A Circadian Clock in Antarctic Krill: An Endogenous Timing System Governs Metabolic Output Rhythms in the Euphausid Species Euphausia superba

PLOS ONE, Oct 2011

Antarctic krill, Euphausia superba, shapes the structure of the Southern Ocean ecosystem. Its central position in the food web, the ongoing environmental changes due to climatic warming, and increasing commercial interest on this species emphasize the urgency of understanding the adaptability of krill to its environment. Krill has evolved rhythmic physiological and behavioral functions which are synchronized with the daily and seasonal cycles of the complex Southern Ocean ecosystem. The mechanisms, however, leading to these rhythms are essentially unknown. Here, we show that krill possesses an endogenous circadian clock that governs metabolic and physiological output rhythms. We found that expression of the canonical clock gene cry2 was highly rhythmic both in a light-dark cycle and in constant darkness. We detected a remarkable short circadian period, which we interpret as a special feature of the krill's circadian clock that helps to entrain the circadian system to the extreme range of photoperiods krill is exposed to throughout the year. Furthermore, we found that important key metabolic enzymes of krill showed bimodal circadian oscillations (∼9–12 h period) in transcript abundance and enzymatic activity. Oxygen consumption of krill showed ∼9–12 h oscillations that correlated with the temporal activity profile of key enzymes of aerobic energy metabolism. Our results demonstrate the first report of an endogenous circadian timing system in Antarctic krill and its likely link to metabolic key processes. Krill's circadian clock may not only be critical for synchronization to the solar day but also for the control of seasonal events. This study provides a powerful basis for the investigation into the mechanisms of temporal synchronization in this marine key species and will also lead to the first comprehensive analyses of the circadian clock of a polar marine organism through the entire photoperiodic cycle.

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A Circadian Clock in Antarctic Krill: An Endogenous Timing System Governs Metabolic Output Rhythms in the Euphausid Species Euphausia superba

Meyer B (2011) A Circadian Clock in Antarctic Krill: An Endogenous Timing System Governs Metabolic Output Rhythms in the Euphausid Species Euphausia superba. PLoS ONE 6(10): e26090. doi:10.1371/journal.pone.0026090 A Circadian Clock in Antarctic Krill: An Endogenous Timing System Governs Metabolic Output Rhythms in the Euphausid Species Euphausia superba Mathias Teschke 0 Sabrina Wendt 0 So Kawaguchi 0 Achim Kramer 0 Bettina Meyer 0 Michael N. Nitabach, Yale School of Medicine, United States of America 0 1 Laboratory of Chronobiology, Charite Universita tsmedizin Berlin , Berlin, Germany , 2 Department of Environment and Heritage, Australian Antarctic Division , Kingston , Australia , 3 Antarctic Climate and Ecosystems Co-operative Research Centre , Hobart , Australia , 4 Scientific Division Polar Biological Oceanography, Alfred Wegener Institute for Polar and Marine Research , Bremerhaven , Germany Antarctic krill, Euphausia superba, shapes the structure of the Southern Ocean ecosystem. Its central position in the food web, the ongoing environmental changes due to climatic warming, and increasing commercial interest on this species emphasize the urgency of understanding the adaptability of krill to its environment. Krill has evolved rhythmic physiological and behavioral functions which are synchronized with the daily and seasonal cycles of the complex Southern Ocean ecosystem. The mechanisms, however, leading to these rhythms are essentially unknown. Here, we show that krill possesses an endogenous circadian clock that governs metabolic and physiological output rhythms. We found that expression of the canonical clock gene cry2 was highly rhythmic both in a light-dark cycle and in constant darkness. We detected a remarkable short circadian period, which we interpret as a special feature of the krill's circadian clock that helps to entrain the circadian system to the extreme range of photoperiods krill is exposed to throughout the year. Furthermore, we found that important key metabolic enzymes of krill showed bimodal circadian oscillations (,9-12 h period) in transcript abundance and enzymatic activity. Oxygen consumption of krill showed ,9-12 h oscillations that correlated with the temporal activity profile of key enzymes of aerobic energy metabolism. Our results demonstrate the first report of an endogenous circadian timing system in Antarctic krill and its likely link to metabolic key processes. Krill's circadian clock may not only be critical for synchronization to the solar day but also for the control of seasonal events. This study provides a powerful basis for the investigation into the mechanisms of temporal synchronization in this marine key species and will also lead to the first comprehensive analyses of the circadian clock of a polar marine organism through the entire photoperiodic cycle. - Funding: This work was supported by the German Ministry of Education and Research (BMBF) through project Lazarev Sea Krill Study (LAKRIS, 03F0400A). MT was supported by funding of the German Research Foundation (DFG) through project Photoperiodic Time Measurement in Antarctic krill (TE 618/3-1). Research in A.K.s laboratory is supported by the 6 th EU framework programme EUCLOCK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Antarctic krill (Euphausia superba Dana), a small shrimp-like crustacean species, shapes the structure of the Southern Ocean ecosystem due to its central position as direct link between primary producers and apex predators. A decline in winter sea ice duration caused by the climatic warming resulted in a long-term decline in krill biomass in the Scotia Sea sector of the Southern Ocean [1]. An increasing krill fishery might in addition impact the krill stocks in this region [2]. Krills central position in the food web, the ongoing environmental changes in its habitat, and increasing commercial interest on this species emphasize the urgency of understanding the adaptability of krill to its environment. Krill has evolved rhythmic physiological and behavioral functions which are synchronized with the cyclic changes of the Southern Ocean ecosystem. These functions occur over a daily cycle, such as diel vertical migration (DVM), which is believed to allow krill to maximise food intake in the upper water column during the night and minimise predator risk by migrating in the deep during the day [3]. In addition, seasonal cycles of metabolic regulation [4] and maturity [5] in krill are synchronized with the extreme seasonal cycles in environmental factors such as day length, sea ice extent and food availability. The mechanisms leading to these rhythms are essentially unknown. They are, however, crucial to predict the response of krill to the ongoing environmental changes and, due to its central position, to predict alterations i (...truncated)


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Mathias Teschke, Sabrina Wendt, So Kawaguchi, Achim Kramer, Bettina Meyer. A Circadian Clock in Antarctic Krill: An Endogenous Timing System Governs Metabolic Output Rhythms in the Euphausid Species Euphausia superba, PLOS ONE, 2011, 10, DOI: 10.1371/journal.pone.0026090