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Molecular Diversity and Gene Evolution of the Venom Arsenal of Terebridae Predatory Marine Snails.

Gorson J, Ramrattan G, Verdes A, Wright EM, Kantor Y, Rajaram Srinivasan R, Musunuri R, Packer D, Albano G, Qiu WG, Holford M - Genome Biol Evol (2015)

Bottom Line: Phylogenetic methodology was used to identify 14 teretoxin gene superfamilies for the first time, 13 of which are unique to the Terebridae.Additionally, basic local algorithm search tool homology-based searches to venom-related genes and posttranslational modification enzymes identified a convergence of certain venom proteins, such as actinoporin, commonly found in venoms.This research provides novel insights into venom evolution and recruitment in Conoidean predatory marine snails and identifies a plethora of terebrid venom peptides that can be used to investigate fundamental questions pertaining to gene evolution.

View Article: PubMed Central - PubMed

Affiliation: Hunter College and The Graduate Center, City University of New York Invertebrate Zoology, Sackler Institute for Comparative Genomics, American Museum of Natural History, New York.

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Putative teretoxins identified from Tr. anilis and Te. subulata transcriptomes. (A) Circos plot showing the distribution of cysteine frameworks of Tr. anilis and Te. subulata putative teretoxins. The teretoxins identified in Tr. anilis and Te. subulata are not same. Tr. anilis teretoxins are shown in blue and Te. subulata's are shown in red. The diversity of Cys frameworks indicates the two species have different venom arsenals. (B) The Cys frameworks identified among Tr. anilis (red) and Te. subulata (blue) putative teretoxins. Each Cys framework is listed and the number of teretoxins found for each species is identified. Fifty-five Te. subulata and 84 Tr. anilis putative teretoxins were identified in total. Of the 12 Cys frameworks identified, two are novel frameworks found in Tr. anilis venom.
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evv104-F4: Putative teretoxins identified from Tr. anilis and Te. subulata transcriptomes. (A) Circos plot showing the distribution of cysteine frameworks of Tr. anilis and Te. subulata putative teretoxins. The teretoxins identified in Tr. anilis and Te. subulata are not same. Tr. anilis teretoxins are shown in blue and Te. subulata's are shown in red. The diversity of Cys frameworks indicates the two species have different venom arsenals. (B) The Cys frameworks identified among Tr. anilis (red) and Te. subulata (blue) putative teretoxins. Each Cys framework is listed and the number of teretoxins found for each species is identified. Fifty-five Te. subulata and 84 Tr. anilis putative teretoxins were identified in total. Of the 12 Cys frameworks identified, two are novel frameworks found in Tr. anilis venom.

Mentions: BLAST searches of the venom duct transcriptomes against an in-house local database of cono- and teretoxins created using the Conoserver database and teretoxins identified in the Holford lab yielded 84 putative teretoxins for Tr. anilis, and 55 putative teretoxins for Te. subulata (fig. 4). It should be noted that discrepancies in teretoxin diversity between the Tr. anilis and Te. subulata might be due to the different depth of sequencing of both trasncriptomes. The transcripts were analyzed for the presence of canonical peptide features as identified in conotoxins, namely the presence of an N-terminal signal sequence, an intervening propeptide region ending with several basic residues identifying a cleavage site, and a C-terminal Cys-rich mature peptide (Terlau and Olivera 2004). Of the 139 total putative teretoxin transcripts identified, 105 contain the full signal-pro-mature toxin canonical structure, and 34 have signal-mature sequence without a proregion, which also occasionally occurs in cone snails. All 139 putative teretoxins were organized by Cys framework, that is, Cys pattern of the mature peptide, using the same Roman numeral nomenclature applied to conotoxins (Akondi et al. 2014; fig. 4). Teretoxins found in Tr. anilis and Te. subualta displayed a wide array of Cys frameworks (fig. 4B). This result is promising as it suggests that, similar to cone snails, each terebrid species can produce a unique cocktail of peptides in its venom arsenal (Norton and Olivera 2006; Kaas et al. 2010; Dutertre et al. 2012). Among the 84 Tr. anilis putative teretoxins identified, ten Cys frameworks were previously known from conotoxins, but two are novel frameworks of 10 and 12 Cys respectively, Tan_10Cys, with Cys framework C-CC-C-C-C-C-C-C-C, and Tan_12Cys, with Cys framework C-CC-CC-C-C-C-C-C-C-C (fig. 4B). The diversity of Cys frameworks found suggests that teretoxins may have a wide array of pharmacological targets. Additionally, novel frameworks Tan_10Cys and Tan_12Cys suggest these teretoxins are distinct from conotoxins in structure and function.Fig. 4.—


Molecular Diversity and Gene Evolution of the Venom Arsenal of Terebridae Predatory Marine Snails.

Gorson J, Ramrattan G, Verdes A, Wright EM, Kantor Y, Rajaram Srinivasan R, Musunuri R, Packer D, Albano G, Qiu WG, Holford M - Genome Biol Evol (2015)

Putative teretoxins identified from Tr. anilis and Te. subulata transcriptomes. (A) Circos plot showing the distribution of cysteine frameworks of Tr. anilis and Te. subulata putative teretoxins. The teretoxins identified in Tr. anilis and Te. subulata are not same. Tr. anilis teretoxins are shown in blue and Te. subulata's are shown in red. The diversity of Cys frameworks indicates the two species have different venom arsenals. (B) The Cys frameworks identified among Tr. anilis (red) and Te. subulata (blue) putative teretoxins. Each Cys framework is listed and the number of teretoxins found for each species is identified. Fifty-five Te. subulata and 84 Tr. anilis putative teretoxins were identified in total. Of the 12 Cys frameworks identified, two are novel frameworks found in Tr. anilis venom.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4494067&req=5

evv104-F4: Putative teretoxins identified from Tr. anilis and Te. subulata transcriptomes. (A) Circos plot showing the distribution of cysteine frameworks of Tr. anilis and Te. subulata putative teretoxins. The teretoxins identified in Tr. anilis and Te. subulata are not same. Tr. anilis teretoxins are shown in blue and Te. subulata's are shown in red. The diversity of Cys frameworks indicates the two species have different venom arsenals. (B) The Cys frameworks identified among Tr. anilis (red) and Te. subulata (blue) putative teretoxins. Each Cys framework is listed and the number of teretoxins found for each species is identified. Fifty-five Te. subulata and 84 Tr. anilis putative teretoxins were identified in total. Of the 12 Cys frameworks identified, two are novel frameworks found in Tr. anilis venom.
Mentions: BLAST searches of the venom duct transcriptomes against an in-house local database of cono- and teretoxins created using the Conoserver database and teretoxins identified in the Holford lab yielded 84 putative teretoxins for Tr. anilis, and 55 putative teretoxins for Te. subulata (fig. 4). It should be noted that discrepancies in teretoxin diversity between the Tr. anilis and Te. subulata might be due to the different depth of sequencing of both trasncriptomes. The transcripts were analyzed for the presence of canonical peptide features as identified in conotoxins, namely the presence of an N-terminal signal sequence, an intervening propeptide region ending with several basic residues identifying a cleavage site, and a C-terminal Cys-rich mature peptide (Terlau and Olivera 2004). Of the 139 total putative teretoxin transcripts identified, 105 contain the full signal-pro-mature toxin canonical structure, and 34 have signal-mature sequence without a proregion, which also occasionally occurs in cone snails. All 139 putative teretoxins were organized by Cys framework, that is, Cys pattern of the mature peptide, using the same Roman numeral nomenclature applied to conotoxins (Akondi et al. 2014; fig. 4). Teretoxins found in Tr. anilis and Te. subualta displayed a wide array of Cys frameworks (fig. 4B). This result is promising as it suggests that, similar to cone snails, each terebrid species can produce a unique cocktail of peptides in its venom arsenal (Norton and Olivera 2006; Kaas et al. 2010; Dutertre et al. 2012). Among the 84 Tr. anilis putative teretoxins identified, ten Cys frameworks were previously known from conotoxins, but two are novel frameworks of 10 and 12 Cys respectively, Tan_10Cys, with Cys framework C-CC-C-C-C-C-C-C-C, and Tan_12Cys, with Cys framework C-CC-CC-C-C-C-C-C-C-C (fig. 4B). The diversity of Cys frameworks found suggests that teretoxins may have a wide array of pharmacological targets. Additionally, novel frameworks Tan_10Cys and Tan_12Cys suggest these teretoxins are distinct from conotoxins in structure and function.Fig. 4.—

Bottom Line: Phylogenetic methodology was used to identify 14 teretoxin gene superfamilies for the first time, 13 of which are unique to the Terebridae.Additionally, basic local algorithm search tool homology-based searches to venom-related genes and posttranslational modification enzymes identified a convergence of certain venom proteins, such as actinoporin, commonly found in venoms.This research provides novel insights into venom evolution and recruitment in Conoidean predatory marine snails and identifies a plethora of terebrid venom peptides that can be used to investigate fundamental questions pertaining to gene evolution.

View Article: PubMed Central - PubMed

Affiliation: Hunter College and The Graduate Center, City University of New York Invertebrate Zoology, Sackler Institute for Comparative Genomics, American Museum of Natural History, New York.

Show MeSH