Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses

The wandering spider, Phoneutria depilata, is one of Colombia’s most active nocturnal arthropod predators of vertebrates and invertebrates. Its venom has been a relevant subject of study in the last two decades. However, the scarcity of transcriptomic data for the species limits our knowledge of the...

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Autores:
Diego Sierra Ramírez
Juan F. Alzate
Yuri Simone
Arie van der Meijden
Giovany Guevara
Lida Marcela Franco Pérez
César González-Gómez
Carlos F. Prada Quiroga
Tipo de recurso:
Article of investigation
Fecha de publicación:
2023
Institución:
Universidad de Ibagué
Repositorio:
Repositorio Universidad de Ibagué
Idioma:
eng
OAI Identifier:
oai:repositorio.unibague.edu.co:20.500.12313/5627
Acceso en línea:
https://doi.org/10.3390/ toxins15070429
https://hdl.handle.net/20.500.12313/5627
https://www.mdpi.com/2072-6651/15/7/429
Palabra clave:
Secuenciación de próxima generación
Araña
Transcriptómica
Venenosa
Glándula venenosa
Next-generation sequencing
Spider
Transcriptomics
Venomics
Venom gland
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openAccess
License
© 2023 by the authors.
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network_name_str Repositorio Universidad de Ibagué
repository_id_str
dc.title.eng.fl_str_mv Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses
title Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses
spellingShingle Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses
Secuenciación de próxima generación
Araña
Transcriptómica
Venenosa
Glándula venenosa
Next-generation sequencing
Spider
Transcriptomics
Venomics
Venom gland
title_short Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses
title_full Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses
title_fullStr Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses
title_full_unstemmed Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses
title_sort Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses
dc.creator.fl_str_mv Diego Sierra Ramírez
Juan F. Alzate
Yuri Simone
Arie van der Meijden
Giovany Guevara
Lida Marcela Franco Pérez
César González-Gómez
Carlos F. Prada Quiroga
dc.contributor.author.none.fl_str_mv Diego Sierra Ramírez
Juan F. Alzate
Yuri Simone
Arie van der Meijden
Giovany Guevara
Lida Marcela Franco Pérez
César González-Gómez
Carlos F. Prada Quiroga
dc.subject.armarc.none.fl_str_mv Secuenciación de próxima generación
Araña
Transcriptómica
Venenosa
Glándula venenosa
topic Secuenciación de próxima generación
Araña
Transcriptómica
Venenosa
Glándula venenosa
Next-generation sequencing
Spider
Transcriptomics
Venomics
Venom gland
dc.subject.proposal.eng.fl_str_mv Next-generation sequencing
Spider
Transcriptomics
Venomics
Venom gland
description The wandering spider, Phoneutria depilata, is one of Colombia’s most active nocturnal arthropod predators of vertebrates and invertebrates. Its venom has been a relevant subject of study in the last two decades. However, the scarcity of transcriptomic data for the species limits our knowledge of the distinct components present in its venom for linking the mainly neurotoxic effects of the spider venom to a particular molecular target. The transcriptome of the P. depilata venom gland was analyzed to understand the effect of different diets or sex and the impact of these variables on the composition of the venom. We sequenced venom glands obtained from ten males and ten females from three diet treatments: (i) invertebrate: Tenebrio molitor, (ii) vertebrate: Hemidactylus frenatus, and (iii) mixed (T. molitor + H. frenatus). Of 17,354 assembled transcripts from all samples, 65 transcripts relating to venom production differed between males and females. Among them, 36 were classified as neurotoxins, 14 as serine endopeptidases, 11 as other proteins related to venom production, three as metalloprotease toxins, and one as a venom potentiator. There were no differences in transcripts across the analyzed diets, but when considering the effect of diets on differences between the sexes, 59 transcripts were differentially expressed. Our findings provide essential information on toxins differentially expressed that can be related to sex and the plasticity of the diet of P. depilata and thus can be used as a reference for venomics of other wandering spider species.
publishDate 2023
dc.date.issued.none.fl_str_mv 2023-06-30
dc.date.accessioned.none.fl_str_mv 2025-09-02T22:59:05Z
dc.date.available.none.fl_str_mv 2025-09-02T22:59:05Z
dc.type.none.fl_str_mv Artículo de revista
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dc.type.content.none.fl_str_mv Text
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dc.identifier.citation.none.fl_str_mv Ramírez, D.S.; Alzate, J.F.; Simone, Y.; van der Meijden, A.; Guevara, G.; Franco Pérez, L.M.; González-Gómez, J.C.; Prada Quiroga, C.F. Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses. Toxins 2023, 15. https://doi.org/10.3390/ toxins15070429
dc.identifier.doi.none.fl_str_mv https://doi.org/10.3390/ toxins15070429
dc.identifier.issn.none.fl_str_mv 20726651
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12313/5627
dc.identifier.url.none.fl_str_mv https://www.mdpi.com/2072-6651/15/7/429
identifier_str_mv Ramírez, D.S.; Alzate, J.F.; Simone, Y.; van der Meijden, A.; Guevara, G.; Franco Pérez, L.M.; González-Gómez, J.C.; Prada Quiroga, C.F. Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses. Toxins 2023, 15. https://doi.org/10.3390/ toxins15070429
20726651
url https://doi.org/10.3390/ toxins15070429
https://hdl.handle.net/20.500.12313/5627
https://www.mdpi.com/2072-6651/15/7/429
dc.language.iso.none.fl_str_mv eng
language eng
dc.relation.citationissue.none.fl_str_mv 7
dc.relation.citationstartpage.none.fl_str_mv 429
dc.relation.citationvolume.none.fl_str_mv 15
dc.relation.ispartofjournal.none.fl_str_mv Toxins
dc.relation.references.none.fl_str_mv Arbuckle, K. Special Issue: Evolutionary Ecology of Venom. Toxins 2021, 13, 310
Fry, B.G.; Roelants, K.; Champagne, D.E.; Scheib, H.; Tyndall, J.D.; 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.
Wong, E.S.; Belov, K. Venom evolution through gene duplications. Gene 2012, 496, 1–7.
Casewell, N.R.; Wüster, W.; Vonk, F.J.; Harrison, R.A.; Fry, B.G. Complex cocktails: The evolutionary novelty of venoms. Trends Ecol. Evol. 2013, 28, 219–229.
Niermann, C.N.; Tate, T.G.; Suto, A.L.; Barajas, R.; White, H.A.; Guswiler, O.D.; Secor, S.M.; Rowe, A.H.; Rowe, M.P. Defensive Venoms: Is Pain Sufficient for Predator Deterrence? Toxins 2020, 12, 260
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.
Zancolli, G.; Reijnders, M.; Waterhouse, R.M.; Robinson-Rechavi, M. Convergent evolution of venom gland transcriptomes across Metazoa. Proc. Natl. Acad. Sci. USA 2022, 119, e2111392119.
Catalog, W.S. World Spider Catalog, Version 23.5; Natural History Museum Bern: Bern, Switzerland, 2022
Lüddecke, T.; Herzig, V.; von Reumont, B.M.; Vilcinskas, A. The biology and evolution of spider venoms. Biol. Rev. Camb. Philos. Soc. 2022, 97, 163–178.
Betz, L.; Tscharntke, T. Enhancing spider families and spider webs in Indian rice fields for conservation biological control, considering local and landscape management. J. Insect Conserv. 2017, 21, 495–508.
Michalko, R.; Pekár, S.; Entling, M.H. An updated perspective on spiders as generalist predators in biological control. Oecologia 2019, 189, 21–36.
Minh, B.Q.; Schmidt, H.A.; Chernomor, O.; Schrempf, D.; Woodhams, M.D.; von Haeseler, A.; Lanfear, R. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Mol. Biol. Evol. 2020, 37, 1530–1534.
Pekár, S.; Toft, S. Trophic specialisation in a predatory group: The case of prey-specialised spiders (Araneae). Biol. Rev. Camb. Philos. Soc. 2015, 90, 744–761.
Nyffeler, M.; Gibbons, J.W. Spiders (Arachnida: Araneae) feeding on snakes (Reptilia: Squamata). J. Arachnol. 2021, 49, 1–27.
Nyffeler, M.; Gibbons, J.W. Spiders feeding on vertebrates is more common and widespread than previously thought, geographically and taxonomically. J. Arachnol. 2022, 50, 121–134.
Nyffeler, M.; Olson, E.J.; Symondson, W.O. Plant-eating by spiders. J. Arachnol. 2016, 44, 15–27
Valdez, J.W. Arthropods as vertebrate predators: A review of global patterns. Glob. Ecol. Biogeogr. 2020, 29, 1691–1703.
Cooper, A.M.; Nelsen, D.R.; Hayes, W.K.J.E.V.A.T.T. The strategic use of venom by spiders. In Evolution of Venomous Animals and Their Toxins; Springer: Dordrecht, The Netherlands, 2015; pp. 1–18.
Pineda, S.S.; Chin, Y.K.; Undheim, E.A.B.; Senff, S.; Mobli, M.; Dauly, C.; Escoubas, P.; Nicholson, G.M.; Kaas, Q.; Guo, S.; et al. Structural venomics reveals evolution of a complex venom by duplication and diversification of an ancient peptide-encoding gene. Proc. Natl. Acad. Sci. USA 2020, 117, 11399–11408.
Davies, E.L.; Arbuckle, K. Coevolution of Snake Venom Toxic Activities and Diet: Evidence that Ecological Generalism Favours Toxicological Diversity. Toxins 2019, 11, 711.
Lyons, K.; Dugon, M.M.; Healy, K. Diet Breadth Mediates the Prey Specificity of Venom Potency in Snakes. Toxins 2020, 12, 74.
Saez, N.J.; Herzig, V. Versatile spider venom peptides and their medical and agricultural applications. Toxicon Off. J. Int. Soc. Toxinology 2019, 158, 109–126.
Wu, T.; Wang, M.; Wu, W.; Luo, Q.; Jiang, L.; Tao, H.; Deng, M. Spider venom peptides as potential drug candidates due to their anticancer and antinociceptive activities. J. Venom. Anim. Toxins Incl. Trop. Dis. 2019, 25, e146318.
King, G.F.; Gentz, M.C.; Escoubas, P.; Nicholson, G.M. A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon Off. J. Int. Soc. Toxinology 2008, 52, 264–276.
De Roodt, A.R.; Lanari, L.C.; Laskowicz, R.D.; Costa de Oliveira, V.; Irazu, L.E.; González, A.; Giambelluca, L.; Nicolai, N.; Barragán, J.H.; Ramallo, L.; et al. Toxicity of the venom of Latrodectus (Araneae: Theridiidae) spiders from different regions of Argentina and neutralization by therapeutic antivenoms. Toxicon Off. J. Int. Soc. Toxinology 2017, 130, 63–72.
Zobel-Thropp, P.A.; Bodner, M.R.; Binford, G.J. Comparative analyses of venoms from American and African Sicarius spiders that differ in sphingomyelinase D activity. Toxicon Off. J. Int. Soc. Toxinology 2010, 55, 1274–1282.
Duran, L.H.; Rymer, T.L.; Wilson, D.T. Variation in venom composition in the Australian funnel-web spiders Hadronyche valida. Toxicon X 2020, 8, 100063.
Gonçalves de Andrade, R.M.; De Oliveira, K.C.; Giusti, A.L.; Dias da Silva, W.; Tambourgi, D.V. Ontogenetic development of Loxosceles intermedia spider venom. Toxicon Off. J. Int. Soc. Toxinology 1999, 37, 627–632.
Herzig, V.; Ward, R.J.; Dos Santos, W.F. Ontogenetic changes in Phoneutria nigriventer (Araneae, Ctenidae) spider venom. Toxicon Off. J. Int. Soc. Toxinology 2004, 44, 635–640.
Santana, R.C.; Perez, D.; Dobson, J.; Panagides, N.; Raven, R.J.; Nouwens, A.; Jones, A.; King, G.F.; Fry, B.G. Venom Profiling of a Population of the Theraphosid Spider Phlogius crassipes Reveals Continuous Ontogenetic Changes from Juveniles through Adulthood. Toxins 2017, 9, 116.
Binford, G.J. An analysis of geographic and intersexual chemical variation in venoms of the spider Tegenaria agrestis (Agelenidae). Toxicon Off. J. Int. Soc. Toxinology 2001, 39, 955–968.
Binford, G.J.; Gillespie, R.G.; Maddison, W.P. Sexual dimorphism in venom chemistry in Tetragnatha spiders is not easily explained by adult niche differences. Toxicon Off. J. Int. Soc. Toxinology 2016, 114, 45–52.
Herzig, V.; John Ward, R.; Ferreira dos Santos, W. Intersexual variations in the venom of the Brazilian ‘armed’ spider Phoneutria nigriventer (Keyserling, 1891). Toxicon Off. J. Int. Soc. Toxinology 2002, 40, 1399–1406
Michálek, O.; Kuhn-Nentwig, L.; Pekár, S. High Specific Efficiency of Venom of Two Prey-Specialized Spiders. Toxins 2019, 11, 687.
Pekár, S.; Toft, S.; Hrusková, M.; Mayntz, D. Dietary and prey-capture adaptations by which Zodarion germanicum, an ant-eating spider (Araneae: Zodariidae), specialises on the Formicinae. Die Nat. 2008, 95, 233–239.
Garb, J.E.; Hayashi, C.Y. Molecular evolution of α-latrotoxin, the exceptionally potent vertebrate neurotoxin in black widow spider venom. Mol. Biol. Evol. 2013, 30, 999–1014.
Thill, V.L.; Moniz, H.A.; Teglas, M.B.; Wasley, M.J.; Feldman, C.R. Preying dangerously: Black widow spider venom resistance in sympatric lizards. R. Soc. Open Sci. 2022, 9, 221012.
Pekár, S.; Michalko, R.; Korenko, S.; Sedo, O.; Líznarová, E.; Sentenská, L.; Zdráhal, Z. Phenotypic integration in a series of trophic traits: Tracing the evolution of myrmecophagy in spiders (Araneae). Zoology 2013, 116, 27–35.
Hazzi, N.A.; Hormiga, G. Morphological and molecular evidence support the taxonomic separation of the medically important Neotropical spiders Phoneutria depilata (Strand, 1909) and P. boliviensis (F.O. Pickard-Cambridge, 1897) (Araneae, Ctenidae). ZooKeys 2021, 1022, 13–50.
Lucas, S.M.; Meier, J. Biology and distribution of spiders of medical importance. In Handbook of: Clinical Toxicology of Animal Venoms and Poisons; CRC Press: Boca Raton, FL, USA, 2017; pp. 239–258.
Hazzi, N.A. Natural history of Phoneutria boliviensis (Araneae: Ctenidae): Habitats, reproductive behavior, postembryonic development and prey-wrapping. J. Arachnol. 2014, 42, 303–310.
Martins, R.; Bertani, R. The non-Amazonian species of the Brazilian wandering spiders of the genus Phoneutria Perty, 1833 (Araneae: Ctenidae), with the description of a new species. J. Zootaxa 2007, 1526, 1–36.
Valenzuela-Rojas, J.C.; González-Gómez, J.C.; van der Meijden, A.; Cortés, J.N.; Guevara, G.; Franco, L.M.; Pekár, S.; García, L.F. Prey and Venom Efficacy of Male and Female Wandering Spider, Phoneutria boliviensis (Araneae: Ctenidae). Toxins 2019, 11, 622.
Sierra Ramírez, D.; Guevara, G.; Franco Pérez, L.M.; van der Meijden, A.; González-Gómez, J.C.; Carlos Valenzuela-Rojas, J.; Prada Quiroga, C.F. Deciphering the diet of a wandering spider (Phoneutria boliviensis; Araneae: Ctenidae) by DNA metabarcoding of gut contents. Ecol. Evol. 2021, 11, 5950–5965.
Hu, Z.; Chen, B.; Xiao, Z.; Zhou, X.; Liu, Z. Transcriptomic Analysis of the Spider Venom Gland Reveals Venom Diversity and Species Consanguinity. Toxins 2019, 11, 68.
Paiva, A.L.B.; Mudadu, M.A.; Pereira, E.H.T.; Marri, C.A.; Guerra-Duarte, C.; Diniz, M.R.V. Transcriptome analysis of the spider Phoneutria pertyi venom glands reveals novel venom components for the genus Phoneutria. Toxicon Off. J. Int. Soc. Toxinology 2019, 163, 59–69.
Vásquez-Escobar, J.; Romero-Gutiérrez, T.; Morales, J.A.; Clement, H.C.; Corzo, G.A.; Benjumea, D.M.; Corrales-García, L.L. Transcriptomic Analysis of the Venom Gland and Enzymatic Characterization of the Venom of Phoneutria depilata (Ctenidae) from Colombia. Toxins 2022, 14, 295.
Gangur, A.N.; Smout, M.; Liddell, M.J.; Seymour, J.E.; Wilson, D.; Northfield, T.D. Changes in predator exposure, but not in diet, induce phenotypic plasticity in scorpion venom. Proc. Biol. Sci. 2017, 284, 20171364.
Pucca, M.B.; Amorim, F.G.; Cerni, F.A.; Bordon Kde, C.; Cardoso, I.A.; Anjolette, F.A.; Arantes, E.C. Influence of post-starvation extraction time and prey-specific diet in Tityus serrulatus scorpion venom composition and hyaluronidase activity. Toxicon Off. J. Int. Soc. Toxinology 2014, 90, 326–336.
McElroy, T.; McReynolds, C.N.; Gulledge, A.; Knight, K.R.; Smith, W.E.; Albrecht, E.A. Differential toxicity and venom gland gene expression in Centruroides vittatus. PLoS ONE 2017, 12, e0184695.
Herzig, V.; Hodgson, W.C. Intersexual variations in the pharmacological properties of Coremiocnemis tropix (Araneae, Theraphosidae) spider venom. Toxicon Off. J. Int. Soc. Toxinology 2009, 53, 196–205.
Wilder, S.M.; Simpson, S.J.J.F.W. A vertebrate, the fence skink, is a common but relatively low-quality prey for an invertebrate predator, the redback spider. Food Webs 2022, 32, e00236.
Cordeiro Mdo, N.; de Figueiredo, S.G.; Valentim Ado, C.; Diniz, C.R.; von Eickstedt, V.R.; Gilroy, J.; Richardson, M. Purification and amino acid sequences of six Tx3 type neurotoxins from the venom of the Brazilian ‘armed’ spider Phoneutria nigriventer (Keys). Toxicon Off. J. Int. Soc. Toxinology 1993, 31, 35–42.
Diniz, M.R.V.; Paiva, A.L.B.; Guerra-Duarte, C.; Nishiyama, M.Y., Jr.; Mudadu, M.A.; Oliveira, U.; Borges, M.H.; Yates, J.R.; Junqueira-de-Azevedo, I.L. An overview of Phoneutria nigriventer spider venom using combined transcriptomic and proteomic approaches. PLoS ONE 2018, 13, e0200628.
Nunes, K.P.; Costa-Gonçalves, A.; Lanza, L.F.; Cortes, S.F.; Cordeiro, M.N.; Richardson, M.; Pimenta, A.M.; Webb, R.C.; Leite, R.; De Lima, M.E. Tx2-6 toxin of the Phoneutria nigriventer spider potentiates rat erectile function. Toxicon Off. J. Int. Soc. Toxinology 2008, 51, 1197–1206.
De Figueiredo, S.G.; de Lima, M.E.; Nascimento Cordeiro, M.; Diniz, C.R.; Patten, D.; Halliwell, R.F.; Gilroy, J.; Richardson, M. Purification and amino acid sequence of a highly insecticidal toxin from the venom of the brazilian spider Phoneutria nigriventer which inhibits NMDA-evoked currents in rat hippocampal neurones. Toxicon Off. J. Int. Soc. Toxinology 2001, 39, 309–317.
Haas, B.J.; Papanicolaou, A.; Yassour, M.; Grabherr, M.; Blood, P.D.; Bowden, J.; Couger, M.B.; Eccles, D.; Li, B.; Lieber, M.; et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 2013, 8, 1494–1512.
Huson, D.H.; Auch, A.F.; Qi, J.; Schuster, S.C. MEGAN analysis of metagenomic data. Genome Res. 2007, 17, 377–386.
Winter, D.J. rentrez: An R package for the NCBI eUtils API. R J. 2017, 9, 520–526.
Anders, S.; Pyl, P.T.; Huber, W. HTSeq—A Python framework to work with high-throughput sequencing data. Bioinformatics 2015, 31, 166–169.
Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550.
Boutet, E.; Lieberherr, D.; Tognolli, M.; Schneider, M.; Bairoch, A. UniProtKB/Swiss-Prot. Methods Mol. Biol. 2007, 406, 89–112.
Karuppasamy, M.P.; Venkateswaran, S.; Subbiah, P. PDB-2-PBv3.0: An updated protein block database. J. Bioinform. Comput. Biol. 2020, 18, 2050009.
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spelling Diego Sierra Ramíreza73ac47e-9280-498c-8ac9-51f82dc8f80e-1Juan F. Alzate87de0c0b-68bd-4b50-b74a-25c7313923e5-1Yuri Simonea69333cb-4506-45d5-8f8b-03b1334b5709-1Arie van der Meijden8e247b50-39a0-41aa-b70b-99e23e5def2c-1Giovany Guevarae278b7fa-3503-404e-bf78-509fa7ccf17a-1Lida Marcela Franco Pérez7516f4ef-c655-4d3f-856d-9ff5b621872d-1César González-Gómez14bab6ca-03c9-4ed7-9c20-e2948ae73457-1Carlos F. Prada Quirogaf4641463-10eb-4f4e-b600-e62ca5c49a8c-12025-09-02T22:59:05Z2025-09-02T22:59:05Z2023-06-30The wandering spider, Phoneutria depilata, is one of Colombia’s most active nocturnal arthropod predators of vertebrates and invertebrates. Its venom has been a relevant subject of study in the last two decades. However, the scarcity of transcriptomic data for the species limits our knowledge of the distinct components present in its venom for linking the mainly neurotoxic effects of the spider venom to a particular molecular target. The transcriptome of the P. depilata venom gland was analyzed to understand the effect of different diets or sex and the impact of these variables on the composition of the venom. We sequenced venom glands obtained from ten males and ten females from three diet treatments: (i) invertebrate: Tenebrio molitor, (ii) vertebrate: Hemidactylus frenatus, and (iii) mixed (T. molitor + H. frenatus). Of 17,354 assembled transcripts from all samples, 65 transcripts relating to venom production differed between males and females. Among them, 36 were classified as neurotoxins, 14 as serine endopeptidases, 11 as other proteins related to venom production, three as metalloprotease toxins, and one as a venom potentiator. There were no differences in transcripts across the analyzed diets, but when considering the effect of diets on differences between the sexes, 59 transcripts were differentially expressed. Our findings provide essential information on toxins differentially expressed that can be related to sex and the plasticity of the diet of P. depilata and thus can be used as a reference for venomics of other wandering spider species.application/pdfRamírez, D.S.; Alzate, J.F.; Simone, Y.; van der Meijden, A.; Guevara, G.; Franco Pérez, L.M.; González-Gómez, J.C.; Prada Quiroga, C.F. Intersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome Analyses. Toxins 2023, 15. https://doi.org/10.3390/ toxins15070429https://doi.org/10.3390/ toxins1507042920726651https://hdl.handle.net/20.500.12313/5627https://www.mdpi.com/2072-6651/15/7/429engMultidisciplinary Digital Publishing Institute (MDPI)Suiza742915ToxinsArbuckle, K. Special Issue: Evolutionary Ecology of Venom. Toxins 2021, 13, 310Fry, B.G.; Roelants, K.; Champagne, D.E.; Scheib, H.; Tyndall, J.D.; 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.Wong, E.S.; Belov, K. Venom evolution through gene duplications. Gene 2012, 496, 1–7.Casewell, N.R.; Wüster, W.; Vonk, F.J.; Harrison, R.A.; Fry, B.G. Complex cocktails: The evolutionary novelty of venoms. Trends Ecol. Evol. 2013, 28, 219–229.Niermann, C.N.; Tate, T.G.; Suto, A.L.; Barajas, R.; White, H.A.; Guswiler, O.D.; Secor, S.M.; Rowe, A.H.; Rowe, M.P. Defensive Venoms: Is Pain Sufficient for Predator Deterrence? Toxins 2020, 12, 260Sunagar, 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.Zancolli, G.; Reijnders, M.; Waterhouse, R.M.; Robinson-Rechavi, M. Convergent evolution of venom gland transcriptomes across Metazoa. Proc. Natl. Acad. Sci. USA 2022, 119, e2111392119.Catalog, W.S. World Spider Catalog, Version 23.5; Natural History Museum Bern: Bern, Switzerland, 2022Lüddecke, T.; Herzig, V.; von Reumont, B.M.; Vilcinskas, A. The biology and evolution of spider venoms. Biol. Rev. Camb. Philos. Soc. 2022, 97, 163–178.Betz, L.; Tscharntke, T. Enhancing spider families and spider webs in Indian rice fields for conservation biological control, considering local and landscape management. J. Insect Conserv. 2017, 21, 495–508.Michalko, R.; Pekár, S.; Entling, M.H. An updated perspective on spiders as generalist predators in biological control. Oecologia 2019, 189, 21–36.Minh, B.Q.; Schmidt, H.A.; Chernomor, O.; Schrempf, D.; Woodhams, M.D.; von Haeseler, A.; Lanfear, R. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Mol. Biol. Evol. 2020, 37, 1530–1534.Pekár, S.; Toft, S. Trophic specialisation in a predatory group: The case of prey-specialised spiders (Araneae). Biol. Rev. Camb. Philos. Soc. 2015, 90, 744–761.Nyffeler, M.; Gibbons, J.W. Spiders (Arachnida: Araneae) feeding on snakes (Reptilia: Squamata). J. Arachnol. 2021, 49, 1–27.Nyffeler, M.; Gibbons, J.W. Spiders feeding on vertebrates is more common and widespread than previously thought, geographically and taxonomically. J. Arachnol. 2022, 50, 121–134.Nyffeler, M.; Olson, E.J.; Symondson, W.O. Plant-eating by spiders. J. Arachnol. 2016, 44, 15–27Valdez, J.W. Arthropods as vertebrate predators: A review of global patterns. Glob. Ecol. Biogeogr. 2020, 29, 1691–1703.Cooper, A.M.; Nelsen, D.R.; Hayes, W.K.J.E.V.A.T.T. The strategic use of venom by spiders. In Evolution of Venomous Animals and Their Toxins; Springer: Dordrecht, The Netherlands, 2015; pp. 1–18.Pineda, S.S.; Chin, Y.K.; Undheim, E.A.B.; Senff, S.; Mobli, M.; Dauly, C.; Escoubas, P.; Nicholson, G.M.; Kaas, Q.; Guo, S.; et al. Structural venomics reveals evolution of a complex venom by duplication and diversification of an ancient peptide-encoding gene. Proc. Natl. Acad. Sci. USA 2020, 117, 11399–11408.Davies, E.L.; Arbuckle, K. Coevolution of Snake Venom Toxic Activities and Diet: Evidence that Ecological Generalism Favours Toxicological Diversity. Toxins 2019, 11, 711.Lyons, K.; Dugon, M.M.; Healy, K. Diet Breadth Mediates the Prey Specificity of Venom Potency in Snakes. Toxins 2020, 12, 74.Saez, N.J.; Herzig, V. Versatile spider venom peptides and their medical and agricultural applications. Toxicon Off. J. Int. Soc. Toxinology 2019, 158, 109–126.Wu, T.; Wang, M.; Wu, W.; Luo, Q.; Jiang, L.; Tao, H.; Deng, M. Spider venom peptides as potential drug candidates due to their anticancer and antinociceptive activities. J. Venom. Anim. Toxins Incl. Trop. Dis. 2019, 25, e146318.King, G.F.; Gentz, M.C.; Escoubas, P.; Nicholson, G.M. A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon Off. J. Int. Soc. Toxinology 2008, 52, 264–276.De Roodt, A.R.; Lanari, L.C.; Laskowicz, R.D.; Costa de Oliveira, V.; Irazu, L.E.; González, A.; Giambelluca, L.; Nicolai, N.; Barragán, J.H.; Ramallo, L.; et al. Toxicity of the venom of Latrodectus (Araneae: Theridiidae) spiders from different regions of Argentina and neutralization by therapeutic antivenoms. Toxicon Off. J. Int. Soc. Toxinology 2017, 130, 63–72.Zobel-Thropp, P.A.; Bodner, M.R.; Binford, G.J. Comparative analyses of venoms from American and African Sicarius spiders that differ in sphingomyelinase D activity. Toxicon Off. J. Int. Soc. Toxinology 2010, 55, 1274–1282.Duran, L.H.; Rymer, T.L.; Wilson, D.T. Variation in venom composition in the Australian funnel-web spiders Hadronyche valida. Toxicon X 2020, 8, 100063.Gonçalves de Andrade, R.M.; De Oliveira, K.C.; Giusti, A.L.; Dias da Silva, W.; Tambourgi, D.V. Ontogenetic development of Loxosceles intermedia spider venom. Toxicon Off. J. Int. Soc. Toxinology 1999, 37, 627–632.Herzig, V.; Ward, R.J.; Dos Santos, W.F. Ontogenetic changes in Phoneutria nigriventer (Araneae, Ctenidae) spider venom. Toxicon Off. J. Int. Soc. Toxinology 2004, 44, 635–640.Santana, R.C.; Perez, D.; Dobson, J.; Panagides, N.; Raven, R.J.; Nouwens, A.; Jones, A.; King, G.F.; Fry, B.G. Venom Profiling of a Population of the Theraphosid Spider Phlogius crassipes Reveals Continuous Ontogenetic Changes from Juveniles through Adulthood. Toxins 2017, 9, 116.Binford, G.J. An analysis of geographic and intersexual chemical variation in venoms of the spider Tegenaria agrestis (Agelenidae). Toxicon Off. J. Int. Soc. Toxinology 2001, 39, 955–968.Binford, G.J.; Gillespie, R.G.; Maddison, W.P. Sexual dimorphism in venom chemistry in Tetragnatha spiders is not easily explained by adult niche differences. Toxicon Off. J. Int. Soc. Toxinology 2016, 114, 45–52.Herzig, V.; John Ward, R.; Ferreira dos Santos, W. Intersexual variations in the venom of the Brazilian ‘armed’ spider Phoneutria nigriventer (Keyserling, 1891). Toxicon Off. J. Int. Soc. Toxinology 2002, 40, 1399–1406Michálek, O.; Kuhn-Nentwig, L.; Pekár, S. High Specific Efficiency of Venom of Two Prey-Specialized Spiders. Toxins 2019, 11, 687.Pekár, S.; Toft, S.; Hrusková, M.; Mayntz, D. Dietary and prey-capture adaptations by which Zodarion germanicum, an ant-eating spider (Araneae: Zodariidae), specialises on the Formicinae. Die Nat. 2008, 95, 233–239.Garb, J.E.; Hayashi, C.Y. Molecular evolution of α-latrotoxin, the exceptionally potent vertebrate neurotoxin in black widow spider venom. Mol. Biol. Evol. 2013, 30, 999–1014.Thill, V.L.; Moniz, H.A.; Teglas, M.B.; Wasley, M.J.; Feldman, C.R. Preying dangerously: Black widow spider venom resistance in sympatric lizards. R. Soc. Open Sci. 2022, 9, 221012.Pekár, S.; Michalko, R.; Korenko, S.; Sedo, O.; Líznarová, E.; Sentenská, L.; Zdráhal, Z. Phenotypic integration in a series of trophic traits: Tracing the evolution of myrmecophagy in spiders (Araneae). Zoology 2013, 116, 27–35.Hazzi, N.A.; Hormiga, G. Morphological and molecular evidence support the taxonomic separation of the medically important Neotropical spiders Phoneutria depilata (Strand, 1909) and P. boliviensis (F.O. Pickard-Cambridge, 1897) (Araneae, Ctenidae). ZooKeys 2021, 1022, 13–50.Lucas, S.M.; Meier, J. Biology and distribution of spiders of medical importance. In Handbook of: Clinical Toxicology of Animal Venoms and Poisons; CRC Press: Boca Raton, FL, USA, 2017; pp. 239–258.Hazzi, N.A. Natural history of Phoneutria boliviensis (Araneae: Ctenidae): Habitats, reproductive behavior, postembryonic development and prey-wrapping. J. Arachnol. 2014, 42, 303–310.Martins, R.; Bertani, R. The non-Amazonian species of the Brazilian wandering spiders of the genus Phoneutria Perty, 1833 (Araneae: Ctenidae), with the description of a new species. J. Zootaxa 2007, 1526, 1–36.Valenzuela-Rojas, J.C.; González-Gómez, J.C.; van der Meijden, A.; Cortés, J.N.; Guevara, G.; Franco, L.M.; Pekár, S.; García, L.F. Prey and Venom Efficacy of Male and Female Wandering Spider, Phoneutria boliviensis (Araneae: Ctenidae). Toxins 2019, 11, 622.Sierra Ramírez, D.; Guevara, G.; Franco Pérez, L.M.; van der Meijden, A.; González-Gómez, J.C.; Carlos Valenzuela-Rojas, J.; Prada Quiroga, C.F. Deciphering the diet of a wandering spider (Phoneutria boliviensis; Araneae: Ctenidae) by DNA metabarcoding of gut contents. Ecol. Evol. 2021, 11, 5950–5965.Hu, Z.; Chen, B.; Xiao, Z.; Zhou, X.; Liu, Z. Transcriptomic Analysis of the Spider Venom Gland Reveals Venom Diversity and Species Consanguinity. Toxins 2019, 11, 68.Paiva, A.L.B.; Mudadu, M.A.; Pereira, E.H.T.; Marri, C.A.; Guerra-Duarte, C.; Diniz, M.R.V. Transcriptome analysis of the spider Phoneutria pertyi venom glands reveals novel venom components for the genus Phoneutria. Toxicon Off. J. Int. Soc. Toxinology 2019, 163, 59–69.Vásquez-Escobar, J.; Romero-Gutiérrez, T.; Morales, J.A.; Clement, H.C.; Corzo, G.A.; Benjumea, D.M.; Corrales-García, L.L. Transcriptomic Analysis of the Venom Gland and Enzymatic Characterization of the Venom of Phoneutria depilata (Ctenidae) from Colombia. Toxins 2022, 14, 295.Gangur, A.N.; Smout, M.; Liddell, M.J.; Seymour, J.E.; Wilson, D.; Northfield, T.D. Changes in predator exposure, but not in diet, induce phenotypic plasticity in scorpion venom. Proc. Biol. Sci. 2017, 284, 20171364.Pucca, M.B.; Amorim, F.G.; Cerni, F.A.; Bordon Kde, C.; Cardoso, I.A.; Anjolette, F.A.; Arantes, E.C. Influence of post-starvation extraction time and prey-specific diet in Tityus serrulatus scorpion venom composition and hyaluronidase activity. Toxicon Off. J. Int. Soc. Toxinology 2014, 90, 326–336.McElroy, T.; McReynolds, C.N.; Gulledge, A.; Knight, K.R.; Smith, W.E.; Albrecht, E.A. Differential toxicity and venom gland gene expression in Centruroides vittatus. PLoS ONE 2017, 12, e0184695.Herzig, V.; Hodgson, W.C. Intersexual variations in the pharmacological properties of Coremiocnemis tropix (Araneae, Theraphosidae) spider venom. Toxicon Off. J. Int. Soc. Toxinology 2009, 53, 196–205.Wilder, S.M.; Simpson, S.J.J.F.W. A vertebrate, the fence skink, is a common but relatively low-quality prey for an invertebrate predator, the redback spider. Food Webs 2022, 32, e00236.Cordeiro Mdo, N.; de Figueiredo, S.G.; Valentim Ado, C.; Diniz, C.R.; von Eickstedt, V.R.; Gilroy, J.; Richardson, M. Purification and amino acid sequences of six Tx3 type neurotoxins from the venom of the Brazilian ‘armed’ spider Phoneutria nigriventer (Keys). Toxicon Off. J. Int. Soc. Toxinology 1993, 31, 35–42.Diniz, M.R.V.; Paiva, A.L.B.; Guerra-Duarte, C.; Nishiyama, M.Y., Jr.; Mudadu, M.A.; Oliveira, U.; Borges, M.H.; Yates, J.R.; Junqueira-de-Azevedo, I.L. An overview of Phoneutria nigriventer spider venom using combined transcriptomic and proteomic approaches. PLoS ONE 2018, 13, e0200628.Nunes, K.P.; Costa-Gonçalves, A.; Lanza, L.F.; Cortes, S.F.; Cordeiro, M.N.; Richardson, M.; Pimenta, A.M.; Webb, R.C.; Leite, R.; De Lima, M.E. Tx2-6 toxin of the Phoneutria nigriventer spider potentiates rat erectile function. Toxicon Off. J. Int. Soc. Toxinology 2008, 51, 1197–1206.De Figueiredo, S.G.; de Lima, M.E.; Nascimento Cordeiro, M.; Diniz, C.R.; Patten, D.; Halliwell, R.F.; Gilroy, J.; Richardson, M. Purification and amino acid sequence of a highly insecticidal toxin from the venom of the brazilian spider Phoneutria nigriventer which inhibits NMDA-evoked currents in rat hippocampal neurones. Toxicon Off. J. Int. Soc. Toxinology 2001, 39, 309–317.Haas, B.J.; Papanicolaou, A.; Yassour, M.; Grabherr, M.; Blood, P.D.; Bowden, J.; Couger, M.B.; Eccles, D.; Li, B.; Lieber, M.; et al. De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 2013, 8, 1494–1512.Huson, D.H.; Auch, A.F.; Qi, J.; Schuster, S.C. MEGAN analysis of metagenomic data. Genome Res. 2007, 17, 377–386.Winter, D.J. rentrez: An R package for the NCBI eUtils API. R J. 2017, 9, 520–526.Anders, S.; Pyl, P.T.; Huber, W. HTSeq—A Python framework to work with high-throughput sequencing data. Bioinformatics 2015, 31, 166–169.Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550.Boutet, E.; Lieberherr, D.; Tognolli, M.; Schneider, M.; Bairoch, A. UniProtKB/Swiss-Prot. Methods Mol. Biol. 2007, 406, 89–112.Karuppasamy, M.P.; Venkateswaran, S.; Subbiah, P. PDB-2-PBv3.0: An updated protein block database. J. Bioinform. Comput. Biol. 2020, 18, 2050009.© 2023 by the authors.info:eu-repo/semantics/openAccesshttp://purl.org/coar/access_right/c_abf2Atribución-NoComercial 4.0 Internacional (CC BY-NC 4.0)https://creativecommons.org/licenses/by-nc/4.0/https://www.mdpi.com/2072-6651/15/7/429Secuenciación de próxima generaciónArañaTranscriptómicaVenenosaGlándula venenosaNext-generation sequencingSpiderTranscriptomicsVenomicsVenom glandIntersexual Differences in the Gene Expression of Phoneutria depilata (Araneae, Ctenidae) Toxins Revealed by Venom Gland Transcriptome AnalysesArtículo de revistahttp://purl.org/coar/resource_type/c_2df8fbb1http://purl.org/coar/version/c_970fb48d4fbd8a85Textinfo:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionPublicationLICENSElicense.txtlicense.txttext/plain; charset=utf-8134https://repositorio.unibague.edu.co/bitstreams/ce74e6ce-0712-48f3-8df3-582644236bb3/download2fa3e590786b9c0f3ceba1b9656b7ac3MD52TEXTArtículo.pdf.txtArtículo.pdf.txtExtracted texttext/plain3894https://repositorio.unibague.edu.co/bitstreams/ec64a542-af7f-483c-979a-f5077dad4862/downloadd03ecd8ab7f961275b0cafeeeb33e73dMD53THUMBNAILArtículo.pdf.jpgArtículo.pdf.jpgIM Thumbnailimage/jpeg35076https://repositorio.unibague.edu.co/bitstreams/ee3f61cb-3047-4ea2-a32e-c2f77e4ddd38/download519615f238ed470b5c98b51100dcc817MD54ORIGINALArtículo.pdfArtículo.pdfapplication/pdf113647https://repositorio.unibague.edu.co/bitstreams/6ed5b49d-472f-4abd-ad18-7c49a868105d/download43c04aaca50157325872790b59a406dbMD5120.500.12313/5627oai:repositorio.unibague.edu.co:20.500.12313/56272025-09-12 12:21:15.262https://creativecommons.org/licenses/by-nc/4.0/© 2023 by the authors.https://repositorio.unibague.edu.coRepositorio Institucional Universidad de Ibaguébdigital@metabiblioteca.comQ3JlYXRpdmUgQ29tbW9ucyBBdHRyaWJ1dGlvbi1Ob25Db21tZXJjaWFsLU5vRGVyaXZhdGl2ZXMgNC4wIEludGVybmF0aW9uYWwgTGljZW5zZQ0KaHR0cHM6Ly9jcmVhdGl2ZWNvbW1vbnMub3JnL2xpY2Vuc2VzL2J5LW5jLW5kLzQuMC8=

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