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Reitzel, A. M.

Publications and source records attributed to Reitzel, A. M..

14 recordsLinked to original sources

Intersection of genotype and environment on the dynamics of the virome and microbiome of an estuarine cnidarian

Estuaries host a rich diversity of microorganisms, creating opportunities for animal-microbe interactions that shape host physiology. The sea anemone Nematostella vectensis spans the eastern coast of North America from Nova Scotia to Florida, and prior work shows that anemones from different regions harbor distinct microbial communities. Although the virome of the standard laboratory population has been characterized, population-level variation in viromes remains largely unknown. To address this gap, we conducted a mesocosm experiment using six N. vectensis populations to test whether geographic origin influences the diversity and functional potential of associated viruses and bacteria. We sampled individuals before mesocosm exposure and 14 days after to sequence their viromes, microbiomes, and host transcriptomes. We also collected anemones from a natural population to compare against experimental animals. Both virome and microbiome analyses revealed increased taxonomic and functional diversity after 14 days, with the strongest increase observed in lower-latitude populations. Notably, experimental anemones did converge toward the natural populations community composition; however, population-specific interactions with viruses and microbes persisted. Differential gene expression indicated a modest host response overall, whereas WGCNA identified a clear north-south expression pattern. Together, these findings demonstrate that N. vectensis genotypes from locations along a latitudinal gradient maintain distinct viral and microbial associations, highlighting geographically structured host-microbe-virus relationships.

ecology↗

A Matter of Degrees: Latitudinal Variation in the Transcriptional Response to High and Low Temperatures in an Estuarine Cnidarian

Populations of the same species inhabiting distinct geographical regions must meet the requirements of local thermal regimes to survive. While individuals integrate both deeply conserved and genotype-specific transcriptional responses to temperature shifts, unique local requirements may diversify the balance between these two mechanisms in distinct populations. The sea anemone Nematostella vectensis inhabits highly variable estuarine environments across a broad geographic range, providing an excellent system to investigate how local adaptations shape responses to temperature stress. While studies have explored the genotypic and phenotypic diversity among N. vectensis populations, the diversity in transcriptional responses to heat and cold remain poorly understood. We used RNA sequencing to characterize transcriptional programs in N. vectensis from Nova Scotia (NS), Maryland (MD), and Florida (FL) under acute temperature treatments at 10{degrees}C and 38{degrees}C. Individuals exhibited a stronger response at 38{degrees}C than at 10{degrees}C, with NS and MD responses being similar and FL exhibiting a unique response. A core set of genes was differentially expressed across all populations under heat stress, while responses to cold were highly population specific. To evaluate the role of a key transcription factor, heat shock factor (HSF), we analyzed the presence of HSF binding sites (HSEs) in promoters of differentially expressed genes (DEGs). Upregulated genes containing three or more promoter HSEs were strongly induced at 38{degrees}C in MD and FL, but not in NS. To identify the involvement of other transcription factors, we searched for overrepresented motifs in the promoters of the top 100 DEGs at 38{degrees}C, revealing a differential enrichment of motifs across the three populations. Together, these findings suggest that N. vectensis populations utilize diverse transcriptional programs in response to common hot and cold temperatures.

ecology↗

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↗

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↗

Rapid speciation in the holopelagic ctenophore Mnemiopsis following glacial recession

BackgroundUnderstanding how populations diverge is one of the most compelling questions in evolutionary biology but our grasp on the genomic mechanisms underpinning divergence is limited to a handful of species. Indeed, we know even less about divergence in the pelagic zone, where barriers to gene flow are seemingly absent. The holopelagic ctenophore Mnemiopsis leidyi is the most widely used ctenophore in experimental biology and has become an important model system in studies ranging from developmental biology to neurobiology. In addition, its relatively small and tractable genome provides a powerful foundation for genomic and evolutionary analyses. However, we still lack a clear understanding of species boundaries, population structure, and the evolutionary forces shaping divergence within Mnemiopsis, limiting both evolutionary and ecological interpretations. To expand our general understanding of divergence across novel environments as well as resolve a long-standing taxonomic debate, we generated the most comprehensive genomic study to date of the holopelagic ctenophore Mnemiopsis across a large expanse of its native range. ResultsBy leveraging multiple analytical approaches and generating two near-chromosome level genomes, we identify two distinct species of Mnemiopsis with high levels of genome-wide divergence along the US Atlantic coast, which correspond to M. leidyi and M. gardeni. Our demographic analyses suggest that M. leidyi and M. gardeni began to diverge during the mid-to-late Pleistocene climate transitions and were later shaped by post-glacial oceanographic changes. We highlight substantial genomic rearrangements and copy number variation between species as well as uncover key genes under selection that are likely important for environmental adaptation. ConclusionsTogether, these findings provide compelling evidence that the ctenophore currently recognized as M. leidyi represents more than one species. Recognizing cryptic species boundaries is critical for future study designs, environmental monitoring, and developing targeted management strategies. Altogether, we connect microevolutionary processes with macroevolutionary patterns and provide new insights into how ocean dynamics drive speciation and adaptation in pelagic ecosystems.

evolutionary biology↗

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↗

A cnidarian phylogenomic tree fitted with hundreds of 18S leaves

Cnidarians are critical members of aquatic communities and have been an experimental system for a diversity of research areas ranging from development to biomechanics to global change biology. Yet we still lack a well-resolved, taxonomically balanced, cnidarian tree of life to place this research in appropriate phylogenetic context. To move towards this goal, we combined data from 26 new anthozoan transcriptomes with 86 previously published cnidarian and outgroup datasets to generate two 748-locus alignments containing 123,051 (trimmed) and 449,935 (untrimmed) amino acids. We estimated maximum likelihood phylogenies for both matrices under partitioned and unpartitioned site-homogeneous and site-heterogenous models of substitution. We used the resulting topology to constrain a phylogenetic analysis of 1,814 small subunit ribosomal (18S) gene sequences from GenBank. Our results confirm the position of Ceriantharia (tube-dwelling anemones), a historically recalcitrant group, as sister to the rest of Hexacorallia across all phylogenies regardless of data matrix or model choice. We also find unanimous support for the sister relationship of Endocnidozoa and Medusozoa and propose the name Operculozoa for the clade uniting these taxa. Our 18S hybrid phylogeny provides insight into relationships of 15% of extant taxa. Together these data are an invaluable resource for comparative cnidarian research and provide perspective to guide future refinement of cnidarian systematics.

evolutionary biology↗

Genotype-environment interactions determine microbiota plasticity in Nematostella vectensis

Most multicellular organisms harbor microbial colonizers that provide various benefits to their hosts. Although these microbial communities may be host species- or even genotype-specific, the associated bacterial communities can respond plastically to environmental changes. In this study, we estimated the relative contribution of environment and host genotype to bacterial community composition in Nematostella vectensis, an estuarine cnidarian. We isolated N. vectensis polyps from five different populations along a north-south gradient on the Atlantic coast of the United States and Canada at three different times of the year. While half of the polyps were immediately analyzed for their bacterial composition by 16S rRNA gene sequencing, the remaining polyps were cultured under laboratory conditions for one month. Bacterial community comparison analyses revealed that laboratory maintenance reduced bacterial diversity by fourfold, but maintained a population-specific bacterial colonization. Interestingly, the differences between bacterial communities correlated strongly with seasonal variations, especially with ambient water temperature. To decipher the contribution of both ambient temperature and host genotype to bacterial colonization, we generated 12 clonal lines from six different populations in order to maintain each genotype at three different temperatures for three months. The bacterial community composition of the same N. vectensis clone differed greatly between the three different temperatures, highlighting the contribution of ambient temperature to bacterial community composition. To a lesser extent, bacterial community composition varied between different genotypes under identical conditions, indicating the influence of host genotype. In addition, we identified a significant genotype x environment interaction determining microbiota plasticity in N. vectensis. From our results we can conclude that N. vectensis-associated bacterial communities respond plastically to changes in ambient temperature, with the association of different bacterial taxa depending in part on the host genotype. Future research will reveal how this genotype-specific microbiota plasticity affects the ability to cope with changing environmental conditions.

evolutionary biology↗

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↗

Vps501, a novel vacuolar SNX-BAR protein cooperates with the SEA complex to induce autophagy

The sorting nexins (SNX), constitute a diverse family of molecules that play varied roles in membrane trafficking, cell signaling, membrane remodeling, organelle motility and autophagy. In particular, the SNX-BAR proteins, a SNX subfamily characterized by a C-terminal dimeric Bin/Amphiphysin/Rvs (BAR) lipid curvature domain and a conserved Phox-homology domain, are of great interest. In budding yeast, many SNX-BARs proteins have well-characterized endo-vacuolar trafficking roles. Phylogenetic analyses allowed us to identify an additional SNX-BAR protein, Vps501, with a novel endo-vacuolar role. We report that Vps501 uniquely localizes to the vacuolar membrane and works with the SEA complex to regulate autophagy. Furthermore, we found cells displayed a severe deficiency in starvation-induced/nonselective autophagy only when SEA complex subunits are ablated in combination with Vps501, indicating a cooperative role with the SEA complex during autophagy. Additionally, we found the SEA complex becomes destabilized in vps501{Delta}sea1{Delta} cells, which resulted in aberrant TORC1 hyperactivity and misregulation of autophagy induction.

cell biology↗

Transcriptomic analysis of four cerianthid (Cnidaria, Ceriantharia) venoms

Tube anemones, or cerianthids, are a phylogenetically informative group of cnidarians with complex life histories, including a pelagic larval stage and tube-dwelling adult stage, both known to utilize venom in stinging-cell rich tentacles. Cnidarians are an entirely venomous group that utilize their proteinaceous-dominated toxins to capture prey and defend against predators, in addition to several other ecological functions, including intraspecific interactions. At present there are no studies describing the venom for any species within cerianthids. Given their unique development, ecology, and distinct phylogenetic-placement within Cnidaria, our objective is to evaluate the venom-like gene diversity of four species of cerianthids from newly collected transcriptomic data. We identified 525 venom-like genes between all four species. The venom-gene profile for each species was dominated by enzymatic protein and peptide families, which is consistent with previous findings in other cnidarian venoms. However, we found few toxins that are typical of sea anemones and corals, and furthermore, three of the four species express toxin-like genes closely related to potent pore-forming toxins in box jellyfish. Our study is the first to provide a survey of the putative venom composition of cerianthids, and contributes to our general understanding of the diversity of cnidarian toxins.

evolutionary biology↗

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↗

Divergent microbiota of echinoid eggs separated by the Isthmus of Panama

Relationships between animals and their associated microbiota is dependent on the evolutionary history of the host and on the environment. The majority of studies tend to focus on one of these factors and rarely consider how both determine the community composition of the associated bacteria. One "natural experiment" to test how evolutionary history, shared environments, and the interaction between these factors drive community composition is to compare geminate species pairs. Echinoids separated by the Isthmus of Panama are suitable for this comparison due to the known evolutionary history and differences in oceanographic characteristics of the Caribbean Sea and Pacific Ocean. By comparing the egg-associated microbiota for the Echinometra and Diadema geminate species pairs, we show that both pairs of geminate species associate with distinct bacterial communities in patterns consistent with phylosymbiosis, and that the interaction between the evolutionary history of the host and the environment best explain differences in these communities. Moreover, we find that particular microbial taxa differed considerably between, but not within, oceans and that the microbiota of the two Caribbean Echinometra species were dominated by the phototrophic Oxyphotobacteria.

ecology↗

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↗