Ecology and physiology of dormancy in a changing world: introduction to a virtual symposium

Author Posting. © University of Chicago, 2019. This article is posted here by permission of University of Chicago for personal use, not for redistribution. The definitive version was published in Biological Bulletin 237(2), (2019): 73-75, doi: 10.1086/706563.Dormancy is a widespread strategy used by diverse animal groups to persist through adverse environmental conditions, spread reproductive risk, and optimize seasonal phenology. Dormancy is an overarching term that refers to a reduction in metabolism, growth, and development; and different types of dormancy have been defined. Quiescence is directly initiated and terminated in response to environmental conditions, while diapause requires a preparatory phase that usually anticipates the onset of unfavorable conditions and also requires some minimum dormancy period (refractory phase) prior to termination. Dormancy is a fundamental feature of seasonal food web dynamics. Zooplankton populations can rapidly boom as individuals emerge from dormancy to feed on ephemeral algal blooms. Such productivity is critical to sustaining higher predators and supporting fisheries, particularly the growth of larval fish. Dormancy traits undergo selective pressure as zooplankton optimize developmental timing to maximize food availability and minimize predation pressure. As oceans warm and environments change, the relationship between dormancy cues, such as temperature and photoperiod, can shift, with as yet unknown effects on the timing of dormancy and resulting ecosystem dynamics. Future ecosystem dynamics are difficult to predict in part because we do not fully understand the cues that regulate the initiation or termination of dormancy, or how dormancy traits may change over time through acclimation and adaptation.2020-10-1

Introduction to the symposium—Keeping Time During Evolution : Conservation and Innovation of the Circadian Clock

Author Posting. © The Author(s), 2013. This is the author's version of the work. It is posted here by permission of Oxford University Press for personal use, not for redistribution. The definitive version was published in Integrative and Comparative Biology 53 (2013): 89-92, doi: 10.1093/icb/ict062.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.The symposium “Keeping Time During Animal Evolution: Conservation and Innovation of the Circadian Clock” was generously supported by the Society of Integrative and Comparative Biology and by Award 1239607 from the Integrative Organismal Systems Program at the National Science Foundation.2014-05-2

Nuclear receptor complement of the cnidarian Nematostella vectensis : phylogenetic relationships and developmental expression patterns

© 2009 Reitzel and Tarrant. This is an open-access article distributed under the terms of the Creative Commons Attribution License. The definitive version was published in BMC Evolutionary Biology 9 (2009): 230, doi:10.1186/1471-2148-9-230.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.We are grateful for financial support from the Woods Hole Oceanographic Institution (WHOI) through the Tropical Research Initiative, the Ocean Life Institute (AMT), the Academic Programs Office, and to the Beacon Institute for Rivers and Estuaries (AMR)

Vibrio elicits targeted transcriptional responses from copepod hosts

Author Posting. © The Author(s), 2016. This is the author's version of the work. It is posted here by permission of Federation of European Microbiological Societies for personal use, not for redistribution. The definitive version was published in FEMS Microbiology Ecology 92 (2016): fiw072, doi:10.1093/femsec/fiw072.Copepods are abundant crustaceans that harbor diverse bacterial communities, yet the nature of their interactions with microbiota are poorly understood . Here, we report that Vibrio elicits targeted transcriptional responses in the estuarine copepod Eurytemora affinis. We pre-treated E. affinis with an antibiotic-cocktail and exposed them to either a zooplankton specialist (Vibrio sp. F10 9ZB36) or a free-living species (V. ordalii 12B09) for 24 hours. We then identified via RNA-Seq a total of 78 genes that were differentially expressed following Vibrio exposure, including homologs of C-type lectins, chitin-binding proteins and saposins. The response differed between the two Vibrio treatments, with the greatest changes elicited upon inoculation with V. sp. F10. We suggest that these differentially regulated genes play important roles in cuticle integrity, the innate immune response, and general stress responses, and that their expression may enable E. affinis to recognize and regulate symbiotic vibrios. We further report that V. sp. F10 culturability is specifically altered upon colonization of E. affinis. These findings suggest that rather than acting as passive environmental vectors, copepods discriminately interact with vibrios, which may ultimately impact the abundance and activity of copepod-associated bacteria.2017-04-0

Light entrained rhythmic gene expression in the sea anemone Nematostella vectensis : the evolution of the animal circadian clock

© The Authors, 2010. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS One 5 (2010): e12805, doi:10.1371/journal.pone.0012805.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.The project described was supported by Award Number F32HD062178 to AMR from the Eunice Kennedy Shriver National Institute of Child Health and Human Development and the Tropical Research Initiative of the Woods Hole Oceanographic Institution

Circadian clocks in the cnidaria : environmental entrainment, molecular regulation, and organismal outputs

Author Posting. © The Author(s), 2013. This is the author's version of the work. It is posted here by permission of Oxford University Press for personal use, not for redistribution. The definitive version was published in Integrative and Comparative Biology 53 (2013): 118-130, doi:10.1093/icb/ict024.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.This work was supported by the United States – Israel Binational Science Foundation award 2011187 (AMT and OL), the National Institutes of Health / National Institute of Child Health and Human Development award HD062178 (AMR), and generous funding from the University of North Carolina at Charlotte (AMR).2014-04-2

Transcriptome-wide analysis of the response of the thecosome pteropod Clio pyramidata to short-term CO2 exposure

Author Posting. © The Author(s), 2015. This is the author's version of the work. It is posted here by permission of Elsevier for personal use, not for redistribution. The definitive version was published in Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 16 (2015): 1-9, doi:10.1016/j.cbd.2015.06.002.Thecosome pteropods, a group of calcifying holoplanktonic molluscs, have recently become a research focus due to their potential sensitivity to increased levels of anthropogenic dissolved CO2 in seawater and the accompanying ocean acidification. Some populations, however, already experience high CO2 in their natural distribution during diel vertical migrations. To achieve a better understanding of the mechanisms of pteropod calcification and physiological response to this sort of short duration CO2 exposure, we characterized the gene complement of Clio pyramidata, a cosmopolitan diel migratory thecosome, and investigated its transcriptomic response to experimentally manipulated CO2 conditions. Individuals were sampled from the Northwest Atlantic in the fall of 2011 and exposed to ambient conditions (~380 ppm) and elevated CO2 (~800 ppm, similar to levels experienced during a diel vertical migration) for ~10 hrs. Following this exposure the respiration rate of the individuals was measured. We then performed RNA-seq analysis, assembled the C. pyramidata transcriptome de novo, annotated the genes, and assessed the differential gene expression patterns in response to exposure to elevated CO2. Within the transcriptome, we identified homologs of genes with known roles in biomineralization in other molluscs, including perlucin, calmodulin, dermatopontin, calponin, and chitin synthases. Respiration rate was not affected by short-term exposure to CO2. Gene expression varied greatly among individuals, and comparison between treatments indicated that C. pyramidata down-regulated a small number of genes associated with aerobic metabolism and up-regulated genes that may be associated with biomineralization, particularly collagens and C- type lectins. These results provide initial insight into the effects of short term CO2 exposure on these important planktonic open-ocean calcifiers, pairing respiration rate and the gene expression level of response, and reveal candidate genes for future ecophysiological, biomaterial and phylogenetic studies.The Extreme Science and Engineering Discovery Environment (XSEDE), which is supported by National Science Foundation grant number OCI-1053575, provided computing resources for the differential expression analysis. This material is based upon work supported by the National Science Foundation’s Ocean Acidification Program under grant number OCE-1041068 (to Lawson, Wang, Lavery, and Wiebe), the Woods Hole Oceanographic Institution’s Access to the Sea program (to Tarrant, Maas and Lawson) and the WHOI postdoctoral scholarship program (to Maas)

Altered gene expression associated with epizootic shell disease in the American lobster, Homarus americanus

Author Posting. © The Author(s), 2010. This is the author's version of the work. It is posted here by permission of Elsevier B.V. for personal use, not for redistribution. The definitive version was published in Fish & Shellfish Immunology 29 (2010): 1003-1009, doi:10.1016/j.fsi.2010.08.008.Epizootic shell disease is a poorly understood condition that has significantly affected the American lobster fishery in New England (northeastern US) since the 1990s. Here we present the results of a study to identify changes in gene expression in lobsters exhibiting symptoms of epizootic shell disease. Suppressive subtractive hybridization (SSH) was used to compare gene expression between cDNA pools from diseased (symptomatic) and apparently healthy (asymptomatic) lobsters. Subsequently, quantitative real‐time polymerase chain reaction (qPCR) was used to measure expression of nine genes that were differentially‐expressed in the SSH analysis, in seven tissues (muscle, gill, heart, hepatopancreas, brain, branchiostegite, gonad) dissected from individual symptomatic and asymptomatic lobsters. Expression of arginine kinase (involved in cellular energetics) was significantly decreased in muscle of symptomatic lobsters. Expression of hemocyanin (a respiratory hemolymph protein involved in oxygen transport) was highest in hepatopancreas and showed highly variable expression with a trend toward higher expression in asymptomatic individuals. α2‐Macroglobulin (involved in the innate immune system) was most highly expressed in the ovary, particularly of symptomatic lobsters. The ESTs produced through this study add to the fledgling field of crustacean genomics and revealed three genes that could be further evaluated in lobsters of varying shell disease severity, molt stage, and reproductive condition, for possible implication in epizootic shell disease.Funding for this research was provided by the National Marine Fisheries Service as the ‘New England Lobster Research Initiative: Lobster Shell Disease’ under NOAA grant NA06NMF4720100 to the University of Rhode Island Fisheries Center

Heat shock protein expression during stress and diapause in the marine copepod Calanus finmarchicus

Author Posting. © The Author(s), 2011. This is the author's version of the work. It is posted here by permission of Elsevier B.V. for personal use, not for redistribution. The definitive version was published in Journal of Insect Physiology 57 (2011): 665-675, doi:10.1016/j.jinsphys.2011.03.007.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.Funding for AMA was provided by the WHOI Summer Student Fellowship Program and an EPA STAR fellowship