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High Conopeptide Diversity in Conus tribblei Revealed Through Analysis of Venom Duct Transcriptome Using Two High-Throughput Sequencing Platforms

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Abstract

The venom of each species of Conus contains different kinds of pharmacologically active peptides which are mostly unique to that species. Collectively, the ~500–700 species of Conus produce a large number of these peptides, perhaps exceeding 140,000 different types in total. To date, however, only a small fraction of this diversity has been characterized via transcriptome sequencing. In addition, the sampling of this chemical diversity has not been uniform across the different lineages in the genus. In this study, we used high-throughput transcriptome sequencing approach to further investigate the diversity of Conus venom peptides. We chose a species, Conus tribblei, as a representative of a poorly studied clade of Conus. Using the Roche 454 and Illumina platforms, we discovered 136 unique and novel putative conopeptides belonging to 30 known gene superfamilies and 6 new conopeptide groups, the greatest diversity so far observed from a transcriptome. Most of the identified peptides exhibited divergence from the known conopeptides, and some contained cysteine frameworks observed for the first time in cone snails. In addition, several enzymes involved in posttranslational modification of conopeptides and also some proteins involved in efficient delivery of the conopeptides to prey were identified as well. Interestingly, a number of conopeptides highly similar to the conopeptides identified in a phylogenetically distant species, the generalist feeder Conus californicus, were observed. The high diversity of conopeptides and the presence of conopeptides similar to those in C. californicus suggest that C. tribblei may have a broad range of prey preferences.

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Acknowledgments

The specimens used in this study were obtained in conjunction with a collection trip supported in part by ICBG grant 1U01TW008163. The Illumina sequencing performed in Oregon Health and Science University was funded by the Philippine PharmaSeas Drug Discovery Program. Roche 454 sequencing was supported by NIH grant GM48677 (BMO) and performed in Marine Science Institute, University of the Philippines. This study was partially supported by the Office of the Vice President for Academic Affairs, University of the Philippines through Philippine Genome Center. The data analysis was carried out using the High-Performance Computing Facility of the Advanced Science and Technology Institute and the Philippine e-Science Grid, Diliman, Quezon City. We would like to thank Joeriggo Reyes for the help in transcriptome analysis and Alexander Fedosov for the help in phylogenetic analysis. We would like to thank Maren Watkins for reviewing the conopeptide sequences and for her constructive comments.

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Authors and Affiliations

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

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

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

    Gisela P. Concepcion & Arturo O. Lluisma

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

    Baldomero M. Olivera

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  1. Neda Barghi
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  2. Gisela P. Concepcion
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  3. Baldomero M. Olivera
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  4. Arturo O. Lluisma
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Correspondence to Arturo O. Lluisma.

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(DOC 27 kb)

Fig. S 1

The putative conopeptide precursors identified by ConoSorter. The prepeptide cleavage sites are shown in bold and are underlined (DOC 31 kb)

Fig. S 2

The truncated putative conopeptide precursors of (a) A-, (b) G- and (c) O1-superfamilies. The conopeptides identified in C. tribblei are shown in black and the conopeptide nomenclature is as described in "Materials and Methods". The name of each conopeptide is presented as Ctr_#_T/N/TN: Ctr: C. tribblei, #: arbitrary assigned number, T: only present in the ‘Trinity conopeptide dataset’, N: only present in the ‘Newbler conopeptide dataset’, TN: present in both Trinity and Newbler conopeptide datasets. The reference sequences are shown in green and cysteine residues are shown in bold italic red. The names of the reference sequences are derived from the ConoServer database unless noted otherwise. The mature regions are underlined and the signal regions are highlighted (DOC 35 kb)

Fig. S 3

The putative conopeptide precursors of (a) M superfamily, (b) con-ikot-ikot and (c) conkunitzin family. The notes are indicated in Fig. S 2 (DOC 46 kb)

Fig. S 4

The putative conopeptide precursors of (a) conopressin/conophysin and (b) conodipine families. Conopressin domain is underlined in red at position 32–40 and conophysin is underlined in gray. The notes are indicated in Fig. S 2 (DOC 45 kb)

Fig. S 5

The putative conopeptide precursors of (a) N-, (b) K- and (c) S-superfamilies. The notes are indicated in Fig. S 2 (DOC 36 kb)

Fig. S 6

The putative conopeptide precursors of (a) I2-, (b) L-, (c) H-, (d) O1- and (e) O2-superfamilies. The notes are indicated in Fig. S 2 (DOC 50 kb)

Fig. S 7

The putative conopeptide precursors of (a) D-, (b) I1- and (c) I3-superfamilies. The notes are indicated in Fig. S 2 (DOC 34 kb)

Fig. S 8

The putative conopeptide precursors of (a) O3-, (b) J-, (c) Y-, (d) F-, and (e) B2-superfamilies. The notes are indicated in Fig. S 2 (DOC 39 kb)

Fig. S 9

The putative conopeptide precursors of (a) P-, (b) R-, (c) W-, (d) Y2- and (e) B1-superfamilies (conantokin family). The notes are indicated in Fig. S 2 (DOC 41 kb)

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Barghi, N., Concepcion, G.P., Olivera, B.M. et al. High Conopeptide Diversity in Conus tribblei Revealed Through Analysis of Venom Duct Transcriptome Using Two High-Throughput Sequencing Platforms. Mar Biotechnol 17, 81–98 (2015). https://doi.org/10.1007/s10126-014-9595-7

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