Horizontal gene transfer of a bacterial insect toxin gene into the Epichloë fungal symbionts of grasses

AbstractHorizontal gene transfer is a major driving force behind the genomic diversity seen in prokaryotes. Theracprophage inE.coliK12 encodes a putative transcription factor RacR, whose deletion is lethal. We have shown that the essentiality ofracRinE.coliK12 is attributed to its role in transcriptionally repressing a toxin gene calledydaS, which is coded adjacent and divergently toracR.

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Horizontal transfer of microbial toxin genes to gall midge genomes

10.1101/2021.02.03.429655 ◽

2021 ◽

Author(s):

Kirsten I. Verster ◽

Rebecca L. Tarnopol ◽

Saron M. Akalu ◽

Noah K. Whiteman

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Horizontal Transfer ◽

Acyrthosiphon Pisum ◽

Phylogenetic Signal ◽

Eukaryotic Cells ◽

Toxin Gene ◽

Toxin Genes ◽

Nuclear Genomes ◽

Secondary Endosymbiont

AbstractA growing body of evidence points to a role for horizontal gene transfer (HGT) in the evolution of animal novelties. Previously, we discovered the horizontal transfer of the gene encoding the eukaryotic genotoxin cytolethal distending toxin B (CdtB) from the Acyrthosiphon pisum Secondary Endosymbiont (APSE) bacteriophage to drosophilid and aphid genomes. Here, we report that cdtB is also found in the nuclear genome of the gall-forming ‘swede midge’ Contarinia nasturtii (Diptera: Cecidomyiidae). We subsequently searched genome sequences of all available cecidomyiid species for evidence of microbe-to-insect HGT events. We found evidence of pervasive transfer of APSE-like toxin genes to cecidomyiid nuclear genomes. Many of the toxins encoded by these horizontally transferred genes target eukaryotic cells, rather than prokaryotes. In insects, catalytic residues important for toxin function are conserved. Phylogenetic analyses of HGT candidates indicated APSE phages were often not the ancestral donor of the toxin gene to cecidomyiid genomes, suggesting a broader pool of microbial donor lineages. We used a phylogenetic signal statistic to test a transfer-by-proximity hypothesis for HGT, which showed, that prokaryotic-to-insect HGT was more likely to occur between taxa in common environments. Our study highlights the horizontal transfer of genes encoding a new functional class of proteins in insects, toxins that target eukaryotic cells, which is potentially important in mediating interactions with eukaryotic pathogens and parasites.Significance StatementThe diversity of genes encoded by phages infecting bacterial symbionts of eukaryotes represents an enormous, relatively unexplored pool of new eukaryotic genes through horizontal gene transfer (HGT). In this study, we discovered pervasive HGT of toxin genes encoded by Acyrthosiphon pisum secondary endosymbiont (APSE) bacteriophages and other microbes to the nuclear genomes of gall midges (Diptera: Cecidomyiidae). We found five toxin genes were transferred horizontally from phage, bacteria, or fungi into genomes of several cecidomyiid species. These genes were aip56, cdtB, lysozyme, rhs, and sltxB. Most of the toxins encoded by these genes antagonize eukaryotic cells, and we posit that they may play a protective role in the insect immune system.

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A competence-regulated toxin-antitoxin system inHaemophilus influenzae

10.1101/633164 ◽

2019 ◽

Author(s):

Hailey Findlay Black ◽

Scott Mastromatteo ◽

Sunita Sinha ◽

Rachel L. Ehrlich ◽

Corey Nislow ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Haemophilus Influenzae ◽

Gene Pair ◽

Carbon Sources ◽

Toxin Gene ◽

Dna Uptake ◽

Rna Seq ◽

Putative Toxin ◽

Species Deletion

ABSTRACTNatural competence allows bacteria to respond to environmental and nutritional cues by taking up free DNA from their surroundings, thus gaining both nutrients and genetic information. In the Gram-negative bacteriumHaemophilus influenzae, the genes needed for DNA uptake are induced by the CRP andSxytranscription factors in response to lack of preferred carbon sources and nucleotide precursors. Here we show that one of these genes,HI0659, encodes the antitoxin of a competence-regulated toxin-antitoxin operon (‘toxTA’), likely acquired by horizontal gene transfer from aStreptococcusspecies. Deletion of the putative toxin(HI0660)restores uptake to the antitoxin mutant. The fulltoxTAoperon was present in only 17 of the 181 strains we examined; complete deletion was seen in 22 strains and deletions removing parts of the toxin gene in 142 others. In addition to the expected Sxy-and CRP-dependent-competence promoter,HI0659/660transcript analysis using RNA-seq identified an internal antitoxin-repressed promoter whose transcription starts withintoxTand will yield nonfunctional protein. We propose that the most likely effect of unopposed toxin expression is non-specific cleavage of mRNAs and arrest or death of competent cells in the culture. Although the high frequency oftoxTandtoxTAdeletions suggests that this competence-regulated toxin-antitoxin system may be mildly deleterious, it could also facilitate downregulation of protein synthesis and recycling of nucleotides under starvation conditions. Although our analyses were focused on the effects oftoxTA, the RNA-seq dataset will be a useful resource for further investigations into competence regulation.ABBREVIATED SUMMARYThe competence regulon ofHaemophilus influenzaeincludes an unprecedented toxin/antitoxin gene pair. When not opposed by antitoxin, the toxin completely prevents DNA uptake but causes only very minor decreases in cell growth and competence gene expression. The TA gene pair was acquired by horizontal gene transfer, and the toxin gene has undergone repeated deletions in other strains.

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