Linear Peptides-A Combinatorial Innovation in the Venom of Some Modern Spiders.

Lucia Kuhn-Nentwig,Heidi E L Lischer,Marco Isaia,Wolfgang Nentwig,Maria J Albo,Nicolas Langenegger,Stano Pekár

doi:10.3389/fmolb.2021.705141

Abstract

In the venom of spiders, linear peptides (LPs), also called cytolytical or antimicrobial peptides, represent a largely neglected group of mostly membrane active substances that contribute in some spider species considerably to the killing power of spider venom. By next-generation sequencing venom gland transcriptome analysis, we investigated 48 spider species from 23 spider families and detected LPs in 20 species, belonging to five spider families (Ctenidae, Lycosidae, Oxyopidae, Pisauridae, and Zodariidae). The structural diversity is extraordinary high in some species: the lynx spider Oxyopes heterophthalmus contains 62 and the lycosid Pardosa palustris 60 different LPs. In total, we identified 524 linear peptide structures and some of them are in lycosids identical on amino acid level. LPs are mainly encoded in complex precursor structures in which, after the signal peptide and propeptide, 13 or more LPs (Hogna radiata) are connected by linkers. Besides Cupiennius species, also in Oxyopidae, posttranslational modifications of some precursor structures result in the formation of two-chain peptides. It is obvious that complex precursor structures represent a very suitable and fast method to produce a high number and a high diversity of bioactive LPs as economically as possible. At least in Lycosidae, Oxyopidae, and in the genus Cupiennius, LPs reach very high Transcripts Per Kilobase Million values, indicating functional importance within the envenomation process.

Highlights

Spiders (Araneae) colonize most terrestrial ecosystems and are with 49,400 confirmed species among the most successful invertebrate groups (WSC, 2021)
Following the here presented state of knowledge, it is remarkable that linear peptides (LPs) in spider venoms occur only in the RTA-clade, a rather modern branch of spiders
This allows the conclusion that LPs are a modern development among the main venom component groups and that the investment into LPs obviously boosted the toxicity of the venom and broadens the spectrum of possible prey

Summary

Introduction

Spiders (Araneae) colonize most terrestrial ecosystems and are with 49,400 confirmed species among the most successful invertebrate groups (WSC, 2021). They appeared at the end of the Carboniferous, some 315 million years ago. One of the most recent and most species-rich spider families, wolf spiders (Lycosidae) (Piacentini and Ramírez, 2019), evolved approximately 20 million years ago and belongs to a group of more than 30 families, the so-called retrolateral tibial apophysis clade (RTA-clade). The identification of LPs in spider venoms was limited to only eight spider species, all belonging to the mentioned RTA-clade, namely lycosids (Yan and Adams, 1998; Budnik et al, 2004; Melo-Braga et al, 2020), oxyopids (Corzo et al, 2002; Dubovskii et al, 2011), zodariids (Kozlov et al, 2006; Vassilevski et al, 2008; Dubovskii et al, 2015), ctenids (Pimenta et al, 2005), and the trechaleids Cupiennius salei and C. getazi (Kuhn-Nentwig et al, 2002; Kuhn-Nentwig, 2021)

Methods

Results

Conclusion