An overview of irritans-mariner transposons in two Mayetiola species (Diptera: Cecidomyiidae)

Amara, Wiem Ben; Djebbi, Salma; Bouktila, Dhia; Makni, Mohamed; Makni, Hanem; Mezghani-Khémakhem, Maha

doi:10.14411/eje.2017.049

Cited by 5 publications

(6 citation statements)

References 66 publications

(57 reference statements)

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“…While we assumed we would identify several instances of APSE-to-insect HGT, our phylogenetic analyses suggested a more diverse pool of HGT donors in Cecidomyiidae. This is consistent with other HGT events in this group, with possible donors including APSE phages ( Zhao et al 2015 ), fungi ( Cobbs et al 2013 ), bacteria ( Cheng et al 2020 ), and even other cecidomyiid species as possible donors ( Ben Amara et al 2017 ). CdtB and sltxB likely had an APSE or APSE-associated bacterial provenance based on AU tests.…”

Section: Discussionsupporting

confidence: 90%

Horizontal Transfer of Microbial Toxin Genes to Gall Midge Genomes

Verster

Tarnopol

Akalu

et al. 2021

Genome Biology and Evolution

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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.

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Section: Discussionsupporting

confidence: 90%

Horizontal Transfer of Microbial Toxin Genes to Gall Midge Genomes

Verster

Tarnopol

Akalu

et al. 2021

Genome Biology and Evolution

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“…Although two MLE subfamilies were identified in M. destructor by Shukle and Russell (1995), the current study allowed the identification for the first time of MLEs belonging to mauritiana subfamily in M. hordei in which only irritans-like elements were reported (Ben Amara et al, 2017). Most of the Desmar1-like elements identified in M. destructor and M. hordei exhibited intact transposases displaying few mutations suggesting their recent invasions in bursts leading to the spread of several copies.…”

Section: In Vitro Search For Mauritiana-like Elementsmentioning

confidence: 78%

“…Subsequently, a full-length copy of MLE with intact ORF and perfect TIRs belonging to mauritiana subfamily were identified experimentally and named Desmar1 Shukle, 1997, Behura et al, 2010). More recently, irritans MLEs from TIR to TIR were identified in M. destructor and M. hordei using complementary approaches combining in silico analyses and in vitro experiments (Ben Amara et al, 2017). In M. hordei, MLEs of mauritiana elements have not yet been reported.…”

Section: Insights On Mauritiana-like Elements Diversity In Mayetiola Destructor and M Hordei (Diptera: Cecidomyiidae) Introductionmentioning

confidence: 99%

Insights on mauritiana-like elements diversity in Mayetiola destructor and M. hordei (Diptera: Cecidomyiidae)

Amara¹,

Djebbi²,

Lazhar-Ajroud³

et al. 2022

Genome

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Mariner-like elements (MLEs) are class II transposons belonging to the Tc1-mariner family, that have successfully invaded many insect genomes. In the current study, the availability of the Hessian fly Mayetiola destructor genome has enabled us to perform in silico analysis of MLEs using as query the previously described mariner element (Desmar1) belonging to mauritiana subfamily. Eighteen mauritiana-like elements were detected and were clustered into three main groups named Desmar1-like, MauCons1 and MauCons2. Subsequently, in vitro analysis was carried out to investigate mauritiana-like elements in M. destructor as well as in Mayetiola hordei using primers designed from TIRs of the previously identified MLEs. PCR amplifications were successful and a total of 12 and 17 mauritiana-like elements were discovered in M. destructor and M. hordei, respectively. Sequence analyses of mauritiana-like elements obtained in silico and in vitro have showed that MauCons1 and MauCons2 elements share low similarity with Desmar1 ranging from 50% to 55% suggesting different groups under mauritiana subfamily have invaded the genomes of M. destructor and M. hordei. These groups are likely inherited by vertical transmission that subsequently underwent different evolutionary histories. This work describes new mauritiana-like elements in M. destructor that are distinct from the previouslydiscovered Desmar1 and provides the first evidence of MLEs belonging to mauritiana subfamily in M. hordei.

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“…aip56 ). Having several possible donors for HGT is not unexpected in cecidomyiids, since HGT has been reported from APSE phages (Zhao et al 2015), fungi (Cobbs et al 2013), and even other cecidomyiid species (Ben Amara et al 2017). We observed that, in most cases, the phylogenies show that HGT occurred between insects and microbes associated with insects ( Figure 2, Figure S1 ).…”

Section: Main Textmentioning

confidence: 98%

Horizontal transfer of microbial toxin genes to gall midge genomes

Verster

Tarnopol

Akalu

et al. 2021

Preprint

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A 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.

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An overview of irritans-mariner transposons in two Mayetiola species (Diptera: Cecidomyiidae)

Cited by 5 publications

References 66 publications

Horizontal Transfer of Microbial Toxin Genes to Gall Midge Genomes

Horizontal Transfer of Microbial Toxin Genes to Gall Midge Genomes

Insights on mauritiana-like elements diversity in Mayetiola destructor and M. hordei (Diptera: Cecidomyiidae)

Horizontal transfer of microbial toxin genes to gall midge genomes

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