"A tale of two toxins: the acquisition of defensive toxins by animals through horizontal gene transfer", Noah Whiteman, Professor, Departments of Integrative Biology and Molecular & Cell Biology, University of California-Berkeley
Abstract: Several disease-causing bacteria produce toxins that damage host cells by triggering preprogrammed cell death. Two such bacterial toxins are called cytolethal distending toxin B (CdtB) and apoptosis-inducing protein of 56 kDa (AIP56). We discovered that diverse insect species co-opted the two bacterial genes encoding each cytotoxin through a phenomenon called horizontal gene transfer (HGT). HGT occurs when a gene from one organism becomes inserted into the genome of another and can contribute to phenotypic evolution when it is subsequently vertically inherited. We found that these two bacterial toxin genes were captured by an ancestral Drosophila fruit fly in the ananassae species clade ~21 million years ago and are necessary for their innate immunity against parasitoid wasps. These horizontally transferred gene products now contribute to the fly’s innate immune system. To recapitulate the horizontal transfer of this toxin cassette from prokaryotes to insects, we used genome editing to insert the genes into the genome of Drosophila melanogaster, which does not natively encode these toxins. The UAS-Gal4 cell and tissue-specific expression system was then used to determine under what conditions a novel and potentially auto-toxic set of germline encoded proteins could lead to de novo wasp protection or host death (or both). Our study demonstrates how animal toxins can be co-opted by animals through HGT and almost instantaneously contribute to the evolution of novelty, similar to the ways in which prokaryotes gain novel phenotypes through the exchange toxin cargo and antibiotic resistance genes. For more information see our recent paper (https://www.pnas.org/doi/10.1073/pnas.2218334120) and a commentary on it (https://www.pnas.org/doi/10.1073/pnas.2304493120). Remarkably, the closest relatives of the HGT-derived genes in the ananassae species clade of flies are homologs encoded by temperate phages or prophages that infect endosymbiotic bacteria of aphids and other sap-feeding insects, which in turn provide robust protection from their own specialist parasitoid wasps (see this paper by Kerry Oliver, Patrick Degnan, Molly Hunter and Nancy Moran: https://www.science.org/doi/abs/10.1126/science.1174463). It therefore appears that the HGT event obviated an ancient, tripartite mutualism involving a phage, a bacterium, and an insect host.
Source: BRS series