Reitzel Adam M.

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Reitzel

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Adam M.

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Actin polymerization controls the activation of multidrug efflux at fertilization by translocation and fine-scale positioning of ABCB1 on microvilli

(American Society for Cell Biology, 2012-08-01) Whalen, Kristen E. ; Reitzel, Adam M. ; Hamdoun, Amro

Fertilization changes the structure and function of the cell surface. In sea urchins, these changes include polymerization of cortical actin and a coincident, switch-like increase in the activity of the multidrug efflux transporter ABCB1a. However, it is not clear how cortical reorganization leads to changes in membrane transport physiology. In this study, we used three-dimensional superresolution fluorescence microscopy to resolve the fine-scale movements of the transporter along polymerizing actin filaments, and we show that efflux activity is established after ABCB1a translocates to the tips of the microvilli. Inhibition of actin polymerization or bundle formation prevents tip localization, resulting in the patching of ABCB1a at the cell surface and decreased efflux activity. In contrast, enhanced actin polymerization promotes tip localization. Finally, interference with Rab11, a regulator of apical recycling, inhibits activation of efflux activity in embryos. Together our results show that actin-mediated, short-range traffic and positioning of transporters at the cell surface regulates multidrug efflux activity and highlight the multifaceted roles of microvilli in the spatial distribution of membrane proteins.
NR3E receptors in cnidarians : a new family of steroid receptor relatives extends the possible mechanisms for ligand binding

( 2018-06) Khalturin, Konstantin ; Billas, Isabelle M. L. ; Chebaro, Yassmine ; Reitzel, Adam M. ; Tarrant, Ann M. ; Laudet, Vincent ; Markov, Gabriel V.

Steroid hormone receptors are important regulators of development and physiology in bilaterian animals, but the role of steroid signaling in cnidarians has been contentious. Cnidarians produce steroids, including A-ring aromatic steroids with a side-chain, but these are probably made through pathways different than the one used by vertebrates to make their A-ring aromatic steroids. Here we present comparative genomic analyses indicating the presence of a previously undescribed nuclear receptor family within medusozoan cnidarians, that we propose to call NR3E. This family predates the diversification of ERR/ER/SR in bilaterians, indicating that the first NR3 evolved in the common ancestor of the placozoan and cnidarian-bilaterian with lineage-specific loss in the anthozoans, even though multiple species in this lineage have been shown to produce aromatic steroids, whose function remain unclear. We discovered serendipitously that a cytoplasmic factor within epidermal cells of transgenic Hydra vulgaris can trigger the nuclear translocation of heterologously expressed human ERα. This led us to hypothesize that aromatic steroids may also be present in the medusozoan cnidarian lineage, which includes Hydra, and may explain the translocation of human ERα. Docking experiments with paraestrol A, a cnidarian A-ring aromatic steroid, into the ligand-binding pocket of Hydra NR3E indicates that, if an aromatic steroid is indeed the true ligand, which remains to be demonstrated, it would bind to the pocket through a partially distinct mechanism from the manner in which estradiol binds to vertebrate ER.
Nuclear receptor complement of the cnidarian Nematostella vectensis : phylogenetic relationships and developmental expression patterns

(BioMed Central, 2009-09-10) Reitzel, Adam M. ; Tarrant, Ann M.

Nuclear receptors are a superfamily of metazoan transcription factors that regulate diverse developmental and physiological processes. Sequenced genomes from an increasing number of bilaterians have provided a more complete picture of duplication and loss of nuclear receptors in protostomes and deuterostomes but have left open the question of which nuclear receptors were present in the cnidarian-bilaterian ancestor. In addition, nuclear receptor expression and function are largely uncharacterized within cnidarians, preventing determination of conserved and novel nuclear receptor functions in the context of animal evolution. Here we report the first complete set of nuclear receptors from a cnidarian, the starlet sea anemone Nematostella vectensis. Genomic searches using conserved DNA- and ligand-binding domains revealed seventeen nuclear receptors in N. vectensis. Phylogenetic analyses support N. vectensis orthologs of bilaterian nuclear receptors in four nuclear receptor subfamilies within nuclear receptor family 2 (COUP-TF, TLL, HNF4, TR2/4) and one putative ortholog of GCNF (nuclear receptor family 6). Other N. vectensis genes grouped well with nuclear receptor family 2 but represented lineage-specific duplications somewhere within the cnidarian lineage and were not clear orthologs of bilaterian genes. Three nuclear receptors were not well-supported within any particular nuclear receptor family. The seventeen nuclear receptors exhibited distinct developmental expression patterns, with expression of several nuclear receptors limited to a subset of developmental stages. N. vectensis contains a diverse complement of nuclear receptors including orthologs of several bilaterian nuclear receptors. Novel nuclear receptors in N. vectensis may be ancient genes lost from triploblastic lineages or may represent cnidarian-specific radiations. Nuclear receptors exhibited distinct developmental expression patterns, which are consistent with diverse regulatory roles for these genes. Understanding the evolutionary relationships and developmental expression of the N. vectensis nuclear receptor complement provides insight into the evolution of the nuclear receptor superfamily and a foundation for mechanistic characterization of cnidarian nuclear receptor function.
Conservation of DNA and ligand binding properties of retinoid X receptor from the placozoan Trichoplax adhaerens to human

( 2018-02) Reitzel, Adam M. ; Macrander, Jason ; Mane-Padros, Daniel ; Fang, Bin ; Sladek, Frances M. ; Tarrant, Ann M.

Nuclear receptors are a superfamily of transcription factors restricted to animals. These transcription factors regulate a wide variety of genes with diverse roles in cellular homeostasis, development, and physiology. The origin and specificity of ligand binding within lineages of nuclear receptors (e.g., subfamilies) continues to be a focus of investigation geared toward understanding how the functions of these proteins were shaped over evolutionary history. Among early-diverging animal lineages, the retinoid X receptor (RXR) is first detected in the placozoan, Trichoplax adhaerens. To gain insight into RXR evolution, we characterized ligand- and DNA-binding activity of the RXR from T. adhaerens (TaRXR). Like bilaterian RXRs, TaRXR specifically bound 9-cis-retinoic acid, which is consistent with a recently published result and supports a conclusion that the ancestral RXR bound ligand. DNA binding site specificity of TaRXR was determined through protein binding microarrays (PBMs) and compared with human RXR. The binding sites for these two RXR proteins were broadly conserved (~85% shared high-affinity sequences within a targeted array), suggesting evolutionary constraint for the regulation of downstream genes. We searched for predicted binding motifs of the T. adhaerens genome within 1000 bases of annotated genes to identify potential regulatory targets. We identified 648 unique protein coding regions with predicted TaRXR binding sites that had diverse predicted functions, with enriched processes related to intracellular signal transduction and protein transport. Together, our data support hypotheses that the original RXR protein in animals bound a ligand with structural similarity to 9-cis-retinoic acid; the DNA motif recognized by RXR has changed little in more than 1 billion years of evolution; and the suite of processes regulated by this transcription factor diversified early in animal evolution.
Light entrained rhythmic gene expression in the sea anemone Nematostella vectensis : the evolution of the animal circadian clock

(Public Library of Science, 2010-09-21) Reitzel, Adam M. ; Behrendt, Lars ; Tarrant, Ann M.

Circadian rhythms in behavior and physiology are the observable phenotypes from cycles in expression of, interactions between, and degradation of the underlying molecular components. In bilaterian animals, the core molecular components include Timeless-Timeout, photoreceptive cryptochromes, and several members of the basic-loop-helix-Per-ARNT-Sim (bHLH-PAS) family. While many of core circadian genes are conserved throughout the Bilateria, their specific roles vary among species. Here, we identify and experimentally study the rhythmic gene expression of conserved circadian clock members in a sea anemone in order to characterize this gene network in a member of the phylum Cnidaria and to infer critical components of the clockwork used in the last common ancestor of cnidarians and bilaterians. We identified homologs of circadian regulatory genes in the sea anemone Nematostella vectensis, including a gene most similar to Timeout, three cryptochromes, and several key bHLH-PAS transcription factors. We then maintained N. vectensis either in complete darkness or in a 12 hour light: 12 hour dark cycle in three different light treatments (blue only, full spectrum, blue-depleted). Gene expression varied in response to light cycle and light treatment, with a particularly strong pattern observed for NvClock. The cryptochromes more closely related to the light-sensitive clade of cryptochromes were upregulated in light treatments that included blue wavelengths. With co-immunoprecipitation, we determined that heterodimerization between CLOCK and CYCLE is conserved within N. vectensis. Additionally, we identified E-box motifs, DNA sequences recognized by the CLOCK:CYCLE heterodimer, upstream of genes showing rhythmic expression. This study reveals conserved molecular and functional components of the circadian clock that were in place at the divergence of the Cnidaria and Bilateria, suggesting the animal circadian clockwork is more ancient than previous data suggest. Characterizing circadian regulation in a cnidarian provides insight into the early origins of animal circadian rhythms and molecular regulation of environmentally cued behaviors.
Introduction to the symposium—Keeping Time During Evolution : Conservation and Innovation of the Circadian Clock

( 2013-04-17) Tarrant, Ann M. ; Reitzel, Adam M.

Diurnal and seasonal cues play critical and conserved roles in behavior, physiology, and reproduction in diverse animals. The circadian clock is a transcription-translation feedback loop that represents the molecular mechanism underlying many of these periodic processes, frequently through responses to light. Although much of the core regulatory machinery is deeply conserved among diverse animal lineages, there are also many examples of innovation in the way the clock either is constructed at the molecular-level or deployed in coordinating behavior and physiology. The nine papers contained within this issue address aspects of circadian signaling in diverse taxa, utilize wide-ranging approaches, and collectively provide thought-provoking discussion of future directions in circadian research.
Upgrades to StellaBase facilitate medical and genetic studies on the starlet sea anemone, Nematostella vectensis

(Oxford University Press, 2007-11-03) Sullivan, James C. ; Reitzel, Adam M. ; Finnerty, John R.

The starlet sea anemone, Nematostella vectensis, is a basal metazoan organism that has recently emerged as an important model system in developmental biology and evolutionary genomics. StellaBase, the Nematostella Genomics Database (http://stellabase.org), was developed in 2005 as a resource to support the Nematostella research community. Recently, it has become apparent that Nematostella may be a particularly useful system for studying (i) microevolutionary variation in natural populations, and (ii) the functional evolution of human disease genes. We have developed two new databases that will foster such studies: StellaBase Disease (http://stellabase.org/disease) is a relational database that houses 155 904 invertebrate homologous isoforms of human disease genes from four leading genomic model systems (fly, worm, yeast and Nematostella), including 14 874 predicted genes from the sea anemone itself. StellaBase SNP (http://stellabase.org/SNP) is a relational database that describes the location and underlying type of mutation for 20 063 single nucleotide polymorphisms.
Physiological and developmental responses to temperature by the sea anemone Nematostella vectensis

(Inter-Research, 2013-06-12) Reitzel, Adam M. ; Chu, Tim ; Edquist, Sara ; Genovese, Caitlyn ; Church, Caitlin ; Tarrant, Ann M. ; Finnerty, John R.

Environmental temperature and an organism’s ability to respond to it are critical determinants of the geographic distribution of species. Nematostella vectensis is a burrowing sea anemone that inhabits estuaries along the Atlantic coast of North America from Nova Scotia (45°N) to Georgia (31°N). Like other estuarine species, N. vectensis is exposed to large daily (>20°C) and seasonal (>25°C) fluctuations in temperature, requiring wide temperature tolerances. At the same time, the natural distribution of this species spans a pronounced thermal cline, which may promote the evolution of different temperature optima and tolerances in populations. We tested the thermal tolerance of N. vectensis adult and developmental stages, which showed all life cycle stages had critical temperatures within 1°C (lethal temperature 39.5 to 40.5°C). When temperature tolerance values were compared with recorded field data, N. vectensis is living in environments very close to their physiological limit. We utilized common garden experiments (13, 21, and 29°C) to test for temperature-specific growth and regeneration rates in N. vectensis from different portions of this species’ range. Temperature had a significant effect on growth and regeneration rate in all clonal lines, with a significant negative relationship between latitude of origin and growth rate at 29°C. Individuals from higher latitudes did not exhibit higher growth rates at cooler temperatures. Together, our results show a combination of broad thermal tolerances for developmental and adult stages and evidence for local adaptation to higher temperatures in populations living in lower latitude locations that would be physiologically compromised with future warming.
Correlated evolution of androgen receptor and aromatase revisited

( 2010-05-11) Reitzel, Adam M. ; Tarrant, Ann M.

Conserved interactions among proteins or other molecules can provide strong evidence for coevolution across their evolutionary history. Diverse phylogenetic methods have been applied to identify potential coevolutionary relationships. In most cases, these methods minimally require comparisons of orthologous sequences and appropriate controls to separate effects of selection from the overall evolutionary relationships. In vertebrates, androgen receptor (AR) and cytochrome p450 aromatase (CYP19) share an affinity for androgenic steroids, which serve as receptor ligands and enzyme substrates. In a recent study, Tiwary and Li (2009) reported that AR and CYP19 displayed a signature of ancient and conserved interactions throughout all of the Eumetazoa (i.e., cnidarians, protostomes, and deuterostomes). Because these findings conflicted with a number of previous studies, we reanalyzed the data set used by Tiwary and Li. First, our analyses demonstrate that the invertebrate genes used in the previous analysis are not orthologous sequences, but instead represent a diverse set of nuclear receptors and cytochrome p450 enzymes with no confirmed or hypothesized relationships with androgens. Second, we show that (1) their analytical approach, which measures correlations in evolutionary distances between proteins, potentially led to spurious significant relationships due simply to conserved domains and (2) control comparisons provide positive evidence for a strong influence of evolutionary history. We discuss how corrections to this method and analysis of key taxa (e.g., duplications in the teleost fish and suiform lineages) can inform investigations of the coevolutionary relationships between androgen receptor and aromatase.
Current directions and future perspectives from the third Nematostella research conference

( 2014-06) Tarrant, Ann M. ; Gilmore, Thomas D. ; Reitzel, Adam M. ; Levy, Oren ; Technau, Ulrich ; Martindale, Mark Q.

The third Nematostella vectensis Research Conference took place in December 2013 in Eilat, Israel, as a satellite to the 8th International Conference on Coelenterate Biology. The starlet sea anemone, Nematostella vectensis, has emerged as a powerful cnidarian model, in large part due to the extensive genomic and transcriptomic resources and molecular approaches that are becoming available for Nematostella, which were the focus of several presentations. In addition, research was presented highlighting the broader utility of this species for studies of development, circadian rhythms, signal transduction, and gene–environment interactions.
Daily cycle in oxygen consumption by the sea anemone Nematostella vectensis Stephenson

(The Company of Biologists, 2016-01-15) Maas, Amy E. ; Jones, Ian T. ; Reitzel, Adam M. ; Tarrant, Ann M.

In bilaterian animals, the circadian clock is intimately involved in regulating energetic metabolism. Although cnidarians exhibit diel behavioral rhythms including cycles in locomotor activity, tentacle extension and spawning, daily cycles in cnidarian metabolism have not been described. To explore a possible circadian metabolic cycle, we maintained the anemone Nematostella vectensis in a 12 h light/dark cycle, a reversed light cycle, or in constant darkness. Oxygen consumption rates were measured at intervals using an optical oxygen meter. Respiration rates responded to entrainment with higher rates during light periods. During a second experiment with higher temporal resolution, respiration rates peaked late in the light period. The diel pattern could be detected after six days in constant darkness. Together, our results suggest that respiration rates in Nematostella exhibit a daily cycle that may be under circadian control and that the cycle in respiration rate is not driven by the previously described nocturnal increase in locomotor activity in this species.
Genomic survey of candidate stress-response genes in the estuarine anemone Nematostella vectensis

(Marine Biological Laboratory, 2008-06) Reitzel, Adam M. ; Sullivan, James C. ; Traylor-Knowles, Nikki ; Finnerty, John R.

Salt marshes are challenging habitats due to natural variability in key environmental parameters including temperature, salinity, ultraviolet light, oxygen, sulfides, and reactive oxygen species. Compounding this natural variation, salt marshes are often heavily impacted by anthropogenic insults including eutrophication, toxic contamination, and coastal development that alter tidal and freshwater inputs. Commensurate with this environmental variability, estuarine animals generally exhibit broader physiological tolerances than freshwater, marine, or terrestrial species. One factor that determines an organism's physiological tolerance is its ability to upregulate "stress-response genes" in reaction to particular stressors. Comparative studies on diverse organisms have identified a number of evolutionarily conserved genes involved in responding to abiotic and biotic stressors. We used homology-based scans to survey the sequenced genome of Nematostella vectensis, the starlet sea anemone, an estuarine specialist, to identify genes involved in the response to three kinds of insult—physiochemical insults, pathogens, and injury. Many components of the stress-response networks identified in triploblastic animals have clear orthologs in the sea anemone, meaning that they must predate the cnidarian-triploblast split (e.g., xenobiotic receptors, biotransformative genes, ATP-dependent transporters, and genes involved in responding to reactive oxygen species, toxic metals, osmotic shock, thermal stress, pathogen exposure, and wounding). However, in some instances, stress-response genes known from triploblasts appear to be absent from the Nematostella genome (e.g., many metal-complexing genes). This is the first comprehensive examination of the genomic stress-response repertoire of an estuarine animal and a member of the phylum Cnidaria. The molecular markers of stress response identified in Nematostella may prove useful in monitoring estuary health and evaluating coastal conservation efforts. These data may also inform conservation efforts on other cnidarians, such as the reef-building corals.
Circadian clocks in the cnidaria : environmental entrainment, molecular regulation, and organismal outputs

( 2013-03-26) Reitzel, Adam M. ; Tarrant, Ann M. ; Levy, Oren

The circadian clock is a molecular network that translates predictable environmental signals, such as light levels, into organismal responses, including behavior and physiology. Regular oscillations of the molecular components of the clock enable individuals to anticipate regularly fluctuating environmental conditions. Cnidarians play important roles in benthic and pelagic marine environments, and also occupy a key evolutionary position as the likely sister group to the bilaterians. Together, these attributes make members of this phylum attractive as models for testing hypotheses on role for circadian clocks in regulating behavior, physiology, and reproduction as well as those regarding the deep evolutionary conservation of circadian regulatory pathways in animal evolution. Here, we review and synthesize the field of cnidarian circadian biology by discussing the diverse effects of daily light cycles on cnidarians, summarizing the molecular evidence for the conservation of a bilaterian-like circadian clock in anthozoan cnidarians, and presenting new empirical data supporting the presence of a conserved feed-forward loop in the starlet sea anemone, Nematostella vectensis. Furthermore, we discuss critical gaps in our current knowledge about the cnidarian clock, including the functions directly regulated by the clock and the precise molecular interactions that drive the oscillating gene-expression patterns. We conclude that the field of cnidarian circadian biology is moving rapidly toward linking molecular mechanisms with physiology and behavior.
Heat shock protein expression during stress and diapause in the marine copepod Calanus finmarchicus

( 2011-03) Aruda, Amalia M. ; Baumgartner, Mark F. ; Reitzel, Adam M. ; Tarrant, Ann M.

Calanoid copepods, such as Calanus finmarchicus, are a key component of marine food webs. C. finmarchicus undergoes a facultative diapause during juvenile development, which profoundly affects their seasonal distribution and availability to their predators. The current ignorance of how copepod diapause is regulated limits understanding of copepod population dynamics, distribution, and ecosystem interactions. Heat shock proteins (Hsps) are a superfamily of molecular chaperones characteristically upregulated in response to stress conditions and frequently associated with diapause in other taxa. In this study, 8 heat shock proteins were identified in C. finmarchicus C5 copepodids (Hsp21, Hsp22, p26, Hsp90, and 4 forms of Hsp70), and expression of these transcripts was characterized in response to handling stress and in association with diapause. Hsp21, Hsp22, and Hsp70A (cytosolic subfamily) were induced by handling stress. Expression of Hsp70A was also elevated in shallow active copepodids relative to deep diapausing copepodids, which may reflect induction of this gene by varied stressors in active animals. In contrast, expression of Hsp22 was elevated in deep diapausing animals; Hsp22 may play a role both in short-term stress responses and in protecting proteins from degradation during diapause. Expression of most of the Hsps examined did not vary in response to diapause, perhaps because the diapause of C. finmarchicus is not associated with the extreme environmental conditions (e.g., freezing, desiccation) experienced by many other taxa, such as overwintering insects or Artemia cysts.
Steroid metabolism in cnidarians : insights from Nematostella vectensis

( 2008-09-26) Tarrant, Ann M. ; Reitzel, Adam M. ; Blomquist, Charles H. ; Haller, Ferdinand ; Tokarz, Janina ; Adamski, Jerzy

Cnidarians occupy a key evolutionary position as a sister group to bilaterian animals. While cnidarians contain a diverse complement of steroids, sterols, and other lipid metabolites, relatively little is known of the endogenous steroid metabolism or function in cnidarian tissues. Incubations of cnidarian tissues with steroid substrates have indicated the presence of steroid metabolizing enzymes, particularly enzymes with 17β-hydroxysteroid dehydrogenase (17β-HSD) activity. Through analysis of the genome of the starlet sea anemone, Nematostella vectensis, we identified a suite of genes in the short chain dehydrogenase/reductase (SDR) superfamily including homologs of genes that metabolize steroids in other animals. A more detailed analysis of Hsd17b4 revealed complex evolutionary relationships, apparent intron loss in several taxa, and predominantly adult expression in N. vectensis. Due to its ease of culture and available molecular tools N. vectensis is an excellent model for investigation of cnidarian steroid metabolism and gene function.
Convergent evolution of sodium ion selectivity in metazoan neuronal signaling

(Cell Press, 2012-08-30) Barzilai, Maya Gur ; Reitzel, Adam M. ; Kraus, Johanna E. M. ; Gordon, Dalia ; Technau, Ulrich ; Gurevitz, Michael ; Moran, Yehu

Ion selectivity of metazoan voltage-gated Na+ channels is critical for neuronal signaling and has long been attributed to a ring of four conserved amino acids that constitute the ion selectivity filter (SF) at the channel pore. Yet, in addition to channels with a preference for Ca2+ ions, the expression and characterization of Na+ channel homologs from the sea anemone Nematostella vectensis, a member of the early-branching metazoan phylum Cnidaria, revealed a sodium-selective channel bearing a noncanonical SF. Mutagenesis and physiological assays suggest that pore elements additional to the SF determine the preference for Na+ in this channel. Phylogenetic analysis assigns the Nematostella Na+-selective channel to a channel group unique to Cnidaria, which diverged >540 million years ago from Ca2+-conducting Na+ channel homologs. The identification of Cnidarian Na+-selective ion channels distinct from the channels of bilaterian animals indicates that selectivity for Na+ in neuronal signaling emerged independently in these two animal lineages.
Larvae of deep-sea invertebrates harbor low-diversity bacterial communities

(University of Chicago Press, 2021-07-28) Carrier, Tyler ; Beaulieu, Stace E. ; Mills, Susan W. ; Mullineaux, Lauren S. ; Reitzel, Adam M.

Microbial symbionts are a common life-history character of marine invertebrates and their developmental stages. Communities of bacteria that associate with the eggs, embryos, and larvae of coastal marine invertebrates tend to be species specific and correlate with aspects of host biology and ecology. The richness of bacteria associated with the developmental stages of coastal marine invertebrates spans four orders of magnitude, from single mutualists to thousands of unique taxa. This understanding stems predominately from the developmental stages of coastal species. If they are broadly representative of marine invertebrates, then we may expect deep-sea species to associate with bacterial communities that are similar in diversity. To test this, we used amplicon sequencing to profile the bacterial communities of invertebrate larvae from multiple taxonomic groups (annelids, molluscs, crustaceans) collected from 2500 to 3670 m in depth in near-bottom waters near hydrothermal vents in 3 different regions of the Pacific Ocean (the East Pacific Rise, the Mariana Back-Arc, and the Pescadero Basin). We find that larvae of deep-sea invertebrates associate with low-diversity bacterial communities (~30 bacterial taxa) that lack specificity between taxonomic groups. The diversity of these communities is estimated to be ~7.9 times lower than that of coastal invertebrate larvae, but this result depends on the taxonomic group. Associating with a low-diversity community may imply that deep-sea invertebrate larvae do not have a strong reliance on a microbiome and that the hypothesized lack of symbiotic contributions would differ from expectations for larvae of coastal marine invertebrates.
Genetic variation at aryl hydrocarbon receptor (AHR) loci in populations of Atlantic killifish (Fundulus heteroclitus) inhabiting polluted and reference habitats

(BioMed Central, 2014-01-14) Reitzel, Adam M. ; Karchner, Sibel I. ; Franks, Diana G. ; Evans, Brad R. ; Nacci, Diane E. ; Champlin, Denise ; Vieira, Veronica M. ; Hahn, Mark E.

The non-migratory killifish Fundulus heteroclitus inhabits clean and polluted environments interspersed throughout its range along the Atlantic coast of North America. Several populations of this species have successfully adapted to environments contaminated with toxic aromatic hydrocarbon pollutants such as polychlorinated biphenyls (PCBs). Previous studies suggest that the mechanism of resistance to these and other “dioxin-like compounds” (DLCs) may involve reduced signaling through the aryl hydrocarbon receptor (AHR) pathway. Here we investigated gene diversity and evidence for positive selection at three AHR-related loci (AHR1, AHR2, AHRR) in F. heteroclitus by comparing alleles from seven locations ranging over 600 km along the northeastern US, including extremely polluted and reference estuaries, with a focus on New Bedford Harbor (MA, USA), a PCB Superfund site, and nearby reference sites. We identified 98 single nucleotide polymorphisms within three AHR-related loci among all populations, including synonymous and nonsynonymous substitutions. Haplotype distributions were spatially segregated and F-statistics suggested strong population genetic structure at these loci, consistent with previous studies showing strong population genetic structure at other F. heteroclitus loci. Genetic diversity at these three loci was not significantly different in contaminated sites as compared to reference sites. However, for AHR2 the New Bedford Harbor population had significant FST values in comparison to the nearest reference populations. Tests for positive selection revealed ten nonsynonymous polymorphisms in AHR1 and four in AHR2. Four nonsynonymous SNPs in AHR1 and three in AHR2 showed large differences in base frequency between New Bedford Harbor and its reference site. Tests for isolation-by-distance revealed evidence for non-neutral change at the AHR2 locus. Together, these data suggest that F. heteroclitus populations in reference and polluted sites have similar genetic diversity, providing no evidence for strong genetic bottlenecks for populations in polluted locations. However, the data provide evidence for genetic differentiation among sites, selection at specific nucleotides in AHR1 and AHR2, and specific AHR2 SNPs and haplotypes that are associated with the PCB-resistant phenotype in the New Bedford Harbor population. The results suggest that AHRs, and especially AHR2, may be important, recurring targets for selection in local adaptation to dioxin-like aromatic hydrocarbon contaminants.
Ultraviolet radiation significantly enhances the molecular response to dispersant and sweet crude oil exposure in Nematostella vectensis

( 2018-01-01) Tarrant, Ann M. ; Payton, Samantha L. ; Reitzel, Adam M. ; Porter, Danielle T. ; Jenny, Matthew J.

Estuarine organisms are subjected to combinations of anthropogenic and natural stressors, which together can reduce an organisms' ability to respond to either stress or can potentiate or synergize the cellular impacts for individual stressors. Nematostella vectensis (starlet sea anemone) is a useful model for investigating novel and evolutionarily conserved cellular and molecular responses to environmental stress. Using RNA-seq, we assessed global changes in gene expression in Nematostella in response to dispersant and/or sweet crude oil exposure alone or combined with ultraviolet radiation (UV). A total of 110 transcripts were differentially expressed by dispersant and/or crude oil exposure, primarily dominated by the down-regulation of 74 unique transcripts in the dispersant treatment. In contrast, UV exposure alone or combined with dispersant and/or oil resulted in the differential expression of 1133 transcripts, of which 436 were shared between all four treatment combinations. Most significant was the differential expression of 531 transcripts unique to one or more of the combined UV/chemical exposures. Main categories of genes affected by one or more of the treatments included enzymes involved in xenobiotic metabolism and transport, DNA repair enzymes, and general stress response genes conserved among vertebrates and invertebrates. However, the most interesting observation was the induction of several transcripts indicating de novo synthesis of mycosporine-like amino acids and other novel cellular antioxidants. Together, our data suggest that the toxicity of oil and/or dispersant and the complexity of the molecular response are significantly enhanced by UV exposure, which may co-occur for shallow water species like Nematostella.

Reitzel Adam M.

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