An ancient, conserved gene regulatory network led to the rise of oral venom systems

Barua, Agneesh; Mikheyev, Alexander S.

doi:10.1101/2020.08.06.240747

Cited by 5 publications

(8 citation statements)

References 98 publications

(109 reference statements)

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“…Setting up venom production requires novel specialized tissues and glands, in which a set of genes originally not related to the venomous function is recruited and modified to encode potent toxins. Most animal toxins represent rather few broad classes of proteins [54], but being broadly distributed across unrelated venomous animal taxa, they expectedly have been recruited from very different genomic backgrounds [57]. This general trend to convergent evolution provides a unique opportunity to disentangle the interplay of conserved and lineage-specific mechanisms that govern recruitment and evolution of venom peptides.…”

Section: Discussionmentioning

confidence: 99%

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Vexitoxins: conotoxin-like venom peptides from predatory gastropods of the genus Vexillum

et al. 2022

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Venoms of predatory marine cone snails are intensely studied because of the biomedical applications of the neuropeptides that they contain, termed conotoxins. Meanwhile some gastropod lineages have independently acquired secretory glands strikingly similar to the venom gland of cone snails, suggesting that they possess similar venoms. Here we focus on the most diversified of these clades, the genus Vexillum . Based on the analysis of a multi-species proteo-transcriptomic dataset, we show that Vexillum species indeed produce complex venoms dominated by highly diversified short cysteine-rich peptides, vexitoxins. Vexitoxins possess the same precursor organization, display overlapping cysteine frameworks and share several common post-translational modifications with conotoxins. Some vexitoxins show sequence similarity to conotoxins and adopt similar domain conformations, including a pharmacologically relevant inhibitory cysteine knot motif. The Vexillum envenomation gland (gL) is a notably more recent evolutionary novelty than the conoidean venom gland. Thus, we hypothesize lower divergence between vexitoxin genes, and their ancestral ‘somatic’ counterparts compared to that in conotoxins, and we find support for this hypothesis in the evolution of the vexitoxin cluster V027. We use this example to discuss how future studies on vexitoxins can inform the origin of conotoxins, and how they may help to address outstanding questions in venom evolution.

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Section: Discussionmentioning

confidence: 99%

“…Currently, most efforts to this end focus on the well-characterized taxa of venomous animals, mainly on snakes (e.g. [57,58]), and extending such studies to new system(s) will greatly magnify the power of comparative analysis. Essentially such system can be seeded by a pair of distantly related taxa that have independently acquired venoms.…”

Section: Discussionmentioning

confidence: 99%

Vexitoxins: conotoxin-like venom peptides from predatory gastropods of the genus Vexillum

et al. 2022

View full text Add to dashboard Cite

show abstract

“…Setting up venom production requires novel specialized tissues and glands, in which a set of genes originally not related to the venomous function is recruited and modified to encode potent toxins. Most animal toxins represent rather few broad classes of proteins, such as cysteine rich secretory peptides (CRISPs), hyaluronidases, kunitz-phospholipase and serine-type proteases (Zancolli & Casewell 2020), but being broadly distributed across unrelated venomous animal taxa, they have been recruited from very different genomic backgrounds (Barua & Mikheyev 2021). This general trend to convergent evolution provides a unique opportunity to disentangle the interplay of lineage-specific and conserved mechanisms that govern recruitment and evolution of venom peptides.…”

Section: Discussionmentioning

confidence: 99%

“…Currently, most efforts to this end focus on the well characterized taxa of venomous animals, mainly on snakes (e.g. Barua & Mikheyev 2019, 2021), and extending such studies to new system(s) will greatly magnify the power of comparative analysis. Essentially, such system can be seeded by a pair of distantly related taxa that have independently acquired venom function, and cone snails and Vexillum representing unrelated evolutionary successful radiations of venomous neogastropods are thus a perfect system.…”

Section: Discussionmentioning

confidence: 99%

Vexitoxins: a novel class of conotoxin-like venom peptides from predatory gastropods of the genus Vexillum

Kuznetsova¹,

Zvonareva

Ziganshin

et al. 2022

Preprint

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Venoms of predatory marine cone snails (the family Conidae, order Neogastropoda) are intensely studied because of the broad range of biomedical applications of the neuropeptides that they contain, conotoxins. Meanwhile anatomy in some other neogastropod lineages strongly suggests that they have evolved similar venoms independently of cone snails, nevertheless their venom composition remains unstudied. Here we focus on the most diversified of these lineages, the genus Vexillum (the family Costellariidae). We have generated comprehensive multi-specimen, multi-tissue RNA-Seq data sets for three Vexillum species, and supported our findings in two species by proteomic profiling. We show that venoms of Vexillum are dominated by highly diversified short cysteine-rich peptides that in many aspects are very similar to conotoxins. Vexitoxins possess the same precursor organization, display overlapping cysteine frameworks and share several common post-translational modifications with conotoxins. Some vexitoxins show detectable sequence similarity to conotoxins, and are predicted to adopt similar domain conformations, including a pharmacologically relevant inhibitory cysteine-know motif (ICK). The tubular gL of Vexillum is a notably more recent evolutionary novelty than the conoidean venom gland. Thus, we hypothesize lower divergence between the toxin genes, and their somatic counterparts compared to that in conotoxins, and we find support for this hypothesis in the molecular evolution of the vexitoxin cluster V027. We use this example to discuss how future studies on vexitoxins can inform origin and evolution of conotoxins, and how they may help addressing standing questions in venom evolution.

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“…To remove these batch effects and identify any existing patterns in expression between tissues and species, we used an empirical Bayes method implemented via the ComBat function in sva R package (72). This approach has been successfully implemented in previous studies (28, 73, 74).…”

Section: Methodsmentioning

confidence: 99%

The genetic basis for adaptation in giant sea anemones to their symbiosis with anemonefish and Symbiodiniaceae

Barua

Kashimoto

Khalturin

et al. 2022

Preprint

Self Cite

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Sea anemones in the order Anthozoa play an integral part in marine ecosystems by providing refuge and habitat for various organisms. Despite this, much of their molecular ecology remains elusive. Sea anemones can nurture numerous symbiotic relationships; the most iconic being the one between giant sea anemones and anemonefish. However, the genes and biological processes associated with this symbiosis in the sea anemones in unknown. Additionally, it is unclear how genes can mediate interactions between sea anemones, anemonefish, and symbionts from the algal family Symbiodiniaceae. Here we compared the gene expression profiles of tentacles from several cnidarians to uncover the genetic basis for adaptations in giant sea anemones to their symbiosis with anemonefish and Symbiodiniaceae. We found that tentacle transcriptomes of cnidarians are highly diverse, with closely related species having more similar expression patterns. However, despite an overall high correlation between gene expression and phylogeny, the giant sea anemones showed distinct expression patterns. The giant sea anemones had gene co-expression clusters enriched for processes involved in nutrient exchange and metabolism. These genes were not only differentially expressed, but also experienced evolutionary shifts in expression in giant sea anemones. Using a phylogenetic multilevel model, we found that Symbiodiniaceae and anemonefish significantly affect gene expression in giant sea anemone tentacles. By characterizing gene expression patterns, we identify genes and biological processes that provide evidence for the cross-talk between Symbiodiniaceae, anemonefish, and giant sea anemones. Our study demonstrates how integrated biological processes can lead to the evolution of a successful multi-organism interaction.

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An ancient, conserved gene regulatory network led to the rise of oral venom systems

Cited by 5 publications

References 98 publications

Vexitoxins: conotoxin-like venom peptides from predatory gastropods of the genus Vexillum

Vexitoxins: conotoxin-like venom peptides from predatory gastropods of the genus Vexillum

Vexitoxins: a novel class of conotoxin-like venom peptides from predatory gastropods of the genus Vexillum

The genetic basis for adaptation in giant sea anemones to their symbiosis with anemonefish and Symbiodiniaceae

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