Recent Horizontal Transfer of Mellifera Subfamily Mariner Transposons into Insect Lineages Representing Four Different Orders Shows that Selection Acts Only During Horizontal Transfer

Lampe, David J.; Witherspoon, David J.; Soto-Adames, Felipe N.; Robertson, Hugh M.

doi:10.1093/molbev/msg069

Cited by 96 publications

(82 citation statements)

References 42 publications

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“…We identified clades of related insect species for which this situation may happen, by relying on the common assumption that inherited TEs evolve neutrally and similarly to synonymous sites of protein coding genes (20). This assumption implies that TEs showing higher interspecific homology than the synonymous sites of orthologous genes should share a more recent ancestor than the host species, and hence be the result of HT (16,21).…”

Section: Resultsmentioning

confidence: 99%

Massive horizontal transfer of transposable elements in insects

Peccoud

Loiseau

Cordaux

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

203

236

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Horizontal transfer (HT) of genetic material is central to the architecture and evolution of prokaryote genomes. Within eukaryotes, the majority of HTs reported so far are transfers of transposable elements (TEs). These reports essentially come from studies focusing on specific lineages or types of TEs. Because of the lack of large-scale survey, the amount and impact of HT of TEs (HTT) in eukaryote evolution, as well as the trends and factors shaping these transfers, are poorly known. Here, we report a comprehensive analysis of HTT in 195 insect genomes, representing 123 genera and 13 of the 28 insect orders. We found that these insects were involved in at least 2,248 HTT events that essentially occurred during the last 10 My. We show that DNA transposons transfer horizontally more often than retrotransposons, and unveil phylogenetic relatedness and geographical proximity as major factors facilitating HTT in insects. Even though our study is restricted to a small fraction of insect biodiversity and to a recent evolutionary timeframe, the TEs we found to be horizontally transferred generated up to 24% (2.08% on average) of all nucleotides of insect genomes. Together, our results establish HTT as a major force shaping insect genome evolution.horizontal transfer | transposable elements | insects | genome evolution | biogeography H orizontal transfer (HT) is the transmission of genetic material between organisms through a mechanism other than reproduction. In prokaryotes, HT is pervasive, its mechanisms are well understood, and it is now viewed as one of the main forces shaping genome architecture and evolution (1, 2). In contrast, the study of HT in eukaryotes is less documented, but has been increasingly investigated. The majority of genes horizontally acquired by eukaryotes come from bacteria, but the extent to which these transfers have contributed to eukaryote evolution is still unclear (3, 4). Gene transfers from eukaryote to eukaryote appear to be largely limited to filamentous organisms, such as oomycetes and fungi (5, 6).In animals and plants, very few cases of such horizontal gene transfers (HGTs) have been reported so far (7,8). In fact, most of the genetic material that is horizontally transferred in animals and plants consists of transposable elements (TEs) (9-11), which are pieces of DNA able to move from a chromosomal locus to another (12). The greater ability of TEs to move between organisms certainly relates to their intrinsic ability to transpose within genomes, which genes cannot do. HT of TEs (HTT) may allow these elements to enter naive genomes, which they invade by making copies of themselves, and then escape before they become fully silenced by anti-TE defenses (13). A growing number of studies have identified such HTT (11,[14][15][16]. However, a common drawback of these studies has been the inclusion of a limited set of TEs (11) or organisms (16), which hampers our understanding of the breadth of HTT, its contribution to genome evolution, and of the factors and barriers shaping these transfe...

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Section: Resultsmentioning

confidence: 99%

Massive horizontal transfer of transposable elements in insects

Peccoud

Loiseau

Cordaux

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

203

236

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“…The exchange of genetic material between two eukaryotes is extremely rare, or at least not well documented to date. The best-studied cases include the transfer of mitochondrial DNA from achlorophyllous or epiphytic plants to the mitochondrial genome (mtDNA) of their closely related photosynthetic hosts (21), the exchange of transposons between two animal (22) or two plant (23) species, and the presence of plant genes in plant parasitic nematodes (in addition to the rhizobial genes discussed previously), which are hypothesized to be ''defense'' genes whose products protect the parasite from host detection (20).…”

mentioning

confidence: 99%

Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica

Rumpho

Worful²,

Lee³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

241

169

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The sea slug Elysia chlorotica acquires plastids by ingestion of its algal food source Vaucheria litorea. Organelles are sequestered in the mollusc's digestive epithelium, where they photosynthesize for months in the absence of algal nucleocytoplasm. This is perplexing because plastid metabolism depends on the nuclear genome for >90% of the needed proteins. Two possible explanations for the persistence of photosynthesis in the sea slug are (i) the ability of V. litorea plastids to retain genetic autonomy and/or (ii) more likely, the mollusc provides the essential plastid proteins. Under the latter scenario, genes supporting photosynthesis have been acquired by the animal via horizontal gene transfer and the encoded proteins are retargeted to the plastid. We sequenced the plastid genome and confirmed that it lacks the full complement of genes required for photosynthesis. In support of the second scenario, we demonstrated that a nuclear gene of oxygenic photosynthesis, psbO, is expressed in the sea slug and has integrated into the germline. The source of psbO in the sea slug is V. litorea because this sequence is identical from the predator and prey genomes. Evidence that the transferred gene has integrated into sea slug nuclear DNA comes from the finding of a highly diverged psbO 3 flanking sequence in the algal and mollusc nuclear homologues and gene absence from the mitochondrial genome of E. chlorotica. We demonstrate that foreign organelle retention generates metabolic novelty (''green animals'') and is explained by anastomosis of distinct branches of the tree of life driven by predation and horizontal gene transfer.symbiosis ͉ Vaucheria litorea ͉ evolution ͉ plastid ͉ stramenopile

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“…ancestral sequence was inferred by maximum likelihood and Quantification of relative transpositional activity of copies agreed with that inferred previously when genomic copies of of Famar1: The relative activity of each functional Famar1 this element were isolated (Lampe et al 2003). Clones isolated coding sequence was measured by using a Famar1-specific matfrom the activity screen were examined to determine which ing-out assay, similar to one developed for Himar1 transposase parts overlapped the ancestral coding sequence, and these acids 78-269).…”

mentioning

confidence: 74%

“…In this screen we identified 45 copies of Famar1 that auricularia genomic library (Lampe et al 2003). We reaencoded a functional transposase ‫%4.2ف(‬ of the total soned that some of these copies might encode funccopies examined).…”

Section: A Large Fraction Of the F Auricularia Genome Consists Of Comentioning

confidence: 99%

A Bacterial Genetic Screen Identifies Functional Coding Sequences of the InsectmarinerTransposable ElementFamar1Amplified From the Genome of the Earwig,Forficula auricularia

Barry¹,

Witherspoon²,

Lampe³

2004

Genetics

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Transposons of the mariner family are widespread in animal genomes and have apparently infected them by horizontal transfer. Most species carry only old defective copies of particular mariner transposons that have diverged greatly from their active horizontally transferred ancestor, while a few contain young, very similar, and active copies. We report here the use of a whole-genome screen in bacteria to isolate somewhat diverged Famar1 copies from the European earwig, Forficula auricularia, that encode functional transposases. Functional and nonfunctional coding sequences of Famar1 and nonfunctional copies of Ammar1 from the European honey bee, Apis mellifera, were sequenced to examine their molecular evolution. No selection for sequence conservation was detected in any clade of a tree derived from these sequences, not even on branches leading to functional copies. This agrees with the current model for mariner transposon evolution that expects neutral evolution within particular hosts, with selection for function occurring only upon horizontal transfer to a new host. Our results further suggest that mariners are not finely tuned genetic entities and that a greater amount of sequence diversification than had previously been appreciated can occur in functional copies in a single host lineage. Finally, this method of isolating active copies can be used to isolate other novel active transposons without resorting to reconstruction of ancestral sequences.

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Recent Horizontal Transfer of Mellifera Subfamily Mariner Transposons into Insect Lineages Representing Four Different Orders Shows that Selection Acts Only During Horizontal Transfer

Cited by 96 publications

References 42 publications

Massive horizontal transfer of transposable elements in insects

Massive horizontal transfer of transposable elements in insects

Horizontal gene transfer of the algal nuclear gene psbO to the photosynthetic sea slug Elysia chlorotica

A Bacterial Genetic Screen Identifies Functional Coding Sequences of the InsectmarinerTransposable ElementFamar1Amplified From the Genome of the Earwig,Forficula auricularia

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