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Structural features of conopeptide genes inferred from partial sequences of the Conus tribblei genome

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Abstract

The evolvability of venom components (in particular, the gene-encoded peptide toxins) in venomous species serves as an adaptive strategy allowing them to target new prey types or respond to changes in the prey field. The structure, organization, and expression of the venom peptide genes may provide insights into the molecular mechanisms that drive the evolution of such genes. Conus is a particularly interesting group given the high chemical diversity of their venom peptides, and the rapid evolution of the conopeptide-encoding genes. Conus genomes, however, are large and characterized by a high proportion of repetitive sequences. As a result, the structure and organization of conopeptide genes have remained poorly known. In this study, a survey of the genome of Conus tribblei was undertaken to address this gap. A partial assembly of C. tribblei genome was generated; the assembly, though consisting of a large number of fragments, accounted for 2160.5 Mb of sequence. A large number of repetitive genomic elements consisting of 642.6 Mb of retrotransposable elements, simple repeats, and novel interspersed repeats were observed. We characterized the structural organization and distribution of conotoxin genes in the genome. A significant number of conopeptide genes (estimated to be between 148 and 193) belonging to different superfamilies with complete or nearly complete exon regions were observed, ~60 % of which were expressed. The unexpressed conopeptide genes represent hidden but significant conotoxin diversity. The conotoxin genes also differed in the frequency and length of the introns. The interruption of exons by long introns in the conopeptide genes and the presence of repeats in the introns may indicate the importance of introns in facilitating recombination, evolution and diversification of conotoxins. These findings advance our understanding of the structural framework that promotes the gene-level molecular evolution of venom peptides.

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Acknowledgments

The specimen used in this study was obtained in conjunction with a collection trip supported in part by ICBG Grant #1U01TW008163. The data analysis was carried out using the high performance computing systems at the Philippine Genome Center-Core Facility for Bioinformatics and the High-Performance Computing Facility of the Advanced Science and Technology Institute and the Philippine e-Science Grid, Diliman, Quezon City. We are grateful to the constructive comments of anonymous reviewers.

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Author notes

  1. Neda Barghi

    Present address: Institut für Populationsgenetik, Vetmeduni Vienna, Vienna, Austria

Authors and Affiliations

  1. Marine Science Institute, University of the Philippines-Diliman, 1101, Quezon City, Philippines

    Neda Barghi, Gisela P. Concepcion & Arturo O. Lluisma

  2. Philippine Genome Center, University of the Philippines, 1101, Quezon City, Philippines

    Gisela P. Concepcion & Arturo O. Lluisma

  3. Department of Biology, University of Utah, Salt Lake City, UT, USA

    Baldomero M. Olivera

Authors
  1. Neda Barghi
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  4. Arturo O. Lluisma
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Corresponding author

Correspondence to Arturo O. Lluisma.

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Conflict of interest

Neda Barghi declares that she has no conflict of interest. Gisela P. Concepcion declares that she has no conflict of interest. Baldomero M. Olivera declares that he has no conflict of interest. Arturo O. Lluisma declares that he has no conflict of interest.

Funding

This study was funded by a research grant to AOL from the Emerging Interdisciplinary Research Program of the University of the Philippines System through the Philippine Genome Center.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Communicated by S. Hohmann.

This Whole Genome Shotgun project has been deposited at DDBJ/EMBL/GenBank under the accession LFLW00000000. The version described in this paper is version LFLW01000000.

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Barghi, N., Concepcion, G.P., Olivera, B.M. et al. Structural features of conopeptide genes inferred from partial sequences of the Conus tribblei genome. Mol Genet Genomics 291, 411–422 (2016). https://doi.org/10.1007/s00438-015-1119-2

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