/10.1186/s12915-020-00945-7 |
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