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  • 1
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    Ecology and physiology of dormancy in a changing world: introduction to a virtual symposium (2020)
    University of Chicago Press
    Details
    Publication Date: 2022-05-25
    Description: 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.
    Description: 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.
    Description: 2020-10-14
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 2
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    Chromatin dynamics enable transcriptional rhythms in the cnidarian Nematostella vectensis (2020)
    Public Library of Science
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Weizman, E. N., Tannenbaum, M., Tarrant, A. M., Hakim, O., & Levy, O. Chromatin dynamics enable transcriptional rhythms in the cnidarian Nematostella vectensis. Plos Genetics, 15(11), (2019): e1008397, doi: 10.1371/journal.pgen.1008397.
    Description: In animals, circadian rhythms are driven by oscillations in transcription, translation, and proteasomal degradation of highly conserved genes, resulting in diel cycles in the expression of numerous clock-regulated genes. Transcription is largely regulated through the binding of transcription factors to cis-regulatory elements within accessible regions of the chromatin. Chromatin remodeling is linked to circadian regulation in mammals, but it is unknown whether cycles in chromatin accessibility are a general feature of clock-regulated genes throughout evolution. To assess this, we applied an ATAC-seq approach using Nematostella vectensis, grown under two separate light regimes (light:dark (LD) and constant darkness (DD)). Based on previously identified N. vectensis circadian genes, our results show the coupling of chromatin accessibility and circadian transcription rhythmicity under LD conditions. Out of 180 known circadian genes, we were able to list 139 gene promoters that were highly accessible compared to common promoters. Furthermore, under LD conditions, we identified 259 active enhancers as opposed to 333 active enhancers under DD conditions, with 171 enhancers shared between the two treatments. The development of a highly reproducible ATAC-seq protocol integrated with published RNA-seq and ChIP-seq databases revealed the enrichment of transcription factor binding sites (such as C/EBP, homeobox, and MYB), which have not been previously associated with circadian signaling in cnidarians. These results provide new insight into the regulation of cnidarian circadian machinery. Broadly speaking, this supports the notion that the association between chromatin remodeling and circadian regulation arose early in animal evolution as reflected in this non-bilaterian lineage.
    Description: The research leading for this paper was funded by the Moore Foundation (https://www.moore.org), “Unwinding the Circadian Clock in a Sea Anemone” (Grant #4598) to A.T and O.L. The founders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
    Repository Name: Woods Hole Open Access Server
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  • 3
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    A crude awakening: effects of crude oil on lipid metabolism in calanoid copepods terminating diapause (2020)
    University of Chicago Press
    Details
    Publication Date: 2022-05-26
    Description: 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): 90-110, doi: 10.1086/705234.
    Description: Calanus finmarchicus and Calanus glacialis are keystone zooplankton species in North Atlantic and Arctic marine ecosystems because they form a link in the trophic transfer of nutritious lipids from phytoplankton to predators on higher trophic levels. These calanoid copepods spend several months of the year in deep waters in a dormant state called diapause, after which they emerge in surface waters to feed and reproduce during the spring phytoplankton bloom. Disruption of diapause timing could have dramatic consequences for marine ecosystems. In the present study, Calanus C5 copepodites were collected in a Norwegian fjord during diapause and were subsequently experimentally exposed to the water-soluble fraction of a naphthenic North Sea crude oil during diapause termination. The copepods were sampled repeatedly while progressing toward adulthood and were analyzed for utilization of lipid stores and for differential expression of genes involved in lipid metabolism. Our results indicate that water-soluble fraction exposure led to a temporary pause in lipid catabolism, suggested by (i) slower utilization of lipid stores in water-soluble fraction-exposed C5 copepodites and (ii) more genes in the β-oxidation pathway being downregulated in water-soluble fraction-exposed C5 copepodites than in the control C5 copepodites. Because lipid content and/or composition may be an important trigger for termination of diapause, our results imply that the timing of diapause termination and subsequent migration to the surface may be delayed if copepods are exposed to oil pollution during diapause or diapause termination. This delay could have detrimental effects on ecosystem dynamics.
    Description: We thank the Department of Biology at the Norwegian University of Science and Technology (NTNU) for additional funding for ES’s stay at Woods Hole Oceanographic Institution (WHOI); Christoffer H. Hilde for help in the field and in the lab; Siv Anina Etter, Øystein Leiknes, Sofia Soloperto, and Clara P. Igisch for help with the fieldwork; Justyna Świeżak, Mari-Ann Østensen, and Signe D. Løvmo for experimental assistance; and Hanny Rivera for help with bioinformatic analyses at WHOI. The RNA-sequencing work was provided by the Genomics Core Facility (GCF). The GCF is funded by the Faculty of Medicine and Health Sciences at NTNU and the Central Norway Regional Health Authority. AMT was funded by the National Science Foundation (award no. OPP-1746087).
    Description: 2020-10-04
    Repository Name: Woods Hole Open Access Server
    Type: Article
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  • 4
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    Lipid metabolism in Calanus finmarchicus is sensitive to variations in predation risk and food availability (2021)
    Nature Research
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Skottene, E., Tarrant, A. M., Altin, D., Olsen, R. E., Choquet, M., & Kvile, K. O. Lipid metabolism in Calanus finmarchicus is sensitive to variations in predation risk and food availability. Scientific Reports, 10(1),(2020): 22322, https://doi.org/10.1038/s41598-020-79165-6.
    Description: Late developmental stages of the marine copepods in the genus Calanus can spend extended periods in a dormant stage (diapause) that is preceded by the accumulation of large lipid stores. We assessed how lipid metabolism during development from the C4 stage to adult is altered in response to predation risk and varying food availability, to ultimately understand more of the metabolic processes during development in Calanus copepods. We used RNA sequencing to assess if perceived predation risk in combination with varied food availability affects expression of genes associated with lipid metabolism and diapause preparation in C. finmarchicus. The lipid metabolism response to predation risk differed depending on food availability, time and life stage. Predation risk caused upregulation of lipid catabolism with high food, and downregulation with low food. Under low food conditions, predation risk disrupted lipid accumulation. The copepods showed no clear signs of diapause preparation, supporting earlier observations of the importance of multiple environmental cues in inducing diapause in C. finmarchicus. This study demonstrates that lipid metabolism is a sensitive endpoint for the interacting environmental effects of predation pressure and food availability. As diapause may be controlled by lipid accumulation, our findings may contribute towards understanding processes that can ultimately influence diapause timing.
    Description: ES was funded by the Department of Biology, Norwegian University of Science and Technology. Support for AMT was provided by the National Science Foundation (NSF) OPP-1746087. KØK was funded by VISTA—a basic research program in collaboration between The Norwegian Academy of Science and Letters, and Equinor. The RNA seq work was provided by the Genomics Core Facility (GCF). GCF is funded by the Faculty of Medicine and Health Sciences at NTNU and Central Norway Regional Health Authority. The authors thank Lotte Thommesen for help conducting the experiment, Mari-Ann Østensen for performing RNA extraction with ES and preparing cDNA libraries for Illumina RNAseq, and the EMBRC-ERIC Laboratory for Low Level Trophic Interactions at NTNU SeaLab for access to the Calanus finmarchicus culture.
    Repository Name: Woods Hole Open Access Server
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  • 5
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    Plasticity in parental effects confers rapid larval thermal tolerance in the estuarine anemone Nematostella vectensis (2021)
    The Company of Biologists
    Details
    Publication Date: 2022-05-27
    Description: Author Posting. © Company of Biologists, 2021. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 224(5), (2021): jeb236745, https://doi.org/10.1242/jeb.236745.
    Description: Parental effects can prepare offspring for different environments and facilitate survival across generations. We exposed parental populations of the estuarine anemone, Nematostella vectensis, from Massachusetts to elevated temperatures and quantified larval mortality across a temperature gradient. We found that parental exposure to elevated temperatures resulted in a consistent increase in larval thermal tolerance, as measured by the temperature at which 50% of larvae die (LT50), with a mean increase in LT50 of 0.3°C. Larvae from subsequent spawns returned to baseline thermal thresholds when parents were returned to normal temperatures, indicating plasticity in these parental effects. Histological analyses of gametogenesis in females suggested that these dynamic shifts in larval thermal tolerance may be facilitated by maternal effects in non-overlapping gametic cohorts. We also compared larvae from North Carolina (a genetically distinct population with higher baseline thermal tolerance) and Massachusetts parents, and observed that larvae from heat-exposed Massachusetts parents had thermal thresholds comparable to those of larvae from unexposed North Carolina parents. North Carolina parents also increased larval thermal tolerance under the same high-temperature regime, suggesting that plasticity in parental effects is an inherent trait for N. vectensis. Overall, we find that larval thermal tolerance in N. vectensis shows a strong genetic basis and can be modulated by parental effects. Further understanding of the mechanisms behind these shifts can elucidate the fate of thermally sensitive ectotherms in a rapidly changing thermal environment.
    Description: The Betty and Gordon Moore Foundation [4598 to A.M.T.] provided funding for this work. Additional funding for H.E.R. was provided by the National Defense Science and Engineering Graduate Fellowship Program, Gates Millennium Scholars Program, the Martin Family Fellowship for Sustainability and the American Association of University Women. C.-Y.C. and M.C.G. were funded by the Stowers Institute for Medical Research.
    Description: 2022-03-11
    Keywords: Acclimation ; Cnidaria ; LT50 ; Maternal effects ; Paternal effects ; Thermal limits
    Repository Name: Woods Hole Open Access Server
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  • 6
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    Chromatin dynamics and gene expression response to heat exposure in field-conditioned versus laboratory-cultured Nematostella vectensis (2021)
    MDPI
    Details
    Publication Date: 2022-05-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Weizman, E., Rinsky, M., Simon-Blecher, N., Lampert-Karako, S., Yaron, O., Tarrant, A. M., & Levy, O. Chromatin dynamics and gene expression response to heat exposure in field-conditioned versus laboratory-cultured Nematostella vectensis. International Journal of Molecular Sciences, 22(14), (2021): 7454, https://doi.org/10.3390/ijms22147454.
    Description: Organisms’ survival is associated with the ability to respond to natural or anthropogenic environmental stressors. Frequently, these responses involve changes in gene regulation and expression, consequently altering physiology, development, or behavior. Here, we present modifications in response to heat exposure that mimics extreme summertime field conditions of lab-cultured and field-conditioned Nematostella vectensis. Using ATAC-seq and RNA-seq data, we found that field-conditioned animals had a more concentrated reaction to short-term thermal stress, expressed as enrichment of the DNA repair mechanism pathway. By contrast, lab animals had a more diffuse reaction that involved a larger number of differentially expressed genes and enriched pathways, including amino acid metabolism. Our results demonstrate that pre-conditioning affects the ability to respond efficiently to heat exposure in terms of both chromatin accessibility and gene expression and reinforces the importance of experimentally addressing ecological questions in the field.
    Keywords: ATAC-seq ; cnidarian ; RNA-seq ; stress response ; pre-conditioning ; thermal
    Repository Name: Woods Hole Open Access Server
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  • 7
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    Diapause vs. reproductive programs: transcriptional phenotypes in a keystone copepod (2021)
    Nature Research
    Details
    Publication Date: 2022-05-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Lenz, P. H., Roncalli, V., Cieslak, M. C., Tarrant, A. M., Castelfranco, A. M., & Hartline, D. K. Diapause vs. reproductive programs: transcriptional phenotypes in a keystone copepod. Communications Biology, 4(1), (2021): 426, https://doi.org/10.1038/s42003-021-01946-0.
    Description: Many arthropods undergo a seasonal dormancy termed “diapause” to optimize timing of reproduction in highly seasonal environments. In the North Atlantic, the copepod Calanus finmarchicus completes one to three generations annually with some individuals maturing into adults, while others interrupt their development to enter diapause. It is unknown which, why and when individuals enter the diapause program. Transcriptomic data from copepods on known programs were analyzed using dimensionality reduction of gene expression and functional analyses to identify program-specific genes and biological processes. These analyses elucidated physiological differences and established protocols that distinguish between programs. Differences in gene expression were associated with maturation of individuals on the reproductive program, while those on the diapause program showed little change over time. Only two of six filters effectively separated copepods by developmental program. The first one included all genes annotated to RNA metabolism and this was confirmed using differential gene expression analysis. The second filter identified 54 differentially expressed genes that were consistently up-regulated in individuals on the diapause program in comparison with those on the reproductive program. Annotated to oogenesis, RNA metabolism and fatty acid biosynthesis, these genes are both indicators for diapause preparation and good candidates for functional studies.
    Description: This work was supported by National Science Foundation Grants (NSF) OCE-1459235 and OCE-1756767 to P.H.L., D.K.H. and AE Christie and OPP-1746087 to A.M.T.
    Repository Name: Woods Hole Open Access Server
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  • 8
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    Diel metabolic patterns in a migratory oceanic copepod (2021)
    Elsevier
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    Publication Date: 2022-05-27
    Description: © The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Tarrant, A. M., McNamara-Bordewick, N., Blanco-Bercial, L., Miccoli, A., & Maas, A. E. Diel metabolic patterns in a migratory oceanic copepod. Journal of Experimental Marine Biology and Ecology, 545, (2021): 151643, https://doi.org/10.1016/j.jembe.2021.151643.
    Description: Diel vertical migration of zooplankton profoundly impacts the transport of nutrients and carbon through the water column. Despite the acknowledged importance of this active flux to ocean biogeochemistry, these contributions remain poorly constrained, in part because daily variations in metabolic rates are not considered or are modeled as simple functions of temperature. To address this uncertainty, we sampled the subtropical copepod Pleuromamma xiphias at 4- to 7-h intervals throughout the daily migration and measured rates of oxygen consumption, ammonium excretion, fecal pellet production and metabolic enzyme activity. No significant patterns were detected in rates of oxygen consumption or ammonium excretion for freshly caught animals over the diel cycle. Fecal pellet production was highest during mid-night, consistent with several hours of feeding near the surface. Surface feeding resulted in fecal pellet production at depth in the morning, providing direct evidence that active flux of particulate organic carbon occurs in this region. Electron transport system activity was highest during the afternoon, contrary to our prediction of reduced daytime metabolism. Activity of both glutamate dehydrogenase and citrate synthase increased during early night, reflecting higher capacity for excretion and aerobic respiration, respectively. Overall, these results show that activities of metabolic enzymes vary during diel vertical migration. The surprising observation of elevated afternoon enzyme activity coupled with daytime fecal pellet and ammonium production suggests that additional characterization of the daytime activity of migratory zooplankton is warranted.
    Description: This work was supported by the National Science Foundation [Grants OCE-1829318 to AEMand LBB, and OCE-1829378 to AMT]. Support for NM-B was provided by the Woods Hole Oceanographic Institution's Summer Student Fellows Program.
    Keywords: Active flux ; DVM ; Excretion ; Fecal pellets ; Respiration
    Repository Name: Woods Hole Open Access Server
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  • 9
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    The beta-oxidation pathway is downregulated during diapause termination in Calanus copepods (2020)
    Nature Research
    Details
    Publication Date: 2022-05-26
    Description: © The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Skottene, E., Tarrant, A. M., Olsen, A. J., Altin, D., Ostensen, M., Hansen, B. H., Choquet, M., Jenssen, B. M., & Olsen, R. E. R. The beta-oxidation pathway is downregulated during diapause termination in Calanus copepods. Scientific Reports, 9, (2019): 16686, doi: 10.1038/s41598-019-53032-5.
    Description: Calanus copepods are keystone species in marine ecosystems, mainly due to their high lipid content, which is a nutritious food source for e.g. juvenile fish. Accumulated lipids are catabolized to meet energy requirements during dormancy (diapause), which occurs during the last copepodite stage (C5). The current knowledge of lipid degradation pathways during diapause termination is limited. We characterized changes in lipid fullness and generated transcriptional profiles in C5s during termination of diapause and progression towards adulthood. Lipid fullness of C5s declined linearly during developmental progression, but more β-oxidation genes were upregulated in early C5s compared to late C5s and adults. We identified four possible master regulators of energy metabolism, which all were generally upregulated in early C5s, compared to late C5s and adults. We discovered that one of two enzymes in the carnitine shuttle is absent from the calanoid copepod lineage. Based on the geographical location of the sampling site, the field-samples were initially presumed to consist of C. finmarchicus. However, the identification of C. glacialis in some samples underlines the need for performing molecular analyses to reliably identify Calanus species. Our findings contributes to a better understanding of molecular events occurring during diapause and diapause termination in calanoid copepods.
    Description: The authors wish to thank Dept. of Biology at Norwegian University of Science and Technology (NTNU) for additional funding for Elise Skottene´s stay at Woods Hole Oceanographic Institution (WHOI), Christoffer H. Hilde for help in the field and in the lab, Siv Anina Etter, Øystein Leiknes, Sofia Soloperto and Clara Igisch for help with the field work, Justyna Świeżak and Signe D. Løvmo for experimental assistance, Hanny Rivera for help with bioinformatic analyses at WHOI. The RNA seq work was provided by the Genomics Core Facility (GCF). GCF is funded by the Faculty of Medicine and Health Sciences at NTNU and Central Norway Regional Health Authority. Ann M. Tarrant was funded by the National Science Foundation (Award Number OPP-1746087).
    Repository Name: Woods Hole Open Access Server
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  • 10
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    Organismal physiological metrics from time series experiments on samples collected on R/V Atlantic Explorer cruise AE1910 in May 2019 (2021)
    Biological and Chemical Oceanography Data Management Office (BCO-DMO). Contact: bco-dmo-data@whoi.edu
    Details
    Publication Date: 2022-05-26
    Description: Dataset: AE1910 Organismal Physiology
    Description: Organismal physiological metrics from time series experiments on samples collected on R/V Atlantic Explorer cruise AE1910 in May 2019. For a complete list of measurements, refer to the full dataset description in the supplemental file 'Dataset_description.pdf'. The most current version of this dataset is available at: https://www.bco-dmo.org/dataset/829777
    Description: NSF Division of Ocean Sciences (NSF OCE) OCE-1829318, NSF Division of Ocean Sciences (NSF OCE) OCE-1829378
    Repository Name: Woods Hole Open Access Server
    Type: Dataset
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