Florida Southern College Digital Repository :: Browsing by Author "Macrander, Jason"

Browsing by Author "Macrander, Jason"

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A cnidarian phylogenomic tree fitted with hundreds of 18S leaves
(bioRxiv, 2022-10-05) DeBiasse, Melissa; Buckenmeyer, Ariane; Macrander, Jason; Babonis, Leslie S.; Bentlage, Bastian; Cartwright, Paulyn; Prada, Carlos; Reitzel, Adam M.; Stampar, Sergio N.; Collins, Allen G.; Daly, Marymegan; Ryan, Joseph F.
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.
The Birth and Death of Toxins with Distinct Functions: A Case Study in the Sea Anemone Nematostella
(Oxford University Press, 2019-09) Sachkova, Maria Y.; Singer, Shir A.; Macrander, Jason; Reitzel, Adam M.; Peigneur, Steve; Tytgat, Jan; Moran, Yehu
The cnidarian Nematostella vectensis has become an established lab model, providing unique opportunities for venom evolution research. The Nematostella venom system is multimodal: involving both nematocytes and ectodermal gland cells, which produce a toxin mixture whose composition changes throughout the life cycle. Additionally, their modes of interaction with predators and prey vary between eggs, larvae, and adults, which is likely shaped by the dynamics of the venom system. Nv1 is a major component of adult venom, with activity against arthropods (through specific inhibition of sodium channel inactivation) and fish. Nv1 is encoded by a cluster of at least 12 nearly identical genes that were proposed to be undergoing concerted evolution. Surprisingly, we found that Nematostella venom includes several Nv1 paralogs escaping a pattern of general concerted evolution, despite belonging to the Nv1-like family. Here, we show two of these new toxins, Nv4 and Nv5, are lethal for zebrafish larvae but harmless to arthropods, unlike Nv1. Furthermore, unlike Nv1, the newly identified toxins are expressed in early life stages. Using transgenesis and immunostaining, we demonstrate that Nv4 and Nv5 are localized to ectodermal gland cells in larvae. The evolution of Nv4 and Nv5 can be described either as neofunctionalization or as subfunctionalization. Additionally, the Nv1-like family includes several pseudogenes being an example of nonfunctionalization and venom evolution through birth-and-death mechanism. Our findings reveal the evolutionary history for a toxin radiation and point toward the ecological function of the novel toxins constituting a complex cnidarian venom. (© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.)
Dominant toxin hypothesis: unravelling the venom phenotype across micro and macroevolution
(bioRxiv, 2022-06-26) Smith, Edward G.; Surm, Joachim M.; Macrander, Jason; Simhi, Adi; Amir, Guy; Sachkova, Maria Y.; Lewandowska, Magda; Reitzel, Adam M.; Moran, Yehu
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.
Exploring Differential Gene Expression Profiles Of Dero (Allodero) Hylae In Their Parasitic And Free-Living Forms
(bioRxiv, 2022-06-18) Bonham, Claire; Roguski, Ashley; Langford, Gabriel J.; Macrander, Jason
Parasitism is ubiquitous in nature, yet little is known about the evolutionary mechanisms that lead to a parasitic lifestyle. Facultative parasites can switch between free-living and parasitic lifestyles, which may provide an opportunity to study the genetic mechanisms underlying a transition to parasitism. The oligochaete Dero (Allodero) hylae is a facultative parasite commonly found within the ureter of various anuran species, such as the Cuban Tree Frog (Osteopilus septentrionalis). Dero hylae makes passage through the frog’s cloaca, where it then infects the ureter. In the ureter, the worm loses free-living characteristics such as hair setae, dorsal setae, a digestive tract, and fossa with gills as it transitions to a parasitic lifestyle. Dero hylae may be expelled from its host during urination, when this occurs the worm will reacquire free-living characteristics. The focus of this study is to compare the differential gene expression profiles observed when this rapid morphological change takes place. Specimens of D. hylae were collected from wild Cuban Tree Frogs and either flash-frozen for their parasitic stage RNA profile or cultured for two weeks to produce their free-living stage and then flash-frozen. Using the sequenced RNA, a de novo transcriptome was assembled and differential gene expression RNA Tag-Seq analysis between the free-living and parasitic life forms was analyzed. Based on these results, we have identified 213 genes differentially expressed transcripts between the two life forms, 190 of these being up-regulated in the free-living life form. While over half of the differential genes recovered did not recover any significant BLAST hits, many of these genes did provide insight into which molecular signals are potentially used by D. hylae to lose and subsequently regrow their setae, digestive tract, and gills. This analysis provides significant insight into which differentially expressed genes are linked to drastic morphological changes observed in this rare oligochaete parasitism across the free-living and parasitic forms of D. hylae.
Identifying Convergence of ShK Toxins in Sea Anemones
(Florida Southern College, 2020-04) Krantz, Jacqueline; Marymegan, Daly; Macrander, Jason
Toxins and other naturally derived products synthesized for predatory defense or prey capture can often be harmful to humans, but in some cases they may also present pharmaceutical potential. One toxin in particular, commonly referred to as ShK, has been isolated from the sea anemone Stichodactyla helianthus and exhibits potential to treat autoimmune diseases such as multiple sclerosis. The currently existing ShK toxin as well as its analogs are not ideal in their target and treatment, exhibiting some flaws regarding effective transport and binding to Kv1.3 channels. Toxins containing this domain are ubiquitous across sea anemones as they target potassium ion channels, potentially being used to immobilize prey or deter predators. We hypothesized that there may be variations of the toxin that are naturally produced by other species. Our bioinformatic approach has found 586 ShK toxin candidates in 23 sea anemone species. Our results are the first step towards identifying ShK proteins that could combat various types of autoimmune or even neurological diseases.
Leveraging Digital Tools (ChatGPT) for Student Success
(2023-09-18) Eicholtz, Matthew; Huneycutt, Keith; Macrander, Jason
Linear Mitochondrial Genome in Anthozoa (Cnidaria): A Case Study in Ceriantharia
(Nature Publishing Group, 2019) Stampar, Sérgio N.; Broe, Michael B.; Macrander, Jason; Reitzel, Adam M.; Brugler, Mercer R.; Daly, Marymegan
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.
Micro and macroevolution of sea anemone venom phenotype
(Nature Communications, 2023-01-16) Smith, E.G.; Surm, J.M.; Macrander, Jason; Simhi, A.; Amir, G.; Sachkova, M.Y.; Lewandowska, M.; Reitzel, A.M.; Moran, Y.
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 toxin expression dynamics that determine the venom phenotype remains unresolved. By interspecific comparisons we reveal that toxin expression in sea anemones evolves rapidly and that in each species different toxin family dictates the venom phenotype by massive gene duplication events. In-depth analysis of the sea anemone, Nematostella vectensis, revealed striking variation of the dominant toxin (Nv1) diploid copy number across populations (1-24 copies) resulting from independent expansion/contraction events, which generate distinct haplotypes. Nv1 copy number correlates with expression at both the transcript and protein levels with one population having a near-complete loss of Nv1 production. Finally, we establish the dominant toxin hypothesis which incorporates observations in other venomous lineages that animals have convergently evolved a similar strategy in shaping their venom. (© 2023. The Author(s).)
Never, Ever Make an Enemy… Out of an Anemone: Transcriptomic Comparison of Clownfish Hosting Sea Anemone Venoms
(Marine Drugs, 2022) Delgado, Alonso; Benedict, Charlotte; Macrander, Jason; Daly, Marymegan
Sea anemones are predatory marine invertebrates and have diverse venom arsenals. Venom is integral to their biology, and is used in competition, defense, and feeding. Three lineages of sea anemones are known to have independently evolved symbiotic relationships with clownfish, however the evolutionary impact of this relationship on the venom composition of the host is still unknown. Here, we investigate the potential of this symbiotic relationship to shape the venom profiles of the sea anemones that host clownfish. We use transcriptomic data to identify differences and similarities in venom profiles of six sea anemone species, representing the three known clades of clownfish-hosting sea anemones. We recovered 1121 transcripts matching verified toxins across all species, and show that hemolytic and hemorrhagic toxins are consistently the most dominant and diverse toxins across all species examined. These results are consistent with the known biology of sea anemones, provide foundational data on venom diversity of these species, and allow for a review of existing hierarchical structures in venomic studies. © 2022 by the authors.
A new color morph of Calappa flammea (Herbst, 1794), with implications for the taxonomy of Calappa Weber, 1795 (Decapoda: Brachyura: Calappidae)
(Oxford University Press, 2021-09-01) Vossgaetter, Lennart; Larson, Paul; Macrander, Jason
Many species of the brachyuran crabs in the family Calappidae, commonly known as 'box crabs' or 'shame-faced crabs,' look alike and are difficult to distinguish at various developmental stages based on morphology alone. Some crabs recently collected as a part of the South East Atlantic Monitoring and Assessment Program (SEAMAP) groundfish surveys were identified as likely members of Calappidae, but could not be determined to species due to their unusual color pattern and size. The use of molecular data in combination with morphometrics suggests that the crabs in question belonged to Calappa flammea (Herbst, 1794). The specimens represent an undescribed unique color morph that deviates from their previous description and should be considered for future identifications. Several ecological factors can cause such color variations in crabs, but further investigation is needed to understand the drivers of the described phenotypic variance in C. flammea. © 2021 The Author(s) 2021. Published by Oxford University Press on behalf of The Crustacean Society. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
Some like it hot: population-specific adaptations in venom production to abiotic stressors in a widely distributed cnidarian
(BMC Biology, 2020) Sachkova, Maria Y.; Macrander, Jason; Surm, Joachim M.; Aharoni, Reuven; Menard-Harvey, Shelcie S.; Klock, Amy; Leach, Whitney B.; Reitzel, Adam M.; Moran, Yehu
Abstract Background 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. Results 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. Conclusions 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.
The Role of the Vascular Endothelial Growth Factor (VEGF) Signaling in Biomineralization of the Oyster Crassostrea gigas Authors: Anna V. Ivanina
(Frontiers Media S.A, 2018) Ivanina, Anna V.; Borah, Ballav; Rimkevicius, Tadas; Macrander, Jason; Piontkivska, Helen; Sokolova, Inna M.; Beniash, Elia
Vascular endothelial growth factor (VEGF) and vascular endothelial growth factor receptor (VEGFR) play a role in early development, organogenesis, and regeneration, as well as biomineralization of invertebrates. The involvement of VEGF and VEGFR in biomineralization was demonstrated in sea urchin larvae but its role in the biomineralization of other invertebrate groups such as mollusks is not known. We assessed the potential role of VEGF signaling on biomineralization of a model marine bivalve, the Pacific oyster Crassostrea gigas, by analyzing the effects of a VEGFR inhibitor (50 nM axitinib) on shell growth, shell hardness, and expression profiles of biomineralization-related genes. Bioinformatics analysis identified a wide range of biomineralization-related genes potentially activated by VEGF including carbonic anhydrases (CAs), sodium/proton and sodium/calcium exchangers, calmodulins, and genes involved in chitin metabolism. Exposure to a VEGFR inhibitor axitinib led to upregulation of CAs (CA7 and CA12), sodium/proton exchanger 10, sodium/calcium exchanger 1 and 3, as well as calmodulin mRNA in hemocytes (HCs). In the mantle tissue, axitinib exposure led to a compensatory upregulation of VEGFR mRNA but did not affect the expression of other studied biomineralization genes. Expression of VEGF, VEGFR mRNA, or that of the downstream biomineralization-related genes in a non-biomineralizing tissue (the gill) was not affected by axitinib. The shell mass was higher in the axitinib treatment group. Inhibition of VEGFR led to significant increase in shell microhardness, and to a small but statistically significant decrease in crystallinity. Our results therefore indicate that, although VEGF signaling might not play a crucial role in shell biomineralization of C. gigas as it does in mammals and echinoderms, it is involved in regulation of shell formation in bivalves and that effects of VEGF on biomineralization are likely mediated by HCs.
Toxin-like neuropeptides in the sea anemone Nematostella unravel recruitment from the nervous system to venom
(National Academy of Sciences, 2020-10) Sachkova, Maria Y.; Landau, Morani; Surm, Joachim M.; Macrander, Jason; Singer, Shir A.; Reitzel, Adam M.; Moran, Yehu
The sea anemone (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 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 -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.
Transcriptomic Analysis of Four Cerianthid (Cnidaria, Ceriantharia) Venoms
(MDPI AG, 2020) Klompen, Anna M. L.; Macrander, Jason; Reitzel, Adam M.; Stampar, Sérgio N.
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.

Browsing by Author "Macrander, Jason"

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