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ArticleA crude awakening: effects of crude oil on lipid metabolism in calanoid copepods terminating diapause(University of Chicago Press, 2019-10-04) Skottene, Elise ; Tarrant, Ann M. ; Olsen, Anders J. ; Altin, Dag ; Hansen, Bjørn Henrik ; Choquet, Marvin ; Olsen, Rolf Erik ; Jenssen, Bjørn M.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.
ArticleTranscriptional profiling of reproductive development, lipid storage and molting throughout the last juvenile stage of the marine copepod Calanus finmarchicus(BioMed Central, 2014-12-16) Tarrant, Ann M. ; Baumgartner, Mark F. ; Hansen, Bjørn Henrik ; Altin, Dag ; Nordtug, Trond ; Olsen, Anders J.Calanus finmarchicus, a highly abundant copepod that is an important primary consumer in North Atlantic ecosystems, has a flexible life history in which copepods in the last juvenile developmental stage (fifth copepodid, C5) may either delay maturation and enter diapause or molt directly into adults. The factors that regulate this developmental plasticity are poorly understood, and few tools have been developed to assess the physiological condition of individual copepods. We sampled a cultured population of C. finmarchicus copepods daily throughout the C5 stage and assessed molt stage progression, gonad development and lipid storage. We used high-throughput sequencing to identify genes that were differentially expressed during progression through the molt stage and then used qPCR to profile daily expression of individual genes. Based on expression profiles of twelve genes, samples were statistically clustered into three groups: (1) an early period occurring prior to separation of the cuticle from the epidermis (apolysis) when expression of genes associated with lipid synthesis and transport (FABP and ELOV) and two nuclear receptors (ERR and HR78) was highest, (2) a middle period of rapid change in both gene expression and physiological condition, including local minima and maxima in several nuclear receptors (FTZ-F1, HR38b, and EcR), and (3) a late period when gonads were differentiated and expression of genes associated with molting (Torso-like, HR38a) peaked. The ratio of Torso-like to HR38b strongly differentiated the early and late groups. This study provides the first dynamic profiles of gene expression anchored with morphological markers of lipid accumulation, development and gonad maturation throughout a copepod molt cycle. Transcriptomic profiling revealed significant changes over the molt cycle in genes with presumed roles in lipid synthesis, molt regulation and gonad development, suggestive of a coupling of these processes in Calanus finmarchicus. Finally, we identified gene expression profiles that strongly differentiate between early and late development within the C5 copepodid stage. We anticipate that these findings and continued development of robust gene expression biomarkers that distinguish between diapause preparation and continuous development will ultimately enable novel studies of the intrinsic and extrinsic factors that govern diapause initiation in Calanus finmarchicus.
ArticleLipid metabolism in Calanus finmarchicus is sensitive to variations in predation risk and food availability(Nature Research, 2020-12-18) Skottene, Elise ; Tarrant, Ann M. ; Altin, Dag ; Olsen, Rolf Erik ; Choquet, Marvin ; Kvile, Kristina ØieLate 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.
ArticleThe beta-oxidation pathway is downregulated during diapause termination in Calanus copepods(Nature Research, 2019-11-13) Skottene, Elise ; Tarrant, Ann M. ; Olsen, Anders J. ; Altin, Dag ; Østensen, Mari-Ann ; Hansen, Bjørn Henrik ; Choquet, Marvin ; Jenssen, Bjørn M. ; Olsen, Rolf ErikCalanus 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.