Molecular Diversity and Evolutionary Trends of Cysteine-rich Peptides from the Venom Glands of Chinese Spider Heteropoda Venatoria

Overview

Journal Sci Rep

Specialty Science

Date 2021 Feb 6

PMID 33547373

Citations 5

Authors

Jie Luo

Yiying Ding

Zhihao Peng

Kezhi Chen

Xuewen Zhang

Tiaoyi Xiao

Jinjun Chen

Affiliations

Soon will be listed here.

Abstract

Heteropoda venatoria in the family Sparassidae is highly valued in pantropical countries because the species feed on domestic insect pests. Unlike most other species of Araneomorphae, H. venatoria uses the great speed and strong chelicerae (mouthparts) with toxin glands to capture the insects instead of its web. Therefore, H. venatoria provides unique opportunities for venom evolution research. The venom of H. venatoria was explored by matrix-assisted laser desorption/ionization tandem time-of-flight and analyzing expressed sequence tags. The 154 sequences coding cysteine-rich peptides (CRPs) revealed 24 families based on the phylogenetic analyses of precursors and cysteine frameworks in the putative mature regions. Intriguingly, four kinds of motifs are first described in spider venom. Furthermore, combining the diverse CRPs of H. venatoria with previous spider venom peptidomics data, the structures of precursors and the patterns of cysteine frameworks were analyzed. This work revealed the dynamic evolutionary trends of venom CRPs in H. venatoria: the precursor has evolved an extended mature peptide with more cysteines, and a diminished or even vanished propeptides between the signal and mature peptides; and the CRPs evolved by multiple duplications of an ancestral ICK gene as well as recruitments of non-toxin genes.

Citing Articles

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References

Kaur G, Iyer L, Subramanian S, Aravind L . Evolutionary convergence and divergence in archaeal chromosomal proteins and Chromo-like domains from bacteria and eukaryotes. Sci Rep. 2018; 8(1):6196. PMC: 5906684. DOI: 10.1038/s41598-018-24467-z. View

Fry B, Roelants K, Champagne D, Scheib H, Tyndall J, King G . The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet. 2009; 10:483-511. DOI: 10.1146/annurev.genom.9.081307.164356. View

Herzig V, Wood D, Newell F, Chaumeil P, Kaas Q, Binford G . ArachnoServer 2.0, an updated online resource for spider toxin sequences and structures. Nucleic Acids Res. 2010; 39(Database issue):D653-7. PMC: 3013666. DOI: 10.1093/nar/gkq1058. View

Ikeda N, Chijiwa T, Matsubara K, Oda-Ueda N, Hattori S, Matsuda Y . Unique structural characteristics and evolution of a cluster of venom phospholipase A2 isozyme genes of Protobothrops flavoviridis snake. Gene. 2010; 461(1-2):15-25. DOI: 10.1016/j.gene.2010.04.001. View

Puillandre N, Bouchet P, Duda Jr T, Kauferstein S, Kohn A, Olivera B . Molecular phylogeny and evolution of the cone snails (Gastropoda, Conoidea). Mol Phylogenet Evol. 2014; 78:290-303. PMC: 5556946. DOI: 10.1016/j.ympev.2014.05.023. View

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

Kaas Q, Craik D . Bioinformatics-Aided Venomics. Toxins (Basel). 2015; 7(6):2159-87. PMC: 4488696. DOI: 10.3390/toxins7062159. View

Zhu S, Peigneur S, Gao B, Luo L, Jin D, Zhao Y . Molecular diversity and functional evolution of scorpion potassium channel toxins. Mol Cell Proteomics. 2010; 10(2):M110.002832. PMC: 3033675. DOI: 10.1074/mcp.M110.002832. View

King G, Gentz M, Escoubas P, Nicholson G . A rational nomenclature for naming peptide toxins from spiders and other venomous animals. Toxicon. 2008; 52(2):264-76. DOI: 10.1016/j.toxicon.2008.05.020. View

10.

Kozlov S, Malyavka A, McCutchen B, Lu A, Schepers E, Herrmann R . A novel strategy for the identification of toxinlike structures in spider venom. Proteins. 2005; 59(1):131-40. DOI: 10.1002/prot.20390. View

11.

Garb J, Hayashi C . Molecular evolution of α-latrotoxin, the exceptionally potent vertebrate neurotoxin in black widow spider venom. Mol Biol Evol. 2013; 30(5):999-1014. PMC: 3670729. DOI: 10.1093/molbev/mst011. View

12.

Vassilevski A, Kozlov S, Grishin E . Molecular diversity of spider venom. Biochemistry (Mosc). 2010; 74(13):1505-34. DOI: 10.1134/s0006297909130069. View

13.

Kumar S, Stecher G, Li M, Knyaz C, Tamura K . MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol. 2018; 35(6):1547-1549. PMC: 5967553. DOI: 10.1093/molbev/msy096. View

14.

Nishikawa T, Ota T, Kawai Y, Ishii S, Saito K, Yamamoto J . Database and analysis system for cDNA clones obtained from full-length enriched cDNA libraries. In Silico Biol. 2002; 2(1):5-18. View

15.

LARKIN M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H . Clustal W and Clustal X version 2.0. Bioinformatics. 2007; 23(21):2947-8. DOI: 10.1093/bioinformatics/btm404. View

16.

Pineda S, Chaumeil P, Kunert A, Kaas Q, Thang M, Le L . ArachnoServer 3.0: an online resource for automated discovery, analysis and annotation of spider toxins. Bioinformatics. 2017; 34(6):1074-1076. DOI: 10.1093/bioinformatics/btx661. View

17.

Norton R, Pallaghy P . The cystine knot structure of ion channel toxins and related polypeptides. Toxicon. 1998; 36(11):1573-83. DOI: 10.1016/s0041-0101(98)00149-4. View

18.

Zhang Y, Huang Y, He Q, Liu J, Luo J, Zhu L . Toxin diversity revealed by a transcriptomic study of Ornithoctonus huwena. PLoS One. 2014; 9(6):e100682. PMC: 4065081. DOI: 10.1371/journal.pone.0100682. View

19.

Berkut A, Peigneur S, Myshkin M, Paramonov A, Lyukmanova E, Arseniev A . Structure of membrane-active toxin from crab spider Heriaeus melloteei suggests parallel evolution of sodium channel gating modifiers in Araneomorphae and Mygalomorphae. J Biol Chem. 2014; 290(1):492-504. PMC: 4281751. DOI: 10.1074/jbc.M114.595678. View

20.

Gracy J, Chiche L . Structure and modeling of knottins, a promising molecular scaffold for drug discovery. Curr Pharm Des. 2011; 17(38):4337-50. DOI: 10.2174/138161211798999339. View