Tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer

Authors: ZHAO, CHAOYANG - University Of California; LIAO, PING - Chinese Academy Of Agricultural Sciences; MIAO, SHAOMING - Chinese Academy Of Agricultural Sciences; NABITY, PAUL - University Of California; Bansal, Raman; LIU, CHENXI - Chinese Academy Of Agricultural Sciences

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/25/2021
Publication Date: 4/6/2021
Citation: Zhao, C., Liao, P., Miao, S., Nabity, P., Bansal, R., Liu, C. 2021. Tripartite parasitic and symbiotic interactions as a possible mechanism of horizontal gene transfer. Ecology and Evolution. https://doi.org/10.1002/ece3.7550.
DOI: https://doi.org/10.1002/ece3.7550

Interpretive Summary: The brown marmorated stink bug (BMSB) is a major pest of agricultural crops with worldwide distribution. It is a highly polyphagous insect with host range of at least 170 plant species. During feeding, BMSB injects saliva into plants that contain proteins, called effectors. Following their secretion into the plant, salivary effectors are known to suppress plants defenses as well as to perform extra-oral digestion. In this study, we performed sequencing to study expressed genes encoding for the salivary effectors. We identified several candidate genes for metabolism and cellular processes which are potentially involved in host manipulation and diet digestion. Further we identified a group of genes encoding for phospholipase C (PLC) proteins which were more closely related to bacteria rather than to insects. Subsequent analysis confirmed that these PLC genes are indeed part of BMSB genome and are acquired from bacteria through horizontal gene transfer (HGT). Our results suggest that BMSB acquired PLCs from bacteria living in a mutually beneficial relationship with insect-parasitic nematodes, a mechanism previously unknown for HGT events.

Technical Abstract: Herbivory is a highly sophisticated feeding behavior that requires abilities of plant defense suppression, phytochemical detoxification, and plant macromolecule digestion. For plant-sucking insects, salivary glands (SGs) play important roles in herbivory by secreting and injecting proteins into plant tissues to facilitate feeding. Little is known on how insects evolved secretory SG proteins for such specialized functions. Here, we investigated the composition and evolution of secretory SG proteins in the brown marmorated stink bug (Halyomorpha halys) and identified a group of secretory SG phospholipase C (PLC) genes with highest sequence similarity to the bacterial homologs. Further analyses demonstrated that they were most closely related to PLCs of Xenorhabdus, a genus of Gammaproteobacteria living in symbiosis with insect-parasitizing nematodes. These suggested that H. halys might acquire these PLCs from Xenorhabdus through the mechanism of horizontal gene transfer (HGT), likely mediated by a nematode during its parasitizing an insect host. We also showed that the original HGT event was followed by gene duplication and expansion, leading to functional diversification of the bacterial-origin PLC genes in H. halys. Thus, this study suggested that an herbivore might enhance adaptation through gaining genes from an endosymbiont of its parasite in the tripartite parasitic and symbiotic interactions.