Biology subjects

Surm, J. M.

Publications and source records attributed to Surm, J. M..

13 recordsLinked to original sources

bioRxiv2025

An ancient anthozoan protein reveals an alternative evolutionary path of antiviral signaling

How antiviral immunity first arose in animals is a central question in evolutionary biology. Using the sea anemone Nematostella vectensis, we identify CARDIB, a previously uncharacterized gene located next to RLRb, a cnidarian homolog of the vertebrate RIG-I-like receptor family. This conserved genomic linkage across Anthozoa reveals an ancient coupling between immune sensing and regulation. Despite sequence similarity to vertebrate MAVS, CARDIB performs an opposing function: it represses immune genes under basal conditions yet is essential for activation upon viral challenge. CARDIB binds RLRb via a single CARD domain, forming a repressive complex. Loss of either gene abolishes antiviral transcription, disrupts apoptosis, and elevates viral load under lab conditions. Both genes as well as the RLRb paralog, RLRa, are essential for antiviral defense under native conditions. Phylogeny places the cnidarian CARDs distinctly from the vertebrate RLR-MAVS families, revealing an ancient antiviral system regulating antiviral response through CARD-based signaling.

evolutionary biology↗

bioRxiv2025

Transcription dynamics and regulation of heat shock protein genes during stress and development in the estuarine cnidarian Nematostella vectensis

Heat shock proteins (HSPs) are conserved molecular chaperones that function in protecting cells from proteotoxic conditions. Most eukaryotes have multiple HSP genes that encode for proteins localizing in the cytoplasm, endoplasmic reticulum (ER), and mitochondria. In marine invertebrates of the phylum Cnidaria, where HSPs are often used as biomarkers of environmental stress, little is known about how particular HSPs vary in copy number, expression, inducibility, and regulation within a species. In this study, we characterized the diversity of the full repertoire of HSP70 and HSP90 genes in an emerging model cnidarian, Nematostella vectensis. We identified five distinct HSP70 and three HSP90 genes, with at least one homolog from each family belonging to the three primary clades based on subcellular localization. Although transcription of none of these HSPs was significantly induced by a temperature change of 10{degrees}C, two cytosolic HSP70s and one cytosolic HSP90 were significantly upregulated with a 20{degrees}C increase in temperature. Most HSPs followed a similar pattern of expression across various developmental stages of N. vectensis, with an increase in expression during the early larval stage followed by a decrease during the juvenile stage. HSPs showed evidence for differential expression in particular cell types, where multiple cytosolic and ER HSPs were highly expressed in neuronal and cnidocyte cell types. Moreover, there were differences in the abundance and sequences of regulatory heat shock element motifs in the putative promoters of N. vectensis HSPs, providing a potential mechanistic basis of functional diversification in response to temperature and development. By characterizing the expression of all HSP70 and HSP90 genes in this cnidarian, we reveal distinct roles of these core genes in the proteostasis response, providing a foundation for future functional studies into the diverse contributions of HSPs to cnidarian life cycle and stress resilience.

physiology↗

bioRxiv2025

Symbiont-specific uptake is mediated by integrins in cnidarian larvae

The symbiotic relationship between dinoflagellate algae and their cnidarian hosts is fundamental to the health of coral reefs. The selection of appropriate symbionts is paramount for the host to gain valuable nutrients and could be tailored to increase stress tolerance against anthropogenic induced changes in ocean environments, such as coral bleaching in response to ocean warming. Previous research suggests glycan-lectin interactions play a role in symbiont uptake; however, blockage of such interactions does not fully inhibit symbiosis establishment, suggesting other receptors are at play. Potential candidates include RGD peptide binding integrins, which are known to mediate phagocytosis of microbes in other systems. Here, we used a combination of cnidarian model systems and human cell lines to determine if integrins facilitate symbiont recognition and uptake. Integrins are highly expressed in the endodermal tissue of the host, where symbiosis takes place, and upon uptake into endodermal cells, symbionts altered the expression of integrins and downstream signaling molecules. Blockage of integrin binding sites with RGD competitor peptides reduced symbiont uptake, but had no effect on the general uptake of non-symbiotic algae, or uptake in a non-symbiotic cnidarian. In addition, inert beads coated with integrin RGD peptide ligands were phagocytosed more readily than beads coated with scrambled peptide. Finally, overexpression of RGD-binding integrins in human cells increased symbiont uptake and mutation of the active binding site abolished uptake. Our findings reveal RGD-binding integrins as key players in symbiosis establishment and shed light on the evolutionary functions of integrins as phagocytic receptors. Significance statementCorals engage in a symbiotic partnership with photosynthetic algae to survive in challenging environments. To date it is largely unclear how the two partners recognize each other. Using a comparative model systems approach, we have identified evolutionary conserved integrins as molecular receptors for specifically engulfing symbionts, but not other algae. This suggests that integrins allow the host to distinguish between symbiotic and non-symbiotic algae and preferentially take up symbionts. Our findings establish a new paradigm for symbiosis establishment in corals and shed light on the ancient function of integrins as environmental sensors.

cell biology↗

bioRxiv2024

A comparative analysis of toxin gene families across diverse sea anemone species

All species from order Actiniaria (sea anemones) are venomous, even though most are of no threat to humans. Currently, we know very little about the toxin gene complement of highly venomous members of this order. To address this gap in knowledge, we sequenced the transcriptome of the highly venomous and medically significant Hells Fire sea anemone, Actinodendron plumosum, as well as five distantly related species, Cryptodendrum adhaesivum, Epiactis australiensis, Heteractis aurora, Isactinia olivacea and Stichodactyla mertensii. We used bioinformatic approaches to identify their toxin gene complements and performed a comparative evolutionary analysis of seven understudied toxin families. Of the 16 toxin families identified, 12-40 candidate toxins were found in the six new sea anemone transcriptomes, with only 12 candidates in eight toxin families identified in A. plumosum. Across 26 sea anemone species, six neurotoxin families showed evidence of taxonomic restriction, whereas the phospholipase A2 toxin family was ubiquitously distributed. Additionally, we identified two alternative forms for the phospholipase A2 toxin family, a 10- and 14-cysteine framework, which warrant further structural and functional characterisation. Overall, we have identified a comprehensive list of toxins from a wide diversity of sea anemone species that provides the basis for future research to structurally and functionally characterise novel candidates for use as therapeutics or for agricultural applications.

genetics↗

bioRxiv2023

Sea anemone MACPF proteins demonstrate an evolutionary transitional state between venomous and developmental functions

Gene duplication is a major force driving evolutionary innovation. A classic example is generating new animal toxins via duplication of physiological protein-encoding genes and recruitment into venom. While this process drives the innovation of many animal venoms, reverse-recruitment of toxins into non-venomous cells remains unresolved. Using comparative genomics, we find members of the Membrane Attack Complex and Perforin Family (MACPF) have been recruited into venom-injecting cells (cnidocytes), in soft and stony corals and sea anemones, suggesting that the ancestral MACPF was a cnidocyte expressed toxin. Further investigation into the model sea anemone Nematostella vectensis, reveals that three members have undergone Nematostella-specific duplications leading to their reverse-recruitment into mesoendodermal cells. Furthermore, simultaneous knock-down of all three mesoendodermally-expressed MACPFs leads to mis-development, supporting that these paralogs have non-venomous function. By resolving the evolutionary history and function of MACPFs in Nematostella, we provide the first proof for reverse-recruitment from venom to organismal development. Significance statementIn this study, we reveal how a gene can gain a new function, even from a most unexpected origin. Specifically, we report that in the last common ancestor of corals and sea anemones a member of the Membrane Attack Complex and Perforin Family (MACPF), which is commonly associated with the immune system, was recruited into venom-injecting cells called cnidocytes. Using the sea anemone Nematostella vectensis we find repeated gene duplication has occurred leading to the new copies adopting divergent functions including being retained in cnidocytes but also recruited into non-venomous mesoendodermal cells. Furthermore, when we deplete Nematostella of mesoendodermally-expressed MACPFs we disrupt normal embryonic development, supporting that these copies have indeed been recruited from venom into the developmental plan.

evolutionary biology↗

bioRxiv2023

Venom tradeoff shapes interspecific interactions, physiology and reproduction

The ability of an animal to effectively capture prey and defend against predators is pivotal for its survival. Venom, a mixture of many toxin proteins, shapes predator-prey interactions. Here, we use the sea anemone Nematostella vectensis to test how toxin genotypes impact predator-prey interactions. We developed a new genetic manipulation tool which significantly reduces both RNA and protein levels of Nv1, a major neurotoxin. In concert we recently discovered a native population of Nematostella that has lost Nv1.We demonstrate that these anemones lacking Nv1, have reduced ability to defend themselves against grass shrimp, a native predator. Additionally, secreted Nv1 can act indirectly in defense by attracting mummichog fish, which are known to prey on grass shrimp. This unravels a tritrophic interaction acting in animal defense at the molecular level. Additionally, our work reveals an evolutionary tradeoff, as the reduction of Nv1 levels causes faster growth and increased sexual and asexual reproductive rates.

evolutionary biology↗

bioRxiv2022

A pan-cnidarian microRNA is an ancient biogenesis regulator of stinging cells

An ancient evolutionary innovation of a novel cell-type, the stinging cell (cnidocyte), appeared >600 million years ago in the phylum Cnidaria (sea anemones, corals, hydroids, and jellyfish). A complex bursting nano-injector of venom, the cnidocyst, is embedded in cnidocytes and enables cnidarians paralyzing prey and predators, contributing to this phylums evolutionary success. In this work, we show that post-transcriptional regulation by a pan-cnidarian microRNA, miR-2022, is essential for biogenesis of these cells. By manipulation of miR-2022 levels in a transgenic reporter line of cnidocytes in the sea anemone Nematostella vectensis, followed by transcriptomics, single-cell data analysis, prey paralysis assays, and cell sorting of transgenic cnidocytes, we reveal that miR-2022 enables cnidocyte biogenesis, while exhibiting a conserved expression domain with its targets in cnidocytes of other cnidarian species. Thus, here we reveal one of natures most ancient microRNA-regulated processes by studying the functional basis for its conservation.

evolutionary biology↗

bioRxiv2022

Genomic, Functional and Structural Analyses Reveal Mechanisms of Evolutionary Innovation within the Sea Anemone 8 Toxin Family

ShK from Stichodactyla helianthus has established the therapeutic potential of sea anemone venom peptides, but many lineage-specific toxin families in actinarians remain uncharacterised. One such peptide family, sea anemone 8 (SA8), is present in all five sea anemone superfamilies. We explored the genomic arrangement and evolution of the SA8 gene family in Actinia tenebrosa and Telmatactis stephensoni, characterised the expression patterns of SA8 sequences, and examined the structure and function of SA8 from the venom of T. stephensoni. We identified ten SA8 genes in two clusters and six SA8 genes in five clusters for T. stephensoni and A. tenebrosa, respectively. Nine SA8 T. stephensoni genes were found in a single cluster and an SA8 peptide encoded by an inverted SA8 gene from this cluster was recruited to venom. We show that SA8 genes in both species are expressed in a tissue-specific manner and the inverted SA8 gene has a unique tissue distribution. While functional activity of the SA8 putative toxin encoded by the inverted gene was inconclusive, its tissue localisation is similar to toxins used for predator deterrence. We demonstrate that, although mature SA8 putative toxins have similar cysteine spacing to ShK, SA8 peptides are distinct from ShK peptides based on structure and disulfide connectivity. Our results provide the first demonstration that SA8 is a unique gene family in actiniarians, evolving through a variety of structural changes including tandem and proximal gene duplication and an inversion event that together allowed SA8 to be recruited into the venom of T. stephensoni.

genetics↗

bioRxiv2022

Distinct features in fish Bouncer proteins determine sperm-egg compatibility

All sexually reproducing organisms depend on fertilization to survive as species. Despite the importance of fertilization, the mechanisms that drive sperm-egg compatibility are poorly understood. In fish, the egg protein Bouncer is necessary for fertilization and is species-specific between medaka and zebrafish. Here, we investigate whether Bouncer is generally species-specific in fish and identify features mediating its medaka/zebrafish specificity. In vitro fertilization experiments using zebrafish and medaka show that Bouncer is not a general specificity factor. Instead, its homologs exhibit wide compatibility with sperm, in line with the pervasive purifying selection that dominates Bouncers evolution. We further uncover specific features of Bouncer-- distinct amino acid residues and N-glycosylation patterns--that differentially influence the function of medaka and zebrafish Bouncer homologs and contribute to medaka/zebrafish specificity. This work reveals important themes central to understanding Bouncers function in sperm binding and clarifying the molecular requirements for Bouncers sperm interaction partner.

developmental biology↗

bioRxiv2022

Dominant toxin hypothesis: unravelling the venom phenotype across micro and macroevolution

Venom is a complex trait with substantial inter- and intraspecific variability resulting from strong selective pressures acting on the expression of many toxic proteins. However, understanding the processes underlying the toxin expression dynamics that determine the venom phenotype remains unresolved. Here, we use comparative genomics and transcriptomics to reveal that toxin expression in sea anemones evolves rapidly with little constraint and that a single toxin family dictates the venom phenotype in each species. This dominant toxin family is characterized by massive gene duplication events. In-depth analysis of the sea anemone, Nematostella vectensis, revealed significant variation in the number of copies of the dominant toxin (Nv1) across populations, corresponding to significant differences in Nv1 expression at both the transcript and protein levels. These differences in Nv1 copies are driven by independent expansion events, resulting in distinct haplotypes that have a restricted geographical distribution. Strikingly, one population has undergone a severe contraction event, causing a near-complete loss of Nv1 production. Our findings across micro- and macroevolutionary scales in sea anemones complement observations of single dominant toxin family present in other venomous organisms and establishes the dominant toxin hypothesis whereby venomous animals have convergently evolved a similar strategy in shaping the venom phenotype.

evolutionary biology↗

bioRxiv2020

Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom

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.

evolutionary biology↗

bioRxiv2020

Population Specific Adaptations in Venom Production to Abiotic Stressors in a Widely Distributed Cnidarian

Nematostella vectensis is a sea anemone (Actiniaria, Cnidaria) inhabiting estuaries over a broad geographic range where environmental conditions such as temperatures and salinity vary widely. In cnidarians, antagonistic interactions with predators and prey are mediated by their venom, which may be metabolically expensive. In this study, we challenged Nematostella polyps with heat, salinity, UV light stressors and a combination of all three 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 suggesting that downregulating venom expression under stressful conditions may be advantageous. Strikingly, under a range of abiotic stressors, individuals from different geographic locations along this latitudinal cline modulate venom production levels differently in a pattern reflecting local adaptation.

evolutionary biology↗

bioRxiv2019

The rapid regenerative response of a model sea anemone species Exaiptasia pallida is characterised by tissue plasticity and highly coordinated cell communication

Regeneration of a limb or tissue can be achieved through multiple different pathways and mechanisms. The sea anemone Exaiptasia pallida has been observed to have excellent regenerative proficiency but this has not yet been described transcriptionally. In this study we examined the genetic expression changes during a regenerative timecourse and report key genes involved in regeneration and wound healing. We found that the major response was an early upregulation of genes involved in cellular movement and cell communication, which likely contribute to a high level of tissue plasticity resulting in the rapid regeneration response observed in this species. We find the immune system is only transcriptionally active in the first eight hours post-amputation and conclude, in accordance with previous literature, that the immune system and regeneration have an inverse relationship. Fifty-nine genes (3.8% of total) differentially expressed during regeneration were identified as having no orthologues in other species, indicating that regeneration in E. pallida may rely on the activation of species-specific novel genes. Additionally, taxonomically-restricted novel genes, including species-specific novels, and highly conserved genes were identified throughout the regenerative timecourse, showing that both may work in concert to achieve complete regeneration. We conclude that E. pallida behaves similarly to other anemone species such as Nematostella vectensis and Calliactis polypus but with some notable novel differences.

evolutionary biology↗