Evolution of an insect immune barrier through horizontal gene transfer mediated by a parasitic wasp

Abstract

Genome sequencing data have recently demonstrated that eukaryote evolution has been remarkably influenced by the acquisition of a large number of genes by horizontal gene transfer (HGT) across different kingdoms. However, in depth-studies on the physiological traits conferred by these accidental DNA acquisitions are largely lacking. Here we elucidate the functional role of Sl gasmin, a gene of a symbiotic virus of a parasitic wasp that has been transferred to an ancestor of the moth species Spodoptera littoralis and domesticated. This gene is highly expressed in circulating immune cells (haemocytes) of larval stages, where its transcription is rapidly boosted by injection of microorganisms into the body cavity. RNAi silencing of Sl gasmin generates a phenotype characterized by a precocious suppression of phagocytic activity by haemocytes, which is rescued when these immune cells are incubated in plasma samples of control larvae, containing high levels of the encoded protein. Proteomic analysis demonstrates that the protein Sl gasmin is released by haemocytes into the haemolymph, where it opsonizes the invading bacteria to promote their phagocytosis, both in vitro and in vivo. Our results show that important physiological traits do not necessarily originate from evolution of pre-existing genes, but can be acquired by HGT events, through unique pathways of symbiotic evolution. These findings indicate that insects can paradoxically acquire selective advantages with the help of their natural enemies.

Venomics of the ectoparasitoid wasp Bracon nigricans

“…Parasitoid and host rearing B. nigricans was reared on larvae of the noctuid moth S. littoralis, which were used as laboratory host, maintained on artificial diet as previously described [120]. Adults of B. nigricans were maintained at 27 ± 1°C, 70 ± 5% RH and 16:8 h (L:D) photoperiod, as previously described [54].…”

Horizontal transfer of microbial toxin genes to gall midge genomes

“…There is growing evidence that horizontal gene transfer (HGT) from microbes to animals has played an important role in animal evolution (Husnik & McCutcheon 2018). Toxin-encoding genes have been horizontally transferred into arthropod genomes and even integrated into their immune systems (Di Lelio et al 2019; Hayes et al 2020; Li et al 2021). However, many of these events involve transfer of genes encoding toxins that target prokaryotes, and few characterized HGTs in animals are of genes encoding toxins that target eukaryotes.…”

“…Our previous knowledge of prokaryote-to-insect HGT events centered on genes involved in conferring new metabolic capabilities, particularly those that allow insects to colonize new plant hosts (Wybouw et al 2016). HGTs of toxin-encoding genes are largely antibacterial in function, when function can be acsertained (Di Lelio et al 2019; Hayes et al 2020; Li et al 2021). The galling midge HGT dataset as a whole highlights that a new functional class of proteins, toxins that antagonize eukaryotic cells, may be common among insects.…”

Are fungi‐derived genomic regions related to antagonism towards fungi in mosses?

“…On the other hand, some other fungi‐derived genes might have been recruited by mosses to regulate or counteract the activities of fungi or other microbes, in addition to their roles in other processes. This second possibility is in line with the role of the HLP gene in plant antimicrobial responses (Piechocki et al ., 2018) and supported by similar cases documented in the literature (Chou et al ., 2015; Di Lelio et al ., 2019). For example, endogenous viral DNAs are known to contribute significantly to the immunity of host animals against viral infection (Aswad & Katzourakis, 2012).…”