Pathogen-origin horizontally transferred genes contribute to the evolution of Lepidopteran insects

Abstract

BackgroundHorizontal gene transfer (HGT), a source of genetic variation, is generally considered to facilitate hosts' adaptability to environments. However, convincing evidence supporting the significant contribution of the transferred genes to the evolution of metazoan recipients is rare.ResultsIn this study, based on sequence data accumulated to date, we used a unified method consisting of similarity search and phylogenetic analysis to detect horizontally transferred genes (HTGs) between prokaryotes and five insect species including Drosophila melanogaster, Anopheles gambiae, Bombyx mori, Tribolium castaneum and Apis mellifera. Unexpectedly, the candidate HTGs were not detected in D. melanogaster, An. gambiae and T. castaneum, and 79 genes in Ap. mellifera sieved by the same method were considered as contamination based on other information. Consequently, 14 types of 22 HTGs were detected only in the silkworm. Additionally, 13 types of the detected silkworm HTGs share homologous sequences in species of other Lepidopteran superfamilies, suggesting that the majority of these HTGs were derived from ancient transfer events before the radiation of Ditrysia clade. On the basis of phylogenetic topologies and BLAST search results, donor bacteria of these genes were inferred, respectively. At least half of the predicted donor organisms may be entomopathogenic bacteria. The predicted biochemical functions of these genes include four categories: glycosyl hydrolase family, oxidoreductase family, amino acid metabolism, and others.ConclusionsThe products of HTGs detected in this study may take part in comprehensive physiological metabolism. These genes potentially contributed to functional innovation and adaptability of Lepidopteran hosts in their ancient lineages associated with the diversification of angiosperms. Importantly, our results imply that pathogens may be advantageous to the subsistence and prosperity of hosts through effective HGT events at a large evolutionary scale.

Horizontal gene transfer: building the web of life

“…In an analysis of HGT in lepidopteran insects, most of the acquired genes were shown to be distributed in multiple lepidopteran groups and related to nutritional metabolism and detoxification 91 . The production of toxins by plants and the corresponding genes for detoxification in lepidopterans, and other phytophagous arthropods, exemplifies a genetic 'arms race' fuelled by HGT.…”

Characterization of an Ancient Lepidopteran Lateral Gene Transfer

“…We noted that the BLASTP output for the gene also contained a strong hit (E value of 0.0) to a glycosyl hydrolase ( BGIBMGA013995 ) from the genome of B. mori . A previous report has described BGIBMGA013995 as a possible LGT [18]. Reciprocal BLASTP comparisons of all D. plexippus and B. mori proteins revealed that DpGH31 and BGIBMGA013995 (henceforth referred to as BmGH31) are 1∶1 BLAST orthologs.…”

“…In contrast to other studies [18], [23], we decided to use a BLASTN based approach that utilizes the rapid decay of DNA homology to greatly reduces the likelihood of false positives resulting from functionally constrained eukaryotic protein motifs that are shared by bacteria. The single best candidate LGT in the D. plexippus genome based on the BLASTN searches, with a strong BLAST match to the glycosyl hydrolase family 31 (GH31) from Enterococcus faecalis , was on scaffold 15050 located within a predicted gene called DPGLEAN20412 (henceforth referred to as DpGH31).…”

“…Other insect associated bacteria have also been donors in LGT events, with these transfers likely mediated through occupation of the bacteria in the gastrointestinal and reproductive tracts, as well as parasitic and/or intracellular life stages [15]–[17]. Recently, Li et al (2011) [18] carried out a screen of LGTs in several insect species with a bioinformatic pipeline. Somewhat surprisingly, LGTs were only detected in B. mori , with a broad range of donor species encompassing 11 genera.…”

“…A complicating factor in searches for LGTs is that many genomes contain contaminating DNA sequences from bacteria that were associated with the sequenced animal. Highlighting this problem Li et al (2011) [18] identified 77 genes on contaminating bacterial scaffolds that remain part of the Official Gene Set release 2 for Apis mellifera . This latter point illustrates the importance of confirming the localization of the LGT in animal genomes, either by PCR and sequencing over insect bacteria boundaries or by in situ hybridization.…”