Abstract
BackgroundHorizontal 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.ResultsUsing 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.ConclusionOur 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.
Highlights
Horizontal gene transfer (HGT) has been documented in many herbivorous insects, conferring the ability to digest plant material and promoting their remarkable ecological diversification
Ladybird cwh genes encode bacterial cell wall hydrolases We detected a set of cell wall hydrolase genes containing the domain of “Hydrolase_2” (Pfam accession: PF07486) from the high-quality genome of a ladybird species Cryptolaemus montrouzieri (NCBI BioProject: PRJNA626074)
These genes encode bacterial cell wall hydrolases but are not derived from contaminated bacterial DNA. This is evidenced by their locations in the beetle genomes, they are flanked by eukaryotic genes (Additional file 1: Fig. S1). They contain introns (Fig. 1), which are absent from genes in bacteria, they share the same splice sites, and they have Guanine-Cytosine contents (GC%) that are similar to the flanking sequences (Additional file 1: Fig. S2)
Summary
Horizontal gene transfer (HGT) has been documented in many herbivorous insects, conferring the ability to digest plant material and promoting their remarkable ecological diversification. Acquisitions by organisms of genetic material from other species, i.e., horizontal gene transfers (HGTs) or lateral gene transfers, play a key role in the evolution of both prokaryotes (Bacteria and Archaea) and eukaryotes [1, 2]. Prominent examples include HGTs that have contributed to the evolution of herbivory in arthropods and nematodes by facilitating plant cell wall digestion and metabolite assimilation and overcoming plant defenses [12, 13]. Plant cell wall-degrading enzymes acquired from bacteria and fungi have been identified in many insect species [14] and are considered to have been vital to the evolutionary success of beetles [15,16,17,18,19]. Acquisitions not directly linked to plant feeding appear to be rarer and include HGTs that enhance eukaryotic innate immune defenses [22]. Deer ticks have genes encoding prokaryotic type VI secretion amidases that degrade bacterial cell walls [23], peptidoglycandegrading bacterial lysozymes have been detected in insects [24, 25] and nematodes [5], and fruit flies have genes related to phagocytosis of bacteria [5]
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