Horizontal Transfer of Microbial Toxin Genes to Gall Midge Genomes.

Kirsten I Verster,Rebecca L Tarnopol,Saron M Akalu,Noah K Whiteman,Laura Katz

doi:10.1093/gbe/evab202

Kirsten I Verster, Rebecca L Tarnopol + Show 3 more

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https://doi.org/10.1093/gbe/evab202

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Abstract

A growing body of evidence has underscored the role of horizontal gene transfer (HGT) in animal evolution. Previously, we discovered the horizontal transfer of the gene encoding the eukaryotic genotoxin cytolethal distending toxin B (cdtB) from the pea aphid Acyrthosiphon pisum secondary endosymbiont (APSE) phages to drosophilid and aphid nuclear genomes. Here, we report cdtB in the nuclear genome of the gall-forming “swede midge” Contarinia nasturtii (Diptera: Cecidomyiidae) via HGT. We searched all available gall midge genome sequences for evidence of APSE-to-insect HGT events and found five toxin genes (aip56, cdtB, lysozyme, rhs, and sltxB) transferred horizontally to cecidomyiid nuclear genomes. Surprisingly, phylogenetic analyses of HGT candidates indicated APSE phages were often not the ancestral donor lineage of the toxin gene to cecidomyiids. We used a phylogenetic signal statistic to test a transfer-by-proximity hypothesis for animal HGT, which suggested that microbe-to-insect HGT was more likely between taxa that share environments than those from different environments. Many of the toxins we found in midge genomes target eukaryotic cells, and catalytic residues important for toxin function are conserved in insect copies. This class of horizontally transferred, eukaryotic cell-targeting genes is potentially important in insect adaptation.

Highlights

There is growing evidence that horizontal gene transfer (HGT) has played an important role in animal evolution (Boto 2014; Husnik and McCutcheon 2018)
We previously discovered HGT of a eukaryote-targeting toxin gene, cytolethal distending toxin B, into the nuclear genomes of four insect lineages within two orders, Diptera and Hemiptera (Verster et al 2019). cdtB is widespread among Proteobacteria and Actinobacteria and encodes a DNAse I-type nuclease that causes cell cycle arrest and apoptosis in eukaryotic cells (Jinadasa et al 2011; Verster et al 2019)
We found evidence of HGT of genes encoding microbial toxins into the nuclear genomes of several gall midge species

Summary

Introduction

There is growing evidence that horizontal gene transfer (HGT) has played an important role in animal evolution (Boto 2014; Husnik and McCutcheon 2018). Some horizontally transferred genes (HTGs) have been co-opted as effectors of the insect immune system. An HTG from a symbiotic virus of a parasitoid wasp, Sl gasmin, plays a central role in mediating phagocytosis in hemocytes of the moth Spodoptera littoralis (Di Lelio et al 2019).

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