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Yehu Moran - One of the best experts on this subject based on the ideXlab platform.
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Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom.
Proceedings of the National Academy of Sciences of the United States of America, 2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Morani Landau, Jason Macrander, Shir A. Singer, Yehu MoranAbstract:The sea anemone Nematostella vectensis (Anthozoa, Cnidaria) is a powerful model for characterizing the evolution of genes functioning in venom and nervous systems. Although venom has evolved independently numerous times in animals, the evolutionary origin of many toxins remains unknown. In this work, we pinpoint an ancestral gene giving rise to a new toxin and functionally characterize both genes in the same species. Thus, we report a case of protein recruitment from the Cnidarian nervous to venom system. The ShK-like1 peptide has a ShKT cysteine motif, is lethal for fish larvae and packaged into nematocysts, the Cnidarian venom-producing stinging capsules. Thus, ShK-like1 is a toxic venom component. Its paralog, ShK-like2, is a neuropeptide localized to neurons and is involved in development. Both peptides exhibit similarities in their functional activities: They provoke contraction in Nematostella polyps and are toxic to fish. Because ShK-like2 but not ShK-like1 is conserved throughout sea anemone phylogeny, we conclude that the two paralogs originated due to a Nematostella-specific duplication of a ShK-like2 ancestor, a neuropeptide-encoding gene, followed by diversification and partial functional specialization. ShK-like2 is represented by two gene isoforms controlled by alternative promoters conferring regulatory flexibility throughout development. Additionally, we characterized the expression patterns of four other peptides with structural similarities to studied venom components and revealed their unexpected neuronal localization. Thus, we employed genomics, transcriptomics, and functional approaches to reveal one venom component, five neuropeptides with two different cysteine motifs, and an evolutionary pathway from nervous to venom system in Cnidaria.
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some like it hot population specific adaptations in venom production to abiotic stressors in a widely distributed Cnidarian
BMC Biology, 2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Jason Macrander, Reuven Aharoni, Shelcie S Menardharvey, Amy Klock, Whitney B Leach, Yehu MoranAbstract:In Cnidarians, antagonistic interactions with predators and prey are mediated by their venom, whose synthesis may be metabolically expensive. The potentially high cost of venom production has been hypothesized to drive population-specific variation in venom expression due to differences in abiotic conditions. However, the effects of environmental factors on venom production have been rarely demonstrated in animals. Here, we explore the impact of specific abiotic stresses on venom production of distinct populations of the sea anemone Nematostella vectensis (Actiniaria, Cnidaria) inhabiting estuaries over a broad geographic range where environmental conditions such as temperatures and salinity vary widely. We challenged Nematostella polyps with heat, salinity, UV light stressors, and a combination of all three factors to determine how abiotic stressors impact toxin expression for individuals collected across this species’ range. Transcriptomics and proteomics revealed that the highly abundant toxin Nv1 was the most downregulated gene under heat stress conditions in multiple populations. Physiological measurements demonstrated that venom is metabolically costly to produce. Strikingly, under a range of abiotic stressors, individuals from different geographic locations along this latitudinal cline modulate differently their venom production levels. We demonstrate that abiotic stress results in venom regulation in Nematostella. Together with anecdotal observations from other Cnidarian species, our results suggest this might be a universal phenomenon in Cnidaria. The decrease in venom production under stress conditions across species coupled with the evidence for its high metabolic cost in Nematostella suggests downregulation of venom production under certain conditions may be highly advantageous and adaptive. Furthermore, our results point towards local adaptation of this mechanism in Nematostella populations along a latitudinal cline, possibly resulting from distinct genetics and significant environmental differences between their habitats.
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Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom
2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Morani Landau, Jason Macrander, Shir A. Singer, Yehu MoranAbstract:Abstract The sea anemone Nematostella vectensis (Anthozoa, Cnidaria) is a powerful model system for characterizing the evolution of genes functioning in venom and nervous systems. Despite being an example for evolutionary novelty, the evolutionary origin of most toxins remains unknown. Here we report the first bona fide case of protein recruitment from the Cnidarian nervous to venom system. The ShK-like1 peptide has ShKT cysteine motif, is lethal for fish larvae and packaged into nematocysts, the Cnidarian venom-producing stinging capsules. Thus, ShK-like1 is a toxic venom component. Its paralog, ShK-like2, is a neuropeptide localized to neurons and is involved in development. Interestingly, both peptides exhibit similarities in their functional activities: both of them provoke contraction in Nematostella polyps and are toxic to fish. Because ShK-like2 but not ShK-like1 is conserved throughout sea anemone phylogeny, we conclude that the two paralogs originated due to a Nematostella-specific duplication of a ShK-like2 ancestor, a neuropeptide-encoding gene, followed by diversification and partial functional specialization. Strikingly, ShK-like2 is represented by two gene isoforms controlled by alternative promoters conferring regulatory flexibility throughout development. Additionally, we characterized the expression patterns of four other peptides with structural similarities to studied venom components, and revealed their unexpected neuronal localization. Thus, we employed genomics, transcriptomics and functional approaches to reveal one new venom component, five neuropeptides with two different cysteine motifs and an evolutionary pathway from nervous to venom system in Cnidaria.
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evolution of an ancient venom recognition of a novel family of Cnidarian toxins and the common evolutionary origin of sodium and potassium neurotoxins in sea anemone
Molecular Biology and Evolution, 2015Co-Authors: Mahdokht Jouiaei, Kartik Sunagar, Aya Federman Gross, Holger Scheib, Paul F Alewood, Yehu MoranAbstract:Despite Cnidaria (sea anemones, corals, jellyfish, and hydroids) being the oldest venomous animal lineage, structure-function relationships, phyletic distributions, and the molecular evolutionary regimes of toxins encoded by these intriguing animals are poorly understood. Hence, we have comprehensively elucidated the phylogenetic and molecular evolutionary histories of pharmacologically characterized Cnidarian toxin families, including peptide neurotoxins (voltage-gated Na+ and K+ channel-targeting toxins: NaTxs and KTxs, respectively), pore-forming toxins (actinoporins, aerolysin-related toxins, and jellyfish toxins), and the newly discovered small cysteine-rich peptides (SCRiPs). We show that despite long evolutionary histories, most Cnidarian toxins remain conserved under the strong influence of negative selection - a finding that is in striking contrast to the rapid evolution of toxin families in evolutionarily younger lineages, such as cone snails and advanced snakes. In contrast to the previous suggestions that implicated SCRiPs in the biomineralization process in corals, we demonstrate that they are potent neurotoxins that are likely involved in the envenoming function, and thus represent the first family of neurotoxins from corals. We also demonstrate the common evolutionary origin of type III KTxs and NaTxs in sea anemones. We show that type III KTxs have evolved from NaTxs under the regime of positive selection, and likely represent a unique evolutionary innovation of the Actinioidea lineage. We report a correlation between the accumulation of episodically adaptive sites and the emergence of novel pharmacological activities in this rapidly evolving neurotoxic clade.
Adam M Reitzel - One of the best experts on this subject based on the ideXlab platform.
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Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom.
Proceedings of the National Academy of Sciences of the United States of America, 2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Morani Landau, Jason Macrander, Shir A. Singer, Yehu MoranAbstract:The sea anemone Nematostella vectensis (Anthozoa, Cnidaria) is a powerful model for characterizing the evolution of genes functioning in venom and nervous systems. Although venom has evolved independently numerous times in animals, the evolutionary origin of many toxins remains unknown. In this work, we pinpoint an ancestral gene giving rise to a new toxin and functionally characterize both genes in the same species. Thus, we report a case of protein recruitment from the Cnidarian nervous to venom system. The ShK-like1 peptide has a ShKT cysteine motif, is lethal for fish larvae and packaged into nematocysts, the Cnidarian venom-producing stinging capsules. Thus, ShK-like1 is a toxic venom component. Its paralog, ShK-like2, is a neuropeptide localized to neurons and is involved in development. Both peptides exhibit similarities in their functional activities: They provoke contraction in Nematostella polyps and are toxic to fish. Because ShK-like2 but not ShK-like1 is conserved throughout sea anemone phylogeny, we conclude that the two paralogs originated due to a Nematostella-specific duplication of a ShK-like2 ancestor, a neuropeptide-encoding gene, followed by diversification and partial functional specialization. ShK-like2 is represented by two gene isoforms controlled by alternative promoters conferring regulatory flexibility throughout development. Additionally, we characterized the expression patterns of four other peptides with structural similarities to studied venom components and revealed their unexpected neuronal localization. Thus, we employed genomics, transcriptomics, and functional approaches to reveal one venom component, five neuropeptides with two different cysteine motifs, and an evolutionary pathway from nervous to venom system in Cnidaria.
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some like it hot population specific adaptations in venom production to abiotic stressors in a widely distributed Cnidarian
BMC Biology, 2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Jason Macrander, Reuven Aharoni, Shelcie S Menardharvey, Amy Klock, Whitney B Leach, Yehu MoranAbstract:In Cnidarians, antagonistic interactions with predators and prey are mediated by their venom, whose synthesis may be metabolically expensive. The potentially high cost of venom production has been hypothesized to drive population-specific variation in venom expression due to differences in abiotic conditions. However, the effects of environmental factors on venom production have been rarely demonstrated in animals. Here, we explore the impact of specific abiotic stresses on venom production of distinct populations of the sea anemone Nematostella vectensis (Actiniaria, Cnidaria) inhabiting estuaries over a broad geographic range where environmental conditions such as temperatures and salinity vary widely. We challenged Nematostella polyps with heat, salinity, UV light stressors, and a combination of all three factors to determine how abiotic stressors impact toxin expression for individuals collected across this species’ range. Transcriptomics and proteomics revealed that the highly abundant toxin Nv1 was the most downregulated gene under heat stress conditions in multiple populations. Physiological measurements demonstrated that venom is metabolically costly to produce. Strikingly, under a range of abiotic stressors, individuals from different geographic locations along this latitudinal cline modulate differently their venom production levels. We demonstrate that abiotic stress results in venom regulation in Nematostella. Together with anecdotal observations from other Cnidarian species, our results suggest this might be a universal phenomenon in Cnidaria. The decrease in venom production under stress conditions across species coupled with the evidence for its high metabolic cost in Nematostella suggests downregulation of venom production under certain conditions may be highly advantageous and adaptive. Furthermore, our results point towards local adaptation of this mechanism in Nematostella populations along a latitudinal cline, possibly resulting from distinct genetics and significant environmental differences between their habitats.
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Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom
2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Morani Landau, Jason Macrander, Shir A. Singer, Yehu MoranAbstract:Abstract The sea anemone Nematostella vectensis (Anthozoa, Cnidaria) is a powerful model system for characterizing the evolution of genes functioning in venom and nervous systems. Despite being an example for evolutionary novelty, the evolutionary origin of most toxins remains unknown. Here we report the first bona fide case of protein recruitment from the Cnidarian nervous to venom system. The ShK-like1 peptide has ShKT cysteine motif, is lethal for fish larvae and packaged into nematocysts, the Cnidarian venom-producing stinging capsules. Thus, ShK-like1 is a toxic venom component. Its paralog, ShK-like2, is a neuropeptide localized to neurons and is involved in development. Interestingly, both peptides exhibit similarities in their functional activities: both of them provoke contraction in Nematostella polyps and are toxic to fish. Because ShK-like2 but not ShK-like1 is conserved throughout sea anemone phylogeny, we conclude that the two paralogs originated due to a Nematostella-specific duplication of a ShK-like2 ancestor, a neuropeptide-encoding gene, followed by diversification and partial functional specialization. Strikingly, ShK-like2 is represented by two gene isoforms controlled by alternative promoters conferring regulatory flexibility throughout development. Additionally, we characterized the expression patterns of four other peptides with structural similarities to studied venom components, and revealed their unexpected neuronal localization. Thus, we employed genomics, transcriptomics and functional approaches to reveal one new venom component, five neuropeptides with two different cysteine motifs and an evolutionary pathway from nervous to venom system in Cnidaria.
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linear mitochondrial genome in anthozoa Cnidaria a case study in ceriantharia
Scientific Reports, 2019Co-Authors: Sérgio N. Stampar, Adam M Reitzel, Jason Macrander, Michael Broe, Mercer R Brugler, Marymegan DalyAbstract:Sequences and structural attributes of mitochondrial genomes have played a critical role in the clarification of relationships among Cnidaria, a key phylum of early-diverging animals. Among the major lineages of Cnidaria, Ceriantharia (“tube anemones”) remains one of the most enigmatic in terms of its phylogenetic position. We sequenced the mitochondrial genomes of two ceriantharians to see whether the complete organellar genome would provide more support for the phylogenetic placement of Ceriantharia. For both Isarachnanthus nocturnus and Pachycerianthus magnus, the mitochondrial gene sequences could not be assembled into a single circular genome. Instead, our analyses suggest that both species have mitochondrial genomes consisting of multiple linear fragments. Linear mitogenomes are characteristic of members of Medusozoa, one of the major lineages of Cnidaria, but are unreported for Anthozoa, which includes the Ceriantharia. The inferred number of fragments and variation in gene order between species is much greater within Ceriantharia than among the lineages of Medusozoa. We identify origins of replication for each of the five putative chromosomes of the Isarachnanthus nocturnus mitogenome and for each of the eight putative chromosomes of the Pachycerianthus magnus mitogenome. At 80,923 bp, I. nocturnus now holds the record for the largest animal mitochondrial genome reported to date. The novelty of the mitogenomic structure in Ceriantharia highlights the distinctiveness of this lineage but, because it appears to be both unique to and diverse within Ceriantharia, it is uninformative about the phylogenetic position of Ceriantharia relative to other Anthozoa. The presence of tRNAMet and tRNATrp in both ceriantharian mitogenomes supports a closer relationship between Ceriantharia and Hexacorallia than between Ceriantharia and any other Cnidarian lineage, but phylogenetic analysis of the genes contained in the mitogenomes suggests that Ceriantharia is sister to a clade containing Octocorallia + Hexacorallia indicating a possible suppression of tRNATrp in Octocorallia.
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leidyi: a new view of ctenophore photocytes
2016Co-Authors: Genomic Organization, Christine E Schnitzler, Adam M Reitzel, Joseph F Ryan, David Simmons, Meghan L. Powers, Takashi Tada, Morgan Park, Jyoti GuptaAbstract:Background: Calcium-activated photoproteins are luciferase variants found in photocyte cells of bioluminescent jellyfish (Phylum Cnidaria) and comb jellies (Phylum Ctenophora). The complete genomic sequence from the ctenophore Mnemiopsis leidyi, a representative of the earliest branch of animals that emit light, provided an opportunity to examine the genome of an organism that uses this class of luciferase for bioluminescence and to look for genes involved in light reception. To determine when photoprotein genes first arose, we examined the genomic sequence from other early-branching taxa. We combined our genomic survey with gene trees, developmental expression patterns, and functional protein assays of photoproteins and opsins to provide a comprehensive view of light production and light reception in Mnemiopsis. Results: The Mnemiopsis genome has 10 full-length photoprotein genes situated within two genomic clusters with high sequence conservation that are maintained due to strong purifying selection and concerted evolution. Photoprotein-like genes were also identified in the genomes of the non-luminescent sponge Amphimedon queenslandica and the non-luminescent Cnidarian Nematostella vectensis, and phylogenomic analysis demonstrated that photoprotein genes arose at the base of all animals. Photoprotein gene expression in Mnemiopsis embryos begins during gastrulation in migrating precursors to photocytes and persists throughout development in th
John R Finnerty - One of the best experts on this subject based on the ideXlab platform.
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Pre-Bilaterian Origins of the Hox Cluster and the Hox Code: Evidence from the Sea Anemone, Nematostella vectensis
2013Co-Authors: Joseph F Ryan, Maureen E Mazza, Andreas D. Baxevanis, Kevin Pang, Mark Q. Martindale, David Q. Matus, John R FinnertyAbstract:Background. Hox genes were critical to many morphological innovations of bilaterian animals. However, early Hox evolution remains obscure. Phylogenetic, developmental, and genomic analyses on the Cnidarian sea anemone Nematostella vectensis challenge recent claims that the Hox code is a bilaterian invention and that no ‘‘true’ ’ Hox genes exist in the phylum Cnidaria. Methodology/Principal Findings. Phylogenetic analyses of 18 Hox-related genes from Nematostella identify putative Hox1, Hox2, and Hox9+ genes. Statistical comparisons among competing hypotheses bolster these findings, including an explicit consideration of the gene losses implied by alternate topologies. In situ hybridization studies of 20 Hox-related genes reveal that multiple Hox genes are expressed in distinct regions along the primary body axis, supporting the existence of a prebilaterian Hox code. Additionally, several Hox genes are expressed in nested domains along the secondary body axis, suggesting a role in ‘‘dorsoventral’ ’ patterning. Conclusions/Significance. A cluster of anterior and posterior Hox genes, as well as ParaHox cluster of genes evolved prior to the Cnidarian-bilaterian split. There is evidence to suggest that these clusters were formed from a series of tandem gene duplication events and played a role in patterning both the primary and secondary body axes in a bilaterally symmetrical common ancestor. Cnidarians and bilaterians shared a common ancestor some 570 to 700 million years ago, and as such, are derived from a common body plan. Our work reveals several conserved genetic components that are found in both of these diverse lineages. This finding is consistent with the hypothesis that a set o
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Figure 7
2013Co-Authors: Joseph F Ryan, Maureen E Mazza, Andreas D. Baxevanis, John R FinnertyAbstract:Hox/ParaHox evolutionary scenarios. The phylogenies drawn here depict six mutually exclusive scenarios regarding the evolution of the Hox and ParaHox genes. Ten distinct Hox and ParaHox lineages are thought to have been present in the ancestral bilaterian (Hox1, Hox2, Hox3, Hox4, Hox5, Hox6–8, Hox9+, Cdx, Gsx, and Xlox). Five distinct Hox/ParaHox lineages are recognized for Nematostella. (Nematostella homeodomains that tend to cluster together in the phylogenetic analyses are grouped together here: anthox1/1a; anthox2/9; anthox6/6a; anthox7/8a/8b.) Assuming no gene loss in the Cnidaria, then the existence of five Hox/ParaHox lineages in Nematostella implies that the Cnidarian-bilaterian ancestor (CBA) could have possessed as few as one Hox/ParaHox gene (scenario A) or as many as five (scenario E). There is some indication that a central class Hox gene was lost in the Cnidaria [47], and that the CBA may have possessed six distinct Hox/ParaHox genes (scenario F). The ancestral Hox/ParaHox genes present in the CBA are indicated by solid squares. If a particular hypothetical clade is recovered on one or more of the phylogenetic analyses presented here, this is indicated above the relevant branch (NJ = neighbor-joining, Figure 2; Ba = Bayesian inference, Figure S1; ML = maximum- likelihood, Figure S2; φ = none). Below each branch, the average statistical support is indicated (NJ-bootstrap proportion+Bayes-posterior probability+ML-boostrap proportion/3). Each scenario implies a different number of lineage-specific gene losses.
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rising starlet the starlet sea anemone nematostella vectensis
BioEssays, 2005Co-Authors: John A Darling, Adam R Reitzel, Patrick M Burton, Maureen E Mazza, Joseph F Ryan, James C Sullivan, John R FinnertyAbstract:In recent years, a handful of model systems from the basal metazoan phylum Cnidaria have emerged to challenge long-held views on the evolution of animal complexity. The most-recent, and in many ways most-promising addition to this group is the starlet sea anemone, Nematostella vectensis. The remarkable amenability of this species to laboratory manipulation has already made it a productive system for exploring Cnidarian development, and a proliferation of molecular and genomic tools, including the currently ongoing Nematostella genome project, further enhances the promise of this species. In addition, the facility with which Nematostella populations can be investigated within their natural ecological context suggests that this model may be profitably expanded to address important questions in molecular and evolutionary ecology. In this review, we explore the traits that make Nematostella exceptionally attractive as a model organism, summarize recent research demonstrating the utility of Nematostella in several different contexts, and highlight a number of developments likely to further increase that utility in the near future.
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The origins of axial patterning in the metazoa: how old is bilateral symmetry?
The International Journal of Developmental Biology, 2003Co-Authors: John R FinnertyAbstract:Bilateral symmetry is a hallmark of the Bilateria. It is achieved by the intersection of two orthogonal axes of polarity: the anterior-posterior (A-P) axis and the dorsal-ventral (D-V) axis. It is widely thought that bilateral symmetry evolved in the common ancestor of the Bilateria. However, it has long been known that members of the phylum Cnidaria, an outgroup to the Bilateria, also exhibit bilateral symmetry. Recent studies have examined the developmental expression of axial patterning genes in members of the phylum Cnidaria. Hox genes play a conserved role in patterning the A-P axis of bilaterians. Hox genes are expressed in staggered axial domains along the oral-aboral axis of Cnidarians, suggesting that Hox patterning of the primary body axis was already present in the Cnidarian-bilaterian ancestor. Dpp plays a conserved role patterning the D-V axis of bilaterians. Asymmetric expression of dpp about the directive axis of Cnidarians implies that this patterning system is similarly ancient. Taken together, these result imply that bilateral symmetry had already evolved before the Cnidaria diverged from the Bilateria.
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Early evolution of a homeobox gene: the parahox gene Gsx in the Cnidaria and the Bilateria
Evolution & development, 2003Co-Authors: John R Finnerty, David A. Paulson, Pat Burton, Kevin Pang, Mark Q. MartindaleAbstract:Summary Homeobox transcription factors are commonly involved in developmental regulation in diverse eukaryotes, including plants, animals, and fungi. The origin of novel homeobox genes is thought to have contributed to many evolutionary innovations in animals. We perform a molecular phylogenetic analysis of cnox2, the best studied homeobox gene from the phylum Cnidaria, a very ancient lineage of animals. Among three competing hypotheses, our analysis decisively favors the hypothesis that cnox2 is orthologous to the gsx gene of Bilateria, thereby establishing the existence of this specific homeobox gene in the eumetazoan stem lineage, some 650–900 million years ago. We assayed the expression of gsx in the planula larva and polyp of the sea anemone Nematostella vectensis using in situ hybridization and reverse transcriptase polymerase chain reaction. The gsx ortholog of Nematostella, known as anthox2, is expressed at high levels in the posterior planula and the corresponding “head” region of the polyp. It cannot be detected in the anterior planula or the corresponding “foot” region of the polyp. We have attempted to reconstruct the evolution of gsx spatiotemporal expression in Cnidarians and bilaterians using a phylogenetic framework. Because of the surprisingly high degree of variability in gsx expression within the Cnidaria, it is currently not possible to infer unambiguously the ancestral Cnidarian condition or the ancestral eumetazoan condition for gsx expression.
Joachim M Surm - One of the best experts on this subject based on the ideXlab platform.
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Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom.
Proceedings of the National Academy of Sciences of the United States of America, 2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Morani Landau, Jason Macrander, Shir A. Singer, Yehu MoranAbstract:The sea anemone Nematostella vectensis (Anthozoa, Cnidaria) is a powerful model for characterizing the evolution of genes functioning in venom and nervous systems. Although venom has evolved independently numerous times in animals, the evolutionary origin of many toxins remains unknown. In this work, we pinpoint an ancestral gene giving rise to a new toxin and functionally characterize both genes in the same species. Thus, we report a case of protein recruitment from the Cnidarian nervous to venom system. The ShK-like1 peptide has a ShKT cysteine motif, is lethal for fish larvae and packaged into nematocysts, the Cnidarian venom-producing stinging capsules. Thus, ShK-like1 is a toxic venom component. Its paralog, ShK-like2, is a neuropeptide localized to neurons and is involved in development. Both peptides exhibit similarities in their functional activities: They provoke contraction in Nematostella polyps and are toxic to fish. Because ShK-like2 but not ShK-like1 is conserved throughout sea anemone phylogeny, we conclude that the two paralogs originated due to a Nematostella-specific duplication of a ShK-like2 ancestor, a neuropeptide-encoding gene, followed by diversification and partial functional specialization. ShK-like2 is represented by two gene isoforms controlled by alternative promoters conferring regulatory flexibility throughout development. Additionally, we characterized the expression patterns of four other peptides with structural similarities to studied venom components and revealed their unexpected neuronal localization. Thus, we employed genomics, transcriptomics, and functional approaches to reveal one venom component, five neuropeptides with two different cysteine motifs, and an evolutionary pathway from nervous to venom system in Cnidaria.
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some like it hot population specific adaptations in venom production to abiotic stressors in a widely distributed Cnidarian
BMC Biology, 2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Jason Macrander, Reuven Aharoni, Shelcie S Menardharvey, Amy Klock, Whitney B Leach, Yehu MoranAbstract:In Cnidarians, antagonistic interactions with predators and prey are mediated by their venom, whose synthesis may be metabolically expensive. The potentially high cost of venom production has been hypothesized to drive population-specific variation in venom expression due to differences in abiotic conditions. However, the effects of environmental factors on venom production have been rarely demonstrated in animals. Here, we explore the impact of specific abiotic stresses on venom production of distinct populations of the sea anemone Nematostella vectensis (Actiniaria, Cnidaria) inhabiting estuaries over a broad geographic range where environmental conditions such as temperatures and salinity vary widely. We challenged Nematostella polyps with heat, salinity, UV light stressors, and a combination of all three factors to determine how abiotic stressors impact toxin expression for individuals collected across this species’ range. Transcriptomics and proteomics revealed that the highly abundant toxin Nv1 was the most downregulated gene under heat stress conditions in multiple populations. Physiological measurements demonstrated that venom is metabolically costly to produce. Strikingly, under a range of abiotic stressors, individuals from different geographic locations along this latitudinal cline modulate differently their venom production levels. We demonstrate that abiotic stress results in venom regulation in Nematostella. Together with anecdotal observations from other Cnidarian species, our results suggest this might be a universal phenomenon in Cnidaria. The decrease in venom production under stress conditions across species coupled with the evidence for its high metabolic cost in Nematostella suggests downregulation of venom production under certain conditions may be highly advantageous and adaptive. Furthermore, our results point towards local adaptation of this mechanism in Nematostella populations along a latitudinal cline, possibly resulting from distinct genetics and significant environmental differences between their habitats.
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Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom
2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Morani Landau, Jason Macrander, Shir A. Singer, Yehu MoranAbstract:Abstract The sea anemone Nematostella vectensis (Anthozoa, Cnidaria) is a powerful model system for characterizing the evolution of genes functioning in venom and nervous systems. Despite being an example for evolutionary novelty, the evolutionary origin of most toxins remains unknown. Here we report the first bona fide case of protein recruitment from the Cnidarian nervous to venom system. The ShK-like1 peptide has ShKT cysteine motif, is lethal for fish larvae and packaged into nematocysts, the Cnidarian venom-producing stinging capsules. Thus, ShK-like1 is a toxic venom component. Its paralog, ShK-like2, is a neuropeptide localized to neurons and is involved in development. Interestingly, both peptides exhibit similarities in their functional activities: both of them provoke contraction in Nematostella polyps and are toxic to fish. Because ShK-like2 but not ShK-like1 is conserved throughout sea anemone phylogeny, we conclude that the two paralogs originated due to a Nematostella-specific duplication of a ShK-like2 ancestor, a neuropeptide-encoding gene, followed by diversification and partial functional specialization. Strikingly, ShK-like2 is represented by two gene isoforms controlled by alternative promoters conferring regulatory flexibility throughout development. Additionally, we characterized the expression patterns of four other peptides with structural similarities to studied venom components, and revealed their unexpected neuronal localization. Thus, we employed genomics, transcriptomics and functional approaches to reveal one new venom component, five neuropeptides with two different cysteine motifs and an evolutionary pathway from nervous to venom system in Cnidaria.
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evidence for a large expansion and subfunctionalization of globin genes in sea anemones
Genome Biology and Evolution, 2018Co-Authors: Hayden L Smith, Joachim M Surm, Ana Pavasovic, Matthew J Phillips, Peter J PrentisAbstract:The globin gene superfamily has been well-characterized in vertebrates, however, there has been limited research in early-diverging lineages, such as phylum Cnidaria. This study aimed to identify globin genes in multiple Cnidarian lineages, and use bioinformatic approaches to characterize the evolution, structure, and expression of these genes. Phylogenetic analyses and in silico protein predictions showed that all Cnidarians have undergone an expansion of globin genes, which likely have a hexacoordinate protein structure. Our protein modeling has also revealed the possibility of a single pentacoordinate globin lineage in anthozoan species. Some Cnidarian globin genes displayed tissue and development specific expression with very few orthologous genes similarly expressed across species. Our phylogenetic analyses also revealed that eumetazoan globin genes form a polyphyletic relationship with vertebrate globin genes. Overall, our analyses suggest that a Ngb-like and GbX-like gene were most likely present in the globin gene repertoire for the last common ancestor of eumetazoans. The identification of a large-scale expansion and subfunctionalization of globin genes in actiniarians provides an excellent starting point to further our understanding of the evolution and function of the globin gene superfamily in early-diverging lineages.
Maria Y. Sachkova - One of the best experts on this subject based on the ideXlab platform.
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Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom.
Proceedings of the National Academy of Sciences of the United States of America, 2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Morani Landau, Jason Macrander, Shir A. Singer, Yehu MoranAbstract:The sea anemone Nematostella vectensis (Anthozoa, Cnidaria) is a powerful model for characterizing the evolution of genes functioning in venom and nervous systems. Although venom has evolved independently numerous times in animals, the evolutionary origin of many toxins remains unknown. In this work, we pinpoint an ancestral gene giving rise to a new toxin and functionally characterize both genes in the same species. Thus, we report a case of protein recruitment from the Cnidarian nervous to venom system. The ShK-like1 peptide has a ShKT cysteine motif, is lethal for fish larvae and packaged into nematocysts, the Cnidarian venom-producing stinging capsules. Thus, ShK-like1 is a toxic venom component. Its paralog, ShK-like2, is a neuropeptide localized to neurons and is involved in development. Both peptides exhibit similarities in their functional activities: They provoke contraction in Nematostella polyps and are toxic to fish. Because ShK-like2 but not ShK-like1 is conserved throughout sea anemone phylogeny, we conclude that the two paralogs originated due to a Nematostella-specific duplication of a ShK-like2 ancestor, a neuropeptide-encoding gene, followed by diversification and partial functional specialization. ShK-like2 is represented by two gene isoforms controlled by alternative promoters conferring regulatory flexibility throughout development. Additionally, we characterized the expression patterns of four other peptides with structural similarities to studied venom components and revealed their unexpected neuronal localization. Thus, we employed genomics, transcriptomics, and functional approaches to reveal one venom component, five neuropeptides with two different cysteine motifs, and an evolutionary pathway from nervous to venom system in Cnidaria.
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some like it hot population specific adaptations in venom production to abiotic stressors in a widely distributed Cnidarian
BMC Biology, 2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Jason Macrander, Reuven Aharoni, Shelcie S Menardharvey, Amy Klock, Whitney B Leach, Yehu MoranAbstract:In Cnidarians, antagonistic interactions with predators and prey are mediated by their venom, whose synthesis may be metabolically expensive. The potentially high cost of venom production has been hypothesized to drive population-specific variation in venom expression due to differences in abiotic conditions. However, the effects of environmental factors on venom production have been rarely demonstrated in animals. Here, we explore the impact of specific abiotic stresses on venom production of distinct populations of the sea anemone Nematostella vectensis (Actiniaria, Cnidaria) inhabiting estuaries over a broad geographic range where environmental conditions such as temperatures and salinity vary widely. We challenged Nematostella polyps with heat, salinity, UV light stressors, and a combination of all three factors to determine how abiotic stressors impact toxin expression for individuals collected across this species’ range. Transcriptomics and proteomics revealed that the highly abundant toxin Nv1 was the most downregulated gene under heat stress conditions in multiple populations. Physiological measurements demonstrated that venom is metabolically costly to produce. Strikingly, under a range of abiotic stressors, individuals from different geographic locations along this latitudinal cline modulate differently their venom production levels. We demonstrate that abiotic stress results in venom regulation in Nematostella. Together with anecdotal observations from other Cnidarian species, our results suggest this might be a universal phenomenon in Cnidaria. The decrease in venom production under stress conditions across species coupled with the evidence for its high metabolic cost in Nematostella suggests downregulation of venom production under certain conditions may be highly advantageous and adaptive. Furthermore, our results point towards local adaptation of this mechanism in Nematostella populations along a latitudinal cline, possibly resulting from distinct genetics and significant environmental differences between their habitats.
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Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom
2020Co-Authors: Maria Y. Sachkova, Joachim M Surm, Adam M Reitzel, Morani Landau, Jason Macrander, Shir A. Singer, Yehu MoranAbstract:Abstract The sea anemone Nematostella vectensis (Anthozoa, Cnidaria) is a powerful model system for characterizing the evolution of genes functioning in venom and nervous systems. Despite being an example for evolutionary novelty, the evolutionary origin of most toxins remains unknown. Here we report the first bona fide case of protein recruitment from the Cnidarian nervous to venom system. The ShK-like1 peptide has ShKT cysteine motif, is lethal for fish larvae and packaged into nematocysts, the Cnidarian venom-producing stinging capsules. Thus, ShK-like1 is a toxic venom component. Its paralog, ShK-like2, is a neuropeptide localized to neurons and is involved in development. Interestingly, both peptides exhibit similarities in their functional activities: both of them provoke contraction in Nematostella polyps and are toxic to fish. Because ShK-like2 but not ShK-like1 is conserved throughout sea anemone phylogeny, we conclude that the two paralogs originated due to a Nematostella-specific duplication of a ShK-like2 ancestor, a neuropeptide-encoding gene, followed by diversification and partial functional specialization. Strikingly, ShK-like2 is represented by two gene isoforms controlled by alternative promoters conferring regulatory flexibility throughout development. Additionally, we characterized the expression patterns of four other peptides with structural similarities to studied venom components, and revealed their unexpected neuronal localization. Thus, we employed genomics, transcriptomics and functional approaches to reveal one new venom component, five neuropeptides with two different cysteine motifs and an evolutionary pathway from nervous to venom system in Cnidaria.