The Significance of Comparative Genomics in Modern Evolutionary Venomics

Abstract

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.

Phylogeny-Guided Selection of Priority Groups for Venom Bioprospecting: Harvesting Toxin Sequences in Tarantulas as a Case Study

“…The advent of venom-focused genomics, transcriptomics, and proteomics has provided the means to study venoms in a high-throughput and cost-effective manner [34,35]. We are confident that the application of venomics to the priority groups we have identified will contribute to the understanding of theraphosid venoms and will help to accelerate venom-based biodiscovery programs focusing on these intriguing and charismatic spiders.…”

“…For example, many of the unstudied venomous species are rather small, and it is notoriously difficult to obtain meaningful amounts of venom for bioactivity screens or proteomic studies from these. Furthermore, some of these species are difficult to study because of their secretive lifestyle or their natural habitat being cumbersome to explore [4,35]. Additionally, political restrictions, such as those imposed by the Nagoya Protocol, are major impediments that somewhat negatively affect venom bioprospecting (see [47] for a discussion on the topic using microbiology as an example).…”

Proteo-Transcriptomic Analysis Identifies Potential Novel Toxins Secreted by the Predatory, Prey-Piercing Ribbon Worm Amphiporus lactifloreus

“…Many toxins arise from the duplication of genes encoding proteins and peptides with normal physiological functions, resulting in high similarities between the neofunctionalized toxin and its ancestral protein [17,27,28]. To reduce false-positive matches, we compared the BLASTP results of the 314 candidate transcripts (e ≤ 0.001) against nemertean-specific toxins, known toxins (ToxProt), and known proteins including normal physiological variants (SwissProt).…”

A brief review on the natural history, venomics and the medical importance of bushmaster (Lachesis) pit viper snakes

“…However, genomic resources are currently only available for a handful of squamous reptiles ( Alföldi et al, 2011 ; Castoe et al, 2013 ; Giorgianni et al, 2020 ; Green et al, 2014 ; Kerkkamp et al, 2016 ; Li et al, 2018 ; Lind et al, 2019 ; Peng et al, 2020 ; Schield et al, 2019 ; Shibata et al, 2018 ; Suryamohan et al, 2020 ; Tollis et al, 2014 ; Ullate-Agote et al, 2014 ; Vonk et al, 2013 ; Yin et al, 2016 ). Comparative Squamata omics (genomics, transcriptomics, and proteomics) will play a fundamental role in filling this gap and addressing the connection between genome evolution and the present-day adaptive phenotype for fitness related traits ( Cenik et al, 2015 ; Drukewitz and von Reumont, 2019 ; Eckalbar et al, 2013 ; Hajirasouliha and Tilgner, 2019 ).…”