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A maximum likelihood tree of PAD sequences shows two clades of centiPAD sequences nested within a paraphyletic backbone of bacterial sequences The tree represents one clade nested within a larger tree (red highlight in inset) made up entirely of bacterial sequences. The tree shows that centiPADs originated from two bacterial HGTs, one within the lithobiomorph lineage, and one within the scutigeromorph lineage. Centipede sequences are in black (present in transcriptomes) and red (present in transcriptomes and venom proteomes). Highlighted sequences are Bacteria (pink) and Fungi (yellow). Metazoan sequences are not highlighted. Collapsed clades have the number of included sequences indicated in parentheses. For the uncollapsed tree see Supplementary Fig. 3. The tree was reconstructed using the WAG + G4 model and is displayed as midpoint rooted. Bootstrap support values are shown for each clade, and clades with support <50% are collapsed into polytomies. Clades without bootstrap values have >95% support. Collembolan image was sourced from Phylopic (www.phylopic.org; credit for the Collembola image is with Birgit Lang: https://creativecommons.org/licenses/by/3.0/).
Source publication
Venoms have evolved over a hundred times in animals. Venom toxins are thought to evolve mostly by recruitment of endogenous proteins with physiological functions. Here we report phylogenetic analyses of venom proteome-annotated venom gland transcriptome data, assisted by genomic analyses, to show that centipede venoms have recruited at least five g...
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A bstract
Animal venoms and other protein-based secretions that perform a variety of functions, from predation to defense, are highly complex cocktails of bioactive compounds. Gene duplication, accompanied by modification of the expression and/or function of one of the duplicates under the action of positive selection, followed by further duplicati...
Citations
... Given that this family is ancestrally a venom component, our results suggest the CAP1 in the telopodal defensive secretion was co-opted from the venom CAP1. Distinct venom and telopodal defensive secretion paralogues are probably also present in the horizontal gene transfer (HGT)-derived PCPDPLP (Fig. 6B) [78], as well as the HGT-derived centiPAD (Additional file 3, Fig. S7) [78], venom peptide families SLPTX30 (Additional file 3, Fig. S8) and SLPTX07 (Additional file 3, Fig. S9), and unknown venom protein family Unchar17 (Additional file 3, Fig. S10). Although our results do not allow us to infer the direction of recruitment, they suggest these families have diversified independently in the two secretions. ...
... Given that this family is ancestrally a venom component, our results suggest the CAP1 in the telopodal defensive secretion was co-opted from the venom CAP1. Distinct venom and telopodal defensive secretion paralogues are probably also present in the horizontal gene transfer (HGT)-derived PCPDPLP (Fig. 6B) [78], as well as the HGT-derived centiPAD (Additional file 3, Fig. S7) [78], venom peptide families SLPTX30 (Additional file 3, Fig. S8) and SLPTX07 (Additional file 3, Fig. S9), and unknown venom protein family Unchar17 (Additional file 3, Fig. S10). Although our results do not allow us to infer the direction of recruitment, they suggest these families have diversified independently in the two secretions. ...
Background
Evolution of novelty is a central theme in evolutionary biology, yet studying the origins of traits with an apparently discontinuous origin remains a major challenge. Venom systems are a well-suited model for the study of this phenomenon because they capture several aspects of novelty across multiple levels of biological complexity. However, while there is some knowledge on the evolution of individual toxins, not much is known about the evolution of venom systems as a whole. One way of shedding light on the evolution of new traits is to investigate less specialised serial homologues, i.e. repeated traits in an organism that share a developmental origin. This approach can be particularly informative in animals with repetitive body segments, such as centipedes.
Results
Here, we investigate morphological and biochemical aspects of the defensive telopodal glandular organs borne on the posterior legs of venomous stone centipedes (Lithobiomorpha), using a multimethod approach, including behavioural observations, comparative morphology, proteomics, comparative transcriptomics and molecular phylogenetics. We show that the anterior venom system and posterior telopodal defence system are functionally convergent serial homologues, where one (telopodal defence) represents a model for the putative early evolutionary state of the other (venom). Venom glands and telopodal glandular organs appear to have evolved from the same type of epidermal gland (four-cell recto-canal type) and while the telopodal defensive secretion shares a great degree of compositional overlap with centipede venoms in general, these similarities arose predominantly through convergent recruitment of distantly related toxin-like components. Both systems are composed of elements predisposed to functional innovation across levels of biological complexity that range from proteins to glands, demonstrating clear parallels between molecular and morphological traits in the properties that facilitate the evolution of novelty.
Conclusions
The evolution of the lithobiomorph telopodal defence system provides indirect empirical support for the plausibility of the hypothesised evolutionary origin of the centipede venom system, which occurred through functional innovation and gradual specialisation of existing epidermal glands. Our results thus exemplify how continuous transformation and functional innovation can drive the apparent discontinuous emergence of novelties on higher levels of biological complexity.
... Occasionally, eukaryotic species formed their own clades, such as for some fungal species. The isolated eukaryotic species among bacterial clades is in agreement with previous analyses of the distribution of DUF3472 domains, which suggested that DUF3472 may have contributed to Chilopoda (centipede) venom repertoires via horizontal gene transfer 43 . Our analysis reveals another potential horizontal gene-transfer event, as evidenced by the monophyletic group containing the animal gut resident Neocallimastix californiae (an early-branching anerobic fungus) and a Clostridiaceae bacterium ( Supplementary Fig. 28). ...
Microbes utilize polysaccharides to protect their surfaces and build biofilms, whereas metazoans employ large mucins densely decorated with O-glycans to protect surfaces and keep microbes at a distance. However, gut microbes in mucus also feed on host mucins, thus imposing a need for continuous renewal to maintain protection, clearance and mucus homeostasis. Glycopeptidases that can cleave mucins are known, but mucinases that specifically cleave mucins are not. Here we report the discovery of such microbial mucinases that cleave mucins with trimmed glycans, recognize dense clusters of O-glycans, and employ a structural fold and catalytic machinery reminiscent of glycan hydrolases and peptidases. These di-glutamate mucinases are also found in eukaryotes, and we propose that they are designed to clear mucins following scavenging of O-glycans to promote healthy gut–microbiome homeostasis.
... El especimen más grande recolectado, con 270 mm, corresponde a Scolopendra gigantea Linnaeus, 1758(Shelley & Kisser, 2000, aunque se conocen fotografías de ejemplares de mayor tamaño (Khanna & Yadav, 1988). La mayoría de los escolopendromorfos posee 21 pares de patas y una minoría considerable 23, con las dos únicas excepciones de Scolopendropsis bahiensis (Brandt, 1841), en la que individuos con 21 segmentos pedales ocurren junto a otros con 23 (Schileyko, 2006), y S. duplicata Chagas-Junior, Edgecombe & Minelli, 2008, en la cual individuos de ambos sexos tienen 39 ó 43 segmentos pedales (Chagas-Júnior et al., 2008;Minelli et al., 2009;Minelli, 2020; ver Apéndice 2). Los ocelos están presentes o ausentes; antenas con 17-35 artejos; segmento forcipular con tergito fusionado al tergito del primer segmento pedal y coxosternito formado por una placa impar sin surco medio; tergitos de los segmentos pedales desiguales (alternancia de grandes y pequeños), Fig. 3. Ejemplos de Lithobiomorpha que se hallan en la Argentina: A-B, Lithobius forficatus (Lithobiidae); C, Lamyctes inermipes inermipes (Henicopidae). ...
Los quilópodos son miriápodos de 4-300 mm de longitud, caracterizados por tener los apéndices del primer segmento corporal transformados en órganos prehensoriales (forcípu-las) con glándulas venenosas. Los ciempiés son artrópodos carnívoros criptozoicos que juegan un papel importante como depredadores en el suelo. Los escolopendromorfos más grandes son de importancia médica porque su morde-dura venenosa puede causar daños a la salud humana. Solo se han reportado 69 taxones (de nivel específico y subespe-cífico) de Argentina, de los cuales 62 son indígenas y siete son exóticos, pertenecientes a los órdenes Geophilomorpha (32), Lithobiomorpha (12), Scolopendromorpha (21) y Scu-tigeromorpha (4). Los escolopendromorfos, seguidos de los geofilomorfos, son los quilópodos argentinos más conocidos en términos de componentes y distribución geográfica. Los litobiomorfos y escutigeromorfos están poco estudiados, como ocurre en otras áreas de la región Neotropical. El nú-mero real de taxones vivos en Argentina podría ser mayor del que se conoce actualmente. Abstract Chilopoda are 4-300 mm length myriapods, characterized by having the appendages of the first body segment transformed in prehensorial organs (forcipulae) with poison glands. Centipedes are cryptozoic, carnivorous arthropods that play an important role as predators in the soil. The larger scolopendromorphs are of medical importance because their poisonous bite can cause injuries to human health. Only 69 taxa (of specific and subspecific level) have been reported from Argentina, of which 62 are indigenous and seven are exotic, belonging to the orders Geophilo-morpha (32), Lithobiomorpha (12), Scolopendromorpha (21) and Scutigeromorpha (4). Scolopendromorphs, followed by geophilomorphs, are the best known Argentine chilopods in terms of components and their geographic distribution. Lithobiomorphs and scutigeromorphs are poorly studied, as occurs in other areas of the Neotropi-cal region. The actual number of living taxa in Argentina could be higher than what is currently known.
... El especimen más grande recolectado, con 270 mm, corresponde a Scolopendra gigantea Linnaeus, 1758(Shelley & Kisser, 2000, aunque se conocen fotografías de ejemplares de mayor tamaño (Khanna & Yadav, 1988). La mayoría de los escolopendromorfos posee 21 pares de patas y una minoría considerable 23, con las dos únicas excepciones de Scolopendropsis bahiensis (Brandt, 1841), en la que individuos con 21 segmentos pedales ocurren junto a otros con 23 (Schileyko, 2006), y S. duplicata Chagas-Junior, Edgecombe & Minelli, 2008, en la cual individuos de ambos sexos tienen 39 ó 43 segmentos pedales (Chagas-Júnior et al., 2008;Minelli et al., 2009;Minelli, 2020; ver Apéndice 2). Los ocelos están presentes o ausentes; antenas con 17-35 artejos; segmento forcipular con tergito fusionado al tergito del primer segmento pedal y coxosternito formado por una placa impar sin surco medio; tergitos de los segmentos pedales desiguales (alternancia de grandes y pequeños), Fig. 3. Ejemplos de Lithobiomorpha que se hallan en la Argentina: A-B, Lithobius forficatus (Lithobiidae); C, Lamyctes inermipes inermipes (Henicopidae). ...
Resumen: Los quilópodos son miriápodos de 4-300 mm de longitud, caracterizados por tener los apéndices del primer segmento corporal transformados en órganos prehensoriales (forcípu-las) con glándulas venenosas. Los ciempiés son artrópodos carnívoros criptozoicos que juegan un papel importante como depredadores en el suelo. Los escolopendromorfos más grandes son de importancia médica porque su morde-dura venenosa puede causar daños a la salud humana. Solo se han reportado 69 taxones (de nivel específico y subespe-cífico) de Argentina, de los cuales 62 son indígenas y siete son exóticos, pertenecientes a los órdenes Geophilomorpha (32), Lithobiomorpha (12), Scolopendromorpha (21) y Scu-tigeromorpha (4). Los escolopendromorfos, seguidos de los geofilomorfos, son los quilópodos argentinos más conocidos en términos de componentes y distribución geográfica. Los litobiomorfos y escutigeromorfos están poco estudiados, como ocurre en otras áreas de la región Neotropical. El número real de taxones vivos en Argentina podría ser mayor del que se conoce actualmente.
Abstract: Chilopoda are 4-300 mm length myriapods, characterized by having the appendages of the first body segment transformed in prehensorial organs (forcipulae) with poison glands. Centipedes are cryptozoic, carnivorous arthropods that play an important role as predators in the soil. The larger scolopendromorphs are of medical importance because their poisonous bite can cause injuries to human health. Only 69 taxa (of specific and subspecific level) have been reported from Argentina, of which 62 are indigenous and seven are exotic, belonging to the orders Geophilo-morpha (32), Lithobiomorpha (12), Scolopendromorpha (21) and Scutigeromorpha (4). Scolopendromorphs, followed by geophilomorphs, are the best known Argentine chilopods in terms of components and their geographic distribution. Lithobiomorphs and scutigeromorphs are poorly studied, as occurs in other areas of the Neotropi-cal region. The actual number of living taxa in Argentina could be higher than what is currently known.
... While evolution acts on genes that are transferred between generations of the same species through normal reproduction (vertical transfer), it also acts on those genes that are more rarely transferred between individuals of different, often distantly related species (horizontal transfer). Horizontal gene transfer increases the genetic diversity that may be recruited to produce venom toxins, and multiple venom toxins encoded by horizontally transferred genes have now been reported (20)(21)(22)(23). ...
... The megalysins are part of the aerolysin toxin family, which is widespread among bacteria, fungi, plants, and animals (38). This protein family has been recruited into the venoms of multiple animal groups including centipedes, cnidarians, and fish, and it is thought to have been transmitted between different lineages of organisms through horizontal gene transfer at least seven times (20,21). Aerolysin-like proteins have also been reported to be produced by nonvenomous lepidopterans, including protein expression in egg yolk (39,40). ...
... The megalysins have been recruited from aerolysin-like proteins which occur in Lepidoptera due to horizontal gene transfer from bacteria. Aerolysin family proteins including the megalysins have been recruited convergently into the venoms of megalopygid caterpillars, centipedes (20), cnidaria, and fish (38). In the case of centipedes, it has been suggested based on phylogenetic analysis that the aerolysin family βpore-forming toxins have been transferred not once but twice from bacteria to centipedes (20). ...
Larvae of the genus Megalopyge (Lepidoptera: Zygaenoidea: Megalopygidae), known as asp or puss caterpillars, produce defensive venoms that cause severe pain. Here, we present the anatomy, chemistry, and mode of action of the venom systems of caterpillars of two megalopygid species, the Southern flannel moth Megalopyge opercularis and the black-waved flannel moth Megalopyge crispata. We show that megalopygid venom is produced in secretory cells that lie beneath the cuticle and are connected to the venom spines by canals. Megalopygid venoms consist of large aerolysin-like pore-forming toxins, which we have named megalysins, and a small number of peptides. The venom system differs markedly from those of previously studied venomous zygaenoids of the family Limacodidae, suggestive of an independent origin. Megalopygid venom potently activates mammalian sensory neurons via membrane permeabilization and induces sustained spontaneous pain behavior and paw swelling in mice. These bioactivities are ablated by treatment with heat, organic solvents, or proteases, indicating that they are mediated by larger proteins such as the megalysins. We show that the megalysins were recruited as venom toxins in the Megalopygidae following horizontal transfer of genes from bacteria to the ancestors of ditrysian Lepidoptera. Megalopygids have recruited aerolysin-like proteins as venom toxins convergently with centipedes, cnidarians, and fish. This study highlights the role of horizontal gene transfer in venom evolution.
... Масштабное выявление HGT началось с наступлением эры секвенирования геномов, и это привело к осознанию того факта, что HGT сыграл большую роль в эволюции не только бактерий, но и одноклеточных эукариот, растений и животных. События HGT, включая древний перено с генов между тремя доменами жизни (археями, бактериями и эукариотами), рассматриваются сейчас, как важная движущая сила эволюции эукариотического генома (Prasad et al. 2021;Undheim, Jenner 2021). Перенос симбиотических генов из митохондрии или пластид в ядро значительно повлиял на формирование геномов эукариот . ...
... События HGT были описаны и для других ядовитых видов, например, генов латротоксинов пауков (Drukewitz, Reumont 2019). Геномный анализ многоножек обнаружил доказательства причастности HGT к эволюционному происхожден ию яда в линии животных, который может обеспечить «ускоренный канал для эволюции новшества за счет превращения бактериального оружия в яды животных» (Undheim, Jenner 2021). ...
Phylogenomics covers various areas of research at the intersection of molecular and evolutionary biology, and in a broad sense can be considered as the science of the reconstruction of life on Earth. This paper provides a brief overview of the achievements of phylogenomics, including historical background, research approaches and methods, and specifi c examples, focusing on molecular phylogenies (for diff erent taxonomic levels, from the global tree of eukaryotes to a single family or genus), evolutionary adaptation of species (for example, to life on land, to a predatory, daytime and nocturnal lifestyle), origin and evolution of innovations (such as arachnoid spheres, stomata, acoustic communications), and also horizontal gene transfer in animals and plants.
... To explore the evolutionary origin of Xt3a, we used blastp (blast+ v.2.10.1 + ) 64 to search both the full-length and single domains against a database of all 228,896 mRNA sequences listed under Remipedia in NCBI and translated to all potential open reading frames encoding 40 amino acids or more (880,562 sequences). We also searched the trinity-assembled venom gland and whole-body transcriptomes reported by von Reumont et al. 17 , the arthropod component of a custom database containing trinity-assembled transcriptomic datasets from 125 species of arthropods obtained from the NCBI SRA reported previously 65,66 , as well as the NCBI nr and UniProtKB databases. We used standard blastp settings and retained all sequence hits containing at least one putative ICK domain, identified as containing either of the canonical cysteine patterns corresponding to either of the three-or four-disulfide ICK forms (3-DS and 4-DS, respectively). ...
Multivalent ligands of ion channels have proven to be both very rare and highly valuable in yielding unique insights into channel structure and pharmacology. Here, we describe a bivalent peptide from the venom of Xibalbanus tulumensis, a troglobitic arthropod from the enigmatic class Remipedia, that causes persistent calcium release by activation of ion channels involved in muscle contraction. The high-resolution solution structure of φ-Xibalbin3-Xt3a reveals a tandem repeat arrangement of inhibitor-cysteine knot (ICK) domains previously only found in spider venoms. The individual repeats of Xt3a share sequence similarity with a family of scorpion toxins that target ryanodine receptors (RyR). Single-channel electrophysiology and quantification of released Ca²⁺ stores within skinned muscle fibers confirm Xt3a as a bivalent RyR modulator. Our results reveal convergent evolution of RyR targeting toxins in remipede and scorpion venoms, while the tandem-ICK repeat architecture is an evolutionary innovation that is convergent with toxins from spider venoms.
... Venoms of scolopendromorphs are particularly complex and quite different between closely related species and even among conspecific individuals (Ward and Rokita, 2018). Eventually (Undheim and Jenner, 2021) it has been discovered that centipedes are the only known animals using, in predation and defence, venoms that contain multiple gene families derived from horizontal gene transfer: their venoms include at least five gene families recruited from bacterial and fungal donors, involving at least eight horizontal gene transfer events. ...
... In some unicellular eukaryotes, about 1% of predicted genes were acquired laterally, with most of them being bacterial in origin (Fan et al., 2020;Matriano et al., 2021). In multicellular organisms, there are unequivocal examples in animals (Bryon et al., 2017;Undheim & Jenner, 2021), fungi (Duarte & Huynen, 2019;Murphy et al., 2019;Szöll} osi et al., 2015), and plants (Wickell & Li, 2020). Among plants, LGT seems especially prevalent between parasites and their hosts, where direct tissue contact via the feeding structures known as haustoria facilitate genetic movements (Vogel et al., 2018;Xi et al., 2012;Yang et al., 2019;Yoshida et al., 2019). ...
Societal Impact Statement
Lateral gene transfer (LGT) refers to the transmission of genetic material without sexual reproduction. LGT is widespread in a number of plant species, including grasses. But how these genes of foreign origin got there is presently unknown. In this review, we show that transformation techniques used to genetically modify organisms could occur in the wild and be responsible for the frequently observed grass‐to‐grass LGTs. The distinction between natural evolutionary processes and genetic engineering might be arbitrary, and its validity will be further debated as agricultural biotechnology becomes more widely used and examples of “natural genetic engineering” through LGT increase.
Summary
Lateral gene transfer (LGT) is the transmission of genetic material among species without sexual reproduction. LGT was initially thought to be restricted to prokaryotes, but it has since been reported in a wide range of eukaryotes, including plants. Grasses seem to be particularly prone to LGT and frequently exchange genes among species. However, the mechanism(s) facilitating these transfers in this economically and ecologically important group of plants are debated. Here, we review vector‐mediated, direct tissue‐to‐tissue contact, wide‐crossing and reproductive contamination LGT mechanisms and discuss the likelihood of each in light of recent studies. Of particular relevance are transformation approaches that require minimal human intervention to transfer DNA among grasses in the lab that could mimic the mechanisms facilitating grass‐to‐grass LGT in the wild. These approaches include relatively simple techniques, such as pollen tube pathway‐mediated transformation, that take advantage of the permeability of the reproductive process to introduce alien genetic material from a third individual into an embryo. This process could be easily mirrored in the wild where pollen from one species lands on the stigma of another, acting as a source of alien DNA that can ultimately contaminate the reproductive process. This contamination is likely to be prevalent in wind pollinated species such as grasses, where the rates of illegitimate pollination will be high. In conclusion, plant transformation methods requiring minimal intervention are likely paralleled in the wild where they act as the mechanism underpinning LGT between distantly related grass species.
... Other potential pain-causing venom peptides are b-poreforming toxins, which are abundant in centipede venoms. 59,125,126 They belong to the bacterial aerolysin-like b-pore-forming toxin superfamily and form polymeric pore structures in cell membranes. 70 b-Pore-forming toxins in centipedes may thus induce pain by disrupting neuronal membranes. ...
