Horizontally transferred genes in the ctenophore  Mnemiopsis leidyi

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Abstract

Horizontal gene transfer (HGT) has had major impacts on the biology of a wide range of organisms from antibiotic resistance in bacteria to adaptations to herbivory in arthropods. A growing body of literature shows that HGT between non-animals and animals is more commonplace than previously thought. In this study, we present a thorough investigation of HGT in the ctenophore Mnemiopsis leidyi. We applied tests of phylogenetic incongruence to identify nine genes that were likely transferred horizontally early in ctenophore evolution from bacteria and non-metazoan eukaryotes. All but one of these HGTs (an uncharacterized protein) are homologous to characterized enzymes, supporting previous observations that genes encoding enzymes are more likely to be retained after HGT events. We found that the majority of these nine horizontally transferred genes were expressed during development, suggesting that they are active and play a role in the biology of M. leidyi. This is the first report of HGT in ctenophores, and contributes to an ever-growing literature on the prevalence of genetic information flowing between non-animals and animals.

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Most cited references 67

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Horizontal gene transfer in eukaryotic evolution.

Patrick Keeling, Jeffrey Palmer (2008)

Horizontal gene transfer (HGT; also known as lateral gene transfer) has had an important role in eukaryotic genome evolution, but its importance is often overshadowed by the greater prevalence and our more advanced understanding of gene transfer in prokaryotes. Recurrent endosymbioses and the generally poor sampling of most nuclear genes from diverse lineages have also complicated the search for transferred genes. Nevertheless, the number of well-supported cases of transfer from both prokaryotes and eukaryotes, many with significant functional implications, is now expanding rapidly. Major recent trends include the important role of HGT in adaptation to certain specialized niches and the highly variable impact of HGT in different lineages.

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Phylogenetic classification and the universal tree.

W. Doolittle (1999)

From comparative analyses of the nucleotide sequences of genes encoding ribosomal RNAs and several proteins, molecular phylogeneticists have constructed a "universal tree of life," taking it as the basis for a "natural" hierarchical classification of all living things. Although confidence in some of the tree's early branches has recently been shaken, new approaches could still resolve many methodological uncertainties. More challenging is evidence that most archaeal and bacterial genomes (and the inferred ancestral eukaryotic nuclear genome) contain genes from multiple sources. If "chimerism" or "lateral gene transfer" cannot be dismissed as trivial in extent or limited to special categories of genes, then no hierarchical universal classification can be taken as natural. Molecular phylogeneticists will have failed to find the "true tree," not because their methods are inadequate or because they have chosen the wrong genes, but because the history of life cannot properly be represented as a tree. However, taxonomies based on molecular sequences will remain indispensable, and understanding of the evolutionary process will ultimately be enriched, not impoverished.

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The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution.

Joseph Ryan, Kevin C.H. Pang, Christine Schnitzler … (2013)

An understanding of ctenophore biology is critical for reconstructing events that occurred early in animal evolution. Toward this goal, we have sequenced, assembled, and annotated the genome of the ctenophore Mnemiopsis leidyi. Our phylogenomic analyses of both amino acid positions and gene content suggest that ctenophores rather than sponges are the sister lineage to all other animals. Mnemiopsis lacks many of the genes found in bilaterian mesodermal cell types, suggesting that these cell types evolved independently. The set of neural genes in Mnemiopsis is similar to that of sponges, indicating that sponges may have lost a nervous system. These results present a newly supported view of early animal evolution that accounts for major losses and/or gains of sophisticated cell types, including nerve and muscle cells.

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Author and article information

Contributors

Joseph F. Ryan

Journal

Journal ID (nlm-ta): PeerJ

Journal ID (iso-abbrev): PeerJ

Journal ID (pmc): PeerJ

Journal ID (publisher-id): PeerJ

Title: PeerJ

Publisher: PeerJ Inc. (San Francisco, USA )

ISSN (Electronic): 2167-8359

Publication date (Electronic): 15 June 2018

Publication date Collection: 2018

Volume: 6

Electronic Location Identifier: e5067

Affiliations

[1 ]Whitney Laboratory for Marine Bioscience , St. Augustine, FL, USA

[2 ]Department of Biology, University of Florida , Gainesville, FL, USA

Article

Publisher ID: 5067

DOI: 10.7717/peerj.5067

PMC ID: 6005172

PubMed ID: 29922518

SO-VID: aec6362e-9bcc-46a3-af2f-b05fedb7db75

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

History

Date received : 14 December 2017

Date accepted : 4 June 2018

Funding

Funded by: University of Florida DSP Research Strategic Initiatives and the Office of the Provost

Funded by: National Science Foundation

Award ID: 1542597

Funded by: McKnight Doctoral Fellowship Program

This work was supported by startup funds to Joseph F. Ryan from the University of Florida DSP Research Strategic Initiatives and the Office of the Provost. This material is based upon work supported by the National Science Foundation under Grant No. (1542597). Alexandra M. Hernandez received support from the McKnight Doctoral Fellowship Program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.