Ecological venomics: How genomics, transcriptomics and proteomics can shed new light on the ecology and evolution of venom

Sunagar, Kartik; Morgenstern, David; Reitzel, Adam M.; Moran, Yehu

doi:10.1016/j.jprot.2015.09.015

Cited by 73 publications

(77 citation statements)

References 174 publications

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“…Among the focal taxa, the potential ecological role of these toxin-like transcripts may play in this tissue-specific venom composition (discussed below) indicates that these genes may be functionally venomous in a tissue that is typically characterized as being nonvenomous in nature. Although not evaluated here, tissue-specific toxin expression could vary over time and across environments (Dutertre et al 2014; Sunagar et al 2016). Future tissue-specific investigations in sea anemone venom composition would benefit from systematically monitoring changes in toxin gene expression during ecologically relevant interactions (i.e., in the presence of symbionts, predators, or prey) over longer time scales.…”

Section: Discussionmentioning

confidence: 99%

Tissue-Specific Venom Composition and Differential Gene Expression in Sea Anemones

2016

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Cnidarians represent one of the few groups of venomous animals that lack a centralized venom transmission system. Instead, they are equipped with stinging capsules collectively known as nematocysts. Nematocysts vary in abundance and type across different tissues; however, the venom composition in most species remains unknown. Depending on the tissue type, the venom composition in sea anemones may be vital for predation, defense, or digestion. Using a tissue-specific RNA-seq approach, we characterize the venom assemblage in the tentacles, mesenterial filaments, and column for three species of sea anemone (Anemonia sulcata, Heteractis crispa, and Megalactis griffithsi). These taxa vary with regard to inferred venom potency, symbiont abundance, and nematocyst diversity. We show that there is significant variation in abundance of toxin-like genes across tissues and species. Although the cumulative toxin abundance for the column was consistently the lowest, contributions to the overall toxin assemblage varied considerably among tissues for different toxin types. Our gene ontology (GO) analyses also show sharp contrasts between conserved GO groups emerging from whole transcriptome analysis and tissue-specific expression among GO groups in our differential expression analysis. This study provides a framework for future characterization of tissue-specific venom and other functionally important genes in this lineage of simple bodied animals.

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Section: Discussionmentioning

confidence: 99%

Tissue-Specific Venom Composition and Differential Gene Expression in Sea Anemones

2016

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“…Thus, in answer to the question posed above, we would like to propose that although there is a remarkable diversity between these portals , they are tightly linked to the amplification attained by the relatively limited cellular signaling transduction cascades. The recent development of venomics [446], toxins proteomics and genomics may facilitate rapid screenings for toxicity of molecules acting on this signal transduction machinery [447,448], based on safety as well as efficacy, thereby providing solid grounds for better drug discovery and translational medicine [449]. …”

Section: Discussionmentioning

confidence: 99%

The Molecular Basis of Toxins’ Interactions with Intracellular Signaling via Discrete Portals

Lahiani

Yavin

Lazarovici

2017

Toxins

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An understanding of the molecular mechanisms by which microbial, plant or animal-secreted toxins exert their action provides the most important element for assessment of human health risks and opens new insights into therapies addressing a plethora of pathologies, ranging from neurological disorders to cancer, using toxinomimetic agents. Recently, molecular and cellular biology dissecting tools have provided a wealth of information on the action of these diverse toxins, yet, an integrated framework to explain their selective toxicity is still lacking. In this review, specific examples of different toxins are emphasized to illustrate the fundamental mechanisms of toxicity at different biochemical, molecular and cellular- levels with particular consideration for the nervous system. The target of primary action has been highlighted and operationally classified into 13 sub-categories. Selected examples of toxins were assigned to each target category, denominated as portal, and the modulation of the different portal’s signaling was featured. The first portal encompasses the plasma membrane lipid domains, which give rise to pores when challenged for example with pardaxin, a fish toxin, or is subject to degradation when enzymes of lipid metabolism such as phospholipases A2 (PLA2) or phospholipase C (PLC) act upon it. Several major portals consist of ion channels, pumps, transporters and ligand gated ionotropic receptors which many toxins act on, disturbing the intracellular ion homeostasis. Another group of portals consists of G-protein-coupled and tyrosine kinase receptors that, upon interaction with discrete toxins, alter second messengers towards pathological levels. Lastly, subcellular organelles such as mitochondria, nucleus, protein- and RNA-synthesis machineries, cytoskeletal networks and exocytic vesicles are also portals targeted and deregulated by other diverse group of toxins. A fundamental concept can be drawn from these seemingly different toxins with respect to the site of action and the secondary messengers and signaling cascades they trigger in the host. While the interaction with the initial portal is largely determined by the chemical nature of the toxin, once inside the cell, several ubiquitous second messengers and protein kinases/ phosphatases pathways are impaired, to attain toxicity. Therefore, toxins represent one of the most promising natural molecules for developing novel therapeutics that selectively target the major cellular portals involved in human physiology and diseases.

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“…Venomous species are extremely diverse and ubiquitously evolved in all known animal phyla, as for example in old lineages such as marine cnidarians, molluscs, or polychaetes, but also terrestrial groups like reptiles, all major arthropod clades and even mammals Dutertre et al, 2014;von Reumont et al, 2014a,b). It is estimated that around 200,000 animal species (Holford et al, 2018) use venom as the utmost important molecular trait that guarantees the fitness and survival of species being employed for defense, predation, and competition von Reumont et al, 2014a;Sunagar et al, 2016), see also Figure 1. In contrast to poisons, which are generally composed of less complex mixtures of toxic substances and used in a rather unspecific manner, venoms are constituted by complex toxin components such as peptides, proteins, and other smaller organic molecules (Fry et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

“…Another reason that venom systems of most taxa remain unstudied is that only in the last years the modern, methodological toolbox has been established to easily assess the composition of venoms and the mode of their delivery of so far neglected, in many cases very small and more difficult to access species (Sunagar et al, 2016;von Reumont, 2018). The research area that addresses all aspects of venom related research is nowadays called venomics, a term that was originally coined in 2004 for proteomic-based analyses on snake venoms (Juárez et al, 2004;Bazaa et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

“…Today the term venomics reflects the combination of several new-omics technologies to conduct general research on venoms in an integrative approach, see also (Calvete, 2017). Besides new approaches to identify more effectively secreted proteins via proteomics, new sequencing technologies provide in unprecedented details the framework to study evolution of venoms and toxin expression (Gopalakrishnakone and Calvete, 2016;Sunagar et al, 2016;von Reumont, 2018). Particularly for small, so far neglected venomous species, transcriptomics and proteo-transcriptomics appear as the foremost methods to assess possible venom compositions and contribute to extend our comprehension of venom diversity in general.…”

Section: Introductionmentioning

confidence: 99%

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The Significance of Comparative Genomics in Modern Evolutionary Venomics

Drukewitz

Reumont

2019

Front. Ecol. Evol.

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Venoms evolved convergently in diverse animal lineages as key adaptations that increase the evolutionary fitness of species which are manifold employed for defense, predation, and competition. They constitute complex cocktails of various toxins that feature a broad range of bioactivities. The majority of described venom proteins belong to protein families that are known to comprise housekeeping genes or harbor protein-domains, which are present in genes with non-venom related functions. However, the evolutionary processes and mechanisms that foster the origin of these venom proteins and triggered their recruitment into the venom delivery system are still critically discussed. In most instances single or combined proteomic and transcriptomic approaches are applied to describe venom compositions and the biological context of venoms. For neglected species these studies represent crucial contributions to improve our understanding of venom diversity on a broader scale. Nonetheless, the inference of the evolutionary origin of putative toxins in these studies could be misleading without appropriate coverage of gene populations from different tissue samples (gene completeness) or complementary genome data. Providing a valid backbone to correctly map transcriptome and proteome data, whole genome sequences facilitate a clear distinction between variability of venom proteins or toxins due to posttranslational modifications, alternative splicing, and false-positive matches that stem from sequencing or read processing and assembly errors. High-quality whole genome sequence data of venomous species are still sparse and unevenly distributed within taxon lineages. However, to reveal the evolutionary pattern of putative toxins in venomous lineages and to identify ancestral variants of venom proteins, the appropriate sampling of genomes from venomous and non-venomous species is crucial. Nevertheless, larger comparative studies based on multiple whole genome data sets are still sparse to uncover processes of venom evolution. Here, we review the general potential of comparative genomics in venomics to unravel mechanisms and patterns of evolutionary origin of toxin genes. Finally, we discuss the benefit of whole genome data to improve transcriptomics and proteomics-only studies, in particular if datasets are applied to assess the evolutionary origin of venom proteins.

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Ecological venomics: How genomics, transcriptomics and proteomics can shed new light on the ecology and evolution of venom

Cited by 73 publications

References 174 publications

Tissue-Specific Venom Composition and Differential Gene Expression in Sea Anemones

Tissue-Specific Venom Composition and Differential Gene Expression in Sea Anemones

The Molecular Basis of Toxins’ Interactions with Intracellular Signaling via Discrete Portals

The Significance of Comparative Genomics in Modern Evolutionary Venomics

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