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

• Published in: PLoS genetics Vol. 15; no. 3; p. e1007998
• Main Authors: Di Lelio, Ilaria, Illiano, Anna, Astarita, Federica, Gianfranceschi, Luca, Horner, David, Varricchio, Paola, Amoresano, Angela, Pucci, Pietro, Pennacchio, Francesco, Caccia, Silvia
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 05.03.2019; Public Library of Science (PLoS)
• Subjects: Analysis; Bacteria; Biology and Life Sciences; DNA; DNA sequencing; Enzymes; Evolution; Evolutionary biology; Evolutionary genetics; Gene expression; Gene transfer; Genes; Genetic aspects; Genetic engineering; Genetic research; Genetic transformation; Genomes; Genomics; Hemocytes; Hemolymph; Immunotherapy; Insect viruses; Insects; Larvae; Metabolism; Methods; Microorganisms; Natural enemies; Natural history; Nematodes; Observations; Organisms; Phagocytes; Phagocytosis; Phenotypes; Phylogenetics; Physiological aspects; Prokaryotes; Proteins; Proteomics; Research and Analysis Methods; RNA interference; RNA-mediated interference; Transcription; Wasps; Italy
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1007998

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.