The evolutionary dynamics of venom toxins made by insects and other animals

Animal venoms are recognised as unique biological systems in which to study molecular evolution. Venom use has evolved numerous times among the insects, and insects today use venom to capture prey, defend themselves from predators, or to subdue and modulate host responses during parasitism. However, little is known about most insect venom toxins or the mode and tempo by which they evolve. Here, I review the evolutionary dynamics of insect venom toxins, and argue that insects offer many opportunities to examine novel aspects of toxin evolution. The key questions addressed are: How do venomous animals evolve from non-venomous animals, and how does this path effect the composition and pharmacology of the venom? What genetic processes (gene duplication, co-option, neofunctionalisation) are most important in toxin evolution? What kinds of selection pressures are acting on toxin-encoding genes and their cognate targets in envenomated animals? The emerging evidence highlights that venom composition and pharmacology adapts quickly in response to changing selection pressures resulting from new ecological interactions, and that such evolution occurs through a stunning variety of genetic mechanisms. Insects offer many opportunities to investigate the evolutionary dynamics of venom toxins due to their evolutionary history rich in venom-related adaptations, and their quick generation time and suitability for culture in the laboratory.

Toxins from scratch? Diverse, multimodal gene origins in the predatory robber fly Dasypogon diadema indicate a dynamic venom evolution in dipteran insects

Background Venoms and the toxins they contain represent molecular adaptations that have evolved on numerous occasions throughout the animal kingdom. However, the processes that shape venom protein evolution are poorly understood because of the scarcity of whole-genome data available for comparative analyses of venomous species. Results We performed a broad comparative toxicogenomic analysis to gain insight into the genomic mechanisms of venom evolution in robber flies (Asilidae). We first sequenced a high-quality draft genome of the hymenopteran hunting robber fly Dasypogon diadema, analysed its venom by a combined proteotranscriptomic approach, and compared our results with recently described robber fly venoms to assess the general composition and major components of asilid venom. We then applied a comparative genomics approach, based on 1 additional asilid genome, 10 high-quality dipteran genomes, and 2 lepidopteran outgroup genomes, to reveal the evolutionary mechanisms and origins of identified venom proteins in robber flies. Conclusions While homologues were identified for 15 of 30 predominant venom protein in the non-asilid genomes, the remaining 15 highly expressed venom proteins appear to be unique to robber flies. Our results reveal that the venom of D. diadema likely evolves in a multimodal fashion comprising (i) neofunctionalization after gene duplication, (ii) expression-dependent co-option of proteins, and (iii) asilid lineage-specific orphan genes with enigmatic origin. The role of such orphan genes is currently being disputed in evolutionary genomics but has not been discussed in the context of toxin evolution. Our results display an unexpected dynamic venom evolution in asilid insects, which contrasts the findings of the only other insect toxicogenomic evolutionary analysis, in parasitoid wasps (Hymenoptera), where toxin evolution is dominated by single gene co-option. These findings underpin the significance of further genomic studies to cover more neglected lineages of venomous taxa and to understand the importance of orphan genes as possible drivers for venom evolution.

Revisiting the Evolution and Taxonomy of Clostridia, a Phylogenomic Update

Clostridium is a large genus of obligate anaerobes belonging to the Firmicutes phylum of bacteria, most of which have a Gram-positive cell wall structure. The genus includes significant human and animal pathogens, causative of potentially deadly diseases such as tetanus and botulism. Despite their relevance and many studies suggesting that they are not a monophyletic group, the taxonomy of the group has largely been neglected. Currently, species belonging to the genus are placed in the unnatural order defined as Clostridiales, which includes the class Clostridia. Here, we used genomic data from 779 strains to study the taxonomy and evolution of the group. This analysis allowed us to 1) confirm that the group is composed of more than one genus, 2) detect major differences between pathogens classified as a single species within the group of authentic Clostridium spp. (sensu stricto), 3) identify inconsistencies between taxonomy and toxin evolution that reflect on the pervasive misclassification of strains, and 4) identify differential traits within central metabolism of members of what has been defined earlier and confirmed by us as cluster I. Our analysis shows that the current taxonomic classification of Clostridium species hinders the prediction of functions and traits, suggests a new classification for this fascinating class of bacteria, and highlights the importance of phylogenomics for taxonomic studies.

Revisiting the evolution and taxonomy of Clostridia, a phylogenomic update

Clostridium is a large genus of obligate anaerobes belonging to the Firmicutes phylum of bacteria, most of which have a Gram-positive cell wall structure. The genus includes significant human and animal pathogens, causative of potentially deadly diseases such as tetanus and botulism. Despite their relevance and many studies suggesting that they are not a monophyletic group, the taxonomy of the group has largely been neglected. Currently, species belonging to the genus are placed in the unnatural order defined as Clostridiales, which includes the class Clostridia. Here we used genomic data from 779 strains to study the taxonomy and evolution of the group. This analysis allowed us to; (i) confirm that the group is composed of more than one genus (ii), detect major differences between pathogens classified as a single species within the group of authentic Clostridium spp. (sensu stricto), identify inconsistencies between taxonomy and toxin evolution that reflect on the pervasive misclassification of strains and, (iv) identify differential traits within central metabolism of members of what has been defined earlier and confirmed by us as cluster I. Our analysis shows that the current taxonomic classification of Clostridium species hinders the prediction of functions and traits, suggests a new classification for this fascinating class of bacteria and highlights the importance of phylogenomics for taxonomic studies.