Horizontally acquired antibacterial genes associated with adaptive radiation of ladybird beetles.
Antibacterial activity
Cell wall hydrolase
Horizontal gene transfer
Ladybirds
Journal
BMC biology
ISSN: 1741-7007
Titre abrégé: BMC Biol
Pays: England
ID NLM: 101190720
Informations de publication
Date de publication:
14 01 2021
14 01 2021
Historique:
received:
19
10
2020
accepted:
22
12
2020
entrez:
15
1
2021
pubmed:
16
1
2021
medline:
1
10
2021
Statut:
epublish
Résumé
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. 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. 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.
Sections du résumé
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.
Identifiants
pubmed: 33446206
doi: 10.1186/s12915-020-00945-7
pii: 10.1186/s12915-020-00945-7
pmc: PMC7807722
doi:
Substances chimiques
Hydrolases
EC 3.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7Subventions
Organisme : National Natural Science Foundation of China
ID : 31702012
Organisme : National Natural Science Foundation of China
ID : 31970439
Organisme : Science and Technology Planning Project of Guangdong Province, China
ID : 2017B020202006
Organisme : National Key R&D Program of China
ID : 2017YFD0201000
Organisme : Basal Research Fund of Sun Yat-sen University
ID : 18lgpy50
Organisme : Science and Technology Planning Project of Guangzhou, China
ID : 201904020041
Organisme : Open Project of the State Key Laboratory of Biocontrol
ID : 2018-04
Organisme : Swiss National Science Foundation
ID : PP00P3_170664
Pays : Switzerland
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