Hao-Sen Li1, Xue-Fei Tang1, Yu-Hao Huang1, Ze-Yu Xu1, Mei-Lan Chen1,2, Xue-Yong Du1, Bo-Yuan Qiu1, Pei-Tao Chen1, Wei Zhang1, Adam Ślipiński3, Hermes E Escalona3, Robert M Waterhouse4, Andreas Zwick3, Hong Pang5. 1. State Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen University, Guangzhou, 510275, China. 2. School of Environment and Life Science, Nanning Normal University, Nanning, 530001, China. 3. Australian National Insect Collection, CSIRO, GPO Box 1700, Canberra, ACT, 2601, Australia. 4. Department of Ecology and Evolution, University of Lausanne and Swiss Institute of Bioinformatics, 1015, Lausanne, Switzerland. 5. State Key Laboratory of Biocontrol, School of Life Sciences / School of Ecology, Sun Yat-sen University, Guangzhou, 510275, China. lsshpang@mail.sysu.edu.cn.
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.
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 ladybirdcwh 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.
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