Pick Your Poison: Molecular Evolution of Venom Proteins in Asilidae (Insecta: Diptera)
Abstract
:1. Introduction
2. Results
2.1. Quality, Assembly, and Completeness of Transcriptome
2.2. Site-Specific Signatures of Selection in Asilidae Venom Gene Families
2.3. Gene Family Gain/Loss in Insects
3. Discussion
4. Materials and Methods
4.1. Taxon Sampling
4.2. RNA Isolation, Sequencing, and Processing
4.3. Site-Specific Signatures of Selection in Asilidae Venom Gene Families
4.4. Venom Protein Family Assignment
4.5. Gene Family Loss/Gain
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Inceoglu, B.; Lango, J.; Jing, J.; Chen, L.; Doymaz, F.; Pessah, I.N.; Hammock, B.D. One scorpion, two venoms: Prevenom of Parabuthus transvaalicus acts as an alternative type of venom with distinct mechanism of action. Proc. Natl. Acad. Sci. USA 2003, 100, 922–927. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sollod, B.L.; Wilson, D.; Zhaxybayeva, O.; Gogarten, J.P.; Drinkwater, R.; King, G.F. Were arachnids the first to use combinatorial peptide libraries? Peptides 2005, 26, 131–139. [Google Scholar] [CrossRef] [PubMed]
- Fry, B.G. From genome to “venome”: Molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins. Genome Res. 2005, 15, 403–420. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Olivera, B.M.; Teichert, R.W. Diversity of the neurotoxic Conus peptides: A model for concerted pharmacological discovery. Mol. Interv. 2007, 7, 251–260. [Google Scholar] [CrossRef] [PubMed]
- Kordis, D.; Gubensek, F. Adaptive evolution of animal toxin multigene families. Gene 2000, 261, 43–52. [Google Scholar] [CrossRef]
- Drukewitz, S.H.; Reumont, B.M. von The Significance of Comparative Genomics in Modern Evolutionary Venomics. Front. Ecol. Evol. 2019, 7, 163. [Google Scholar] [CrossRef] [Green Version]
- Fry, B.G.; Roelants, K.; Champagne, D.E.; Scheib, H.; Tyndall, J.D.A.; King, G.F.; Nevalainen, T.J.; Norman, J.A.; Lewis, R.J.; Norton, R.S.; et al. The toxicogenomic multiverse: Convergent recruitment of proteins into animal venoms. Annu. Rev. Genom. Hum. Genet. 2009, 10, 483–511. [Google Scholar] [CrossRef] [Green Version]
- Von Reumont, B.; Campbell, L.; Jenner, R. Quo Vadis Venomics? A Roadmap to Neglected Venomous Invertebrates. Toxins 2014, 6, 3488–3551. [Google Scholar] [CrossRef]
- Wilcox, J. Mydidae. In Manual of Nearctic Diptera; McAlpine, J.F., Peterson, B.V., Shewell, G.E., Teskey, H.J., Vockeroth, J.R., Wood, D.M., Eds.; Monograph No. 27; Research Branch Agriculture Canada: Ottawa, ON, Canada, 1981; Volume 1, pp. 533–540. [Google Scholar]
- Peterson, B.V. Apioceridae. In Manual of Nearctic Diptera; McAlpine, J.F., Peterson, B.V., Shewell, G.E., Teskey, H.J., Vockeroth, J.R., Wood, D.M., Eds.; Monograph No. 27; Research Branch Agriculture Canada: Ottawa, ON, Canada, 1981; Volume 1, pp. 541–548. [Google Scholar]
- Melin, D. Contributions to the knowledge of the biology, metamorphosis and distribution of the Swedish asilids in relation to the whole family of asilids. Zool. Bidr. Fran Upps. 1923, 8, 1–337. [Google Scholar]
- Whitfield, F.G.S. The Relation between the Feeding-habits and the Structure of the Mouth-parts in the Asilidae (Diptera). Proc. Zool. Soc. Lond. 1925, 2, 599–638. [Google Scholar]
- Cholodkovsky, N.A. Pischevaritelny apparat lafrii. Trav. Soc. Nat. St. Petersbourg 1900, 31, 25–27. [Google Scholar]
- Owsley, W.B. The comparative morphology of internal structures of the Asilidae (Diptera). Ann. Entomol. Soc. Am. 1946, 39, 33–68. [Google Scholar] [CrossRef]
- Drukewitz, S.H.; Fuhrmann, N.; Undheim, E.A.B.; Blanke, A.; Giribaldi, J.; Rosanna, M.; Laconde, G.; Dutertre, S.; Reumont, B.M. von A Dipteran’s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae Diptera). Toxins 2018, 10, 29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Le Conte, J.L. On some curious habits of a species of Asilus. Proc. Second Meet. Am. Assoc. Adv. Sci. 1850, 2, 195. [Google Scholar]
- Wallis, J.B. Robber-fly and tiger-beetle. Can. Entomol. 1913, 45, 135. [Google Scholar] [CrossRef]
- Blanton, F.S. Collecting notes on the family Asilidae (Diptera). Bull. Brooklyn Entomol. Soc. 1939, 34, 229–235. [Google Scholar]
- Knowlton, G.F.; Stains, G.S. Robberfly Attacks Grasshoppers. Bull. Brooklyn Entomol. Soc. 1942, 37, 42. [Google Scholar]
- Roberts, R. An observation on Promachus, a large robberfly. J. Kans. Entomol. Soc. 1942, 15, 134–135. [Google Scholar]
- Lehr, P.A. Contribution to the biology and importance of robber flies (Asilidae-Diptera). Tr. Inst. Zool. Akad. Nauk Kaz. Ssr 1958, 8, 173–196. [Google Scholar]
- Walker, A.A.; Dobson, J.; Jin, J.; Robinson, S.D.; Herzig, V.; Vetter, I.; King, G.F.; Fry, B.G. Buzz Kill: Function and Proteomic Composition of Venom from the Giant Assassin Fly Dolopus genitalis (Diptera: Asilidae). Toxins 2018, 10, 456. [Google Scholar] [CrossRef] [Green Version]
- Drukewitz, S.H.; Bokelmann, L.; Undheim, E.A.; von Reumont, B.M. Toxins from scratch? Diverse, multimodal gene origins in the predatory robber fly Dasypogon diadema indicate a dynamic venom evolution in dipteran insects. Gigascience 2019, 8, giz081. [Google Scholar] [CrossRef] [PubMed]
- Kahan, D. The toxic effect of the bite and the proteolytic activity of the saliva and stomach contents of the robber flies (Diptera Asilidae). Isr. J. Zool. 1965, 13, 47–57. [Google Scholar]
- Musso, J.-J. Observations sur le comportement alimentaire, l’anatomie et l’histologie des glandes salivaires de deux asilides mediterraneens. Ann. Soc. Entomol. Fr. 1968, 93, 245–255. [Google Scholar]
- Musso, J.-J. Digestion extra-intestinale chez Stenopogon sabaudus F. Et Machimus pilipes Meig. (Dipt. Asilidae). Bulletin de la Société Zoologique de France 1968, 93, 487–497. [Google Scholar]
- Musso, J.-J. Etude comparative des glandes salivaires de quelques asilides de provence. Ann. Soc. Entomol. Fr. 1969, 5, 975–981. [Google Scholar]
- Musso, J.-J.; Garnier, R.; Legier, F. Comparaison de la toxicite du venin de quelques asilides (Dipt. Brachycera) sur le criquet migrateur. Ann. Soc. Entomol. Fr. 1978, 14, 177–184. [Google Scholar]
- Donadey, C.; Musso, J.-J. Premieres observations ultra-structurales des glandes a venin d’ Asilides (Diptera-Brachycera). C. R. Acad. Sc. Paris 1977, 284, 937–940. [Google Scholar]
- Jin, J.; Agwa, A.J.; Szanto, T.G.; Csóti, A.; Panyi, G.; Schroeder, C.I.; Walker, A.A.; King, G.F. Weaponisation ’on the fly’: Convergent recruitment of knottin and defensin peptide scaffolds into the venom of predatory assassin flies. Insect Biochem. Mol. Biol. 2019, 118, 103310. [Google Scholar] [CrossRef]
- Sunagar, K.; Moran, Y. The Rise and Fall of an Evolutionary Innovation: Contrasting Strategies of Venom Evolution in Ancient and Young Animals. PLoS Genet. 2015, 11, e1005596. [Google Scholar] [CrossRef] [Green Version]
- Wiegmann, B.M.; Trautwein, M.D.; Winkler, I.S.; Barr, N.B.; Kim, J.-W.; Lambkin, C.; Bertone, M.A.; Cassel, B.K.; Bayless, K.M.; Heimberg, A.M.; et al. Episodic radiations in the fly tree of life. Proc. Natl. Acad. Sci. USA 2011, 108, 5690–5695. [Google Scholar] [CrossRef] [Green Version]
- Dikow, R.B.; Frandsen, P.B.; Turcatel, M.; Dikow, T. Genomic and transcriptomic resources for assassin flies including the complete genome sequence of Proctacanthus coquilletti (Insecta: Diptera: Asilidae) and 16 representative transcriptomes. PeerJ 2017, 5, e2951. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hedges, S.B.; Vidal, N. Lizards, snakes, and amphisbaenians (Squamata). In The Timetree of Life; Hedges, S.B., Kumar, S., Eds.; Oxford University Press: Oxford, UK, 2009; pp. 383–389. [Google Scholar]
- Cole, J.T.; Brewer, M.S. FUSTr: A tool to find gene Families under Selection in Transcriptomes. PeerJ 2018, 6, e4234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cole, T.J.; Brewer, M.S. TOXIFY: A deep learning approach to classify animal venom proteins. PeerJ 2019, 7, e7200. [Google Scholar] [CrossRef] [PubMed]
- Dikow, T. Phylogeny of Asilidae inferred from morphological characters of imagines (Insecta: Diptera: Brachycera: Asiloidea). Bull. Am. Mus. Nat. Hist. 2009, 319, 1–175. [Google Scholar] [CrossRef]
- Krueger, F. Trim Galore! A Wrapper Tool around Cutadapt and FastQC to Consistently Apply Quality and Adapter Trimming to FastQ files. Available online: https://www.bioinformatics.babraham.ac.uk/projects/trim_galore/ (accessed on 30 April 2017).
- Grabherr, M.G.; Haas, B.J.; Yassour, M.; Levin, J.Z.; Thompson, D.A.; Amit, I.; Xian, A.; Fan, L.; Raychowdhury, R.; Zeng, Q.; et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 2011, 29, 644–652. [Google Scholar] [CrossRef] [Green Version]
- Simão, F.A.; Waterhouse, R.M.; Ioannidis, P.; Kriventseva, E.V.; Zdobnov, E.M. BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 2015, 31, 3210–3212. [Google Scholar] [CrossRef] [Green Version]
- Haas, B.; Papanicolaou, A. TransDecoder (Find Coding Regions within Transcripts). Github, nd. Available online: https://github.com/TransDecoder/TransDecoder (accessed on 30 April 2017).
- Miele, V.; Penel, S.; Duret, L. Ultra-fast sequence clustering from similarity networks with SiLiX. BMC Bioinform. 2011, 12, 116. [Google Scholar] [CrossRef] [Green Version]
- Armenteros, J.J.A.; Tsirigos, K.D.; Sønderby, C.K.; Petersen, T.N.; Winther, O.; Brunak, S.; von Heijne, G.; Nielsen, H. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat. Biotechnol. 2019, 37, 420–423. [Google Scholar] [CrossRef]
- Emms, D.M.; Kelly, S. STAG: Species Tree Inference from All Genes. BioRxiv 2018, 267914. [Google Scholar] [CrossRef]
- Felsenstein, J. Inferring phylogenies from protein sequences by parsimony distance, and likelihood methods. Methods Enzymol. 1996, 266, 418–427. [Google Scholar]
- Li, Z.; Tiley, G.P.; Galuska, S.R.; Reardon, C.R.; Kidder, T.I.; Rundell, R.J.; Barker, M.S. Multiple large-scale gene and genome duplications during the evolution of hexapods. Proc. Natl. Acad. Sci. USA 2018, 115, 4713–4718. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Taxon | Family | Reads | Transcripts | CDS | BUSCO | SRA |
---|---|---|---|---|---|---|
Apiocera parkeri | Apioceridae | 143,373,948 | 298,313 | 112,400 | 65% | SRX2213179 |
Diogmites neoternatus | Asilidae | 120,499,106 | 43,199 | 18,145 | 80% | SRX2212172 |
Eudioctria media | Asilidae | 133,342,485 | 103,000 | 37,075 | 86% | SRR10386632 |
Eutolmus rufibarbis | Asilidae | 87,187,856 | 56,640 | 15,055 | 94.50% | SRX2501518 |
Laphystia limatula | Asilidae | 60,777,554 | 30,019 | 20,511 | 25% | SRX2213169 |
Machimus arthriticus | Asilidae | 83,421,201 | 69,849 | 16,916 | 90% | SRX2501520 |
Mydas clavatus | Mydidae | 90,390,602 | 54,643 | 26,033 | 63% | SRX2212335 |
Philonicus albiceps | Asilidae | 107,425,636 | 46,977 | 27,750 | 90% | SRX2222448 |
Proctacanthus coquilletti | Asilidae | 21,978,654 | 56,925 | 36,770 | 79% | SRX2213473 |
Scleropogon duncani | Asilidae | 111,276,014 | 50,672 | 25,148 | 69% | SRX2213475 |
Tolmerus atricapillus | Asilidae | 108,444,670 | 43,915 | 23,324 | 90% | SRX2213152 |
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Cohen, C.M.; Cole, T.J.; Brewer, M.S. Pick Your Poison: Molecular Evolution of Venom Proteins in Asilidae (Insecta: Diptera). Toxins 2020, 12, 738. https://doi.org/10.3390/toxins12120738
Cohen CM, Cole TJ, Brewer MS. Pick Your Poison: Molecular Evolution of Venom Proteins in Asilidae (Insecta: Diptera). Toxins. 2020; 12(12):738. https://doi.org/10.3390/toxins12120738
Chicago/Turabian StyleCohen, Chris M., T. Jeffrey Cole, and Michael S. Brewer. 2020. "Pick Your Poison: Molecular Evolution of Venom Proteins in Asilidae (Insecta: Diptera)" Toxins 12, no. 12: 738. https://doi.org/10.3390/toxins12120738
APA StyleCohen, C. M., Cole, T. J., & Brewer, M. S. (2020). Pick Your Poison: Molecular Evolution of Venom Proteins in Asilidae (Insecta: Diptera). Toxins, 12(12), 738. https://doi.org/10.3390/toxins12120738