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Evidence for Oscillating Circadian Clock Genes in the Copepod

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Evidence for Oscillating Circadian Clock Genes in the Copepod Marine biology Evidence for oscillating circadian clock royalsocietypublishing.org/journal/rsbl genes in the copepod Calanus finmarchicus during the summer solstice in the high Arctic Research 1,2,3 1,3 4 5 Cite this article: Hüppe L, Payton L, Last K, Lukas Hüppe , Laura Payton , Kim Last , David Wilcockson , Wilcockson D, Ershova E, Meyer B. 2020 Elizaveta Ershova6,7 and Bettina Meyer1,2,3 Evidence for oscillating circadian clock genes in 1 the copepod Calanus finmarchicus during the Institute for Chemistry and Biology of the Marine Environment, Carl von Ossietzky University of Oldenburg, 26111 Oldenburg, Germany summer solstice in the high Arctic. Biol. Lett. 2Helmholtz Institute for Functional Marine Biodiversity (HIFMB) at the University of Oldenburg, 16: 20200257. 26111 Oldenburg, Germany 3 http://dx.doi.org/10.1098/rsbl.2020.0257 Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Department of Biosciences, Section Polar Biological Oceanography, 27570 Bremerhaven, Germany 4Scottish Association for Marine Science, Oban, Argyll PA37 1QA, UK 5Institute of Biological, Environmental, and Rural Sciences, Aberystwyth University, Aberystwyth SY23 3DA, UK 6Department for Arctic and Marine Biology, Faculty for Biosciences, Fisheries and Economics, UiT The Arctic Received: 16 April 2020 University of Norway, 9019 Tromsø, Norway Accepted: 16 June 2020 7Shirshov Institute of Oceanology, Russian Academy of Sciences, Russian Federation, 36 Nakhimova Avenue, Moscow 117997, Russia LH, 0000-0002-7793-9046; LP, 0000-0001-5090-0929; KL, 0000-0001-9402-2347; DW, 0000-0002-5923-4472; EE, 0000-0002-9007-2811; BM, 0000-0001-6804-9896 Subject Areas: The circadian clock provides a mechanism for anticipating environmental cycles ecology, molecular biology, environmental and is synchronized by temporal cues such as daily light/dark cycle or photo- science period. However, the Arctic environment is characterized by several months of Midnight Sun when the sun is continuously above the horizon and where sea ice Keywords: further attenuates photoperiod. To test if the oscillations of circadian clock genes Arctic, Midnight Sun, circadian clock, copepod, remain in synchrony with subtle environmental changes, we sampled the cope- zooplankton, sea ice pod Calanus finmarchicus, a key zooplankter in the north Atlantic, to determine in situ daily circadian clock gene expression near the summer solstice at a southern (74.5° N) sea ice-free and a northern (82.5° N) sea ice-covered station. Results revealed significant oscillation of genes at both stations, indicating the Authors for correspondence: persistence of the clock at this time. While copepods from the southern station Lukas Hüppe showed oscillations in the daily range, those from the northern station exhibited e-mail: [email protected] an increase in ultradian oscillations. We suggest that in C. finmarchicus,even Laura Payton small daily changes of solar altitude seem to be sufficient to entrain the circadian clock and propose that at very high latitudes, in under-ice ecosystems, tidal cues e-mail: [email protected] may be used as an additional entrainment cue. Bettina Meyer e-mail: [email protected] 1. Introduction Biological clocks are ubiquitous, ancient and adaptive mechanisms enabling organisms to track and anticipate environmental cycles and regulate biological processes accordingly. Recent work on Calanus finmarchicus, a key pelagic species in the northern Atlantic food web [1], revealed that C. finmarchicus pos- sesses a functional circadian clock that might be involved in the timing of both diel vertical migration (DVM) [2] and seasonal events such as diapause [3]. Electronic supplementary material is available The Arctic is characterized by strong seasonal fluctuations in photoperiod lead- online at https://doi.org/10.6084/m9.figshare. ing to permanent illumination during Midnight Sun and permanent darkness c.5042051. © 2020 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. (a)(b) 2 40 royalsocietypublishing.org/journal/rsbl 20 80° N 0 Svalbard midday solar altitude (°) 75° N Barents JFMAMJJASOND Sea month (c) 40 ) 1500 –1 s –2 30 70° N 1000 20 Biol. Lett. E×m Ocean data view 0° Norway 40° E 500 10 10° E 30° E 20° E solar altitude (°) 16 PAR ( PAR 0 0 : 20200257 0 612180 JR85 (18./19.06.2018) time of day (h) B13 (30.06./01.07.2018) (d) position of the ice edge (18.6.2018) horizon 0.2 summer solstice (21.06.2018) 0.1 0 −0.1 tidal height (m) −0.2 −0.3 0 6 12 18 0 time of day (h) Figure 1. Physical characteristics of the sampling sites. (a) Map with sampled stations JR85 (blue) and B13 (red) and the position of the sea ice edge at the day of sampling at JR85 (18.06.2018). (b) Solar altitude at 12.00 throughout the year 2018 at both stations. The dashed yellow line marks the day of summer solstice, the dashed black line marks the horizon and the blue and red dots mark the day of sampling for the respective station. (c) Diel fluctuations in PAR (area plot) and solaraltitude (lines) over the course of the first sampling day at each station (18.06.2018 and 30.06.2018 for JR85 and B13, respectively). (d) Tidal height over the course of the first sampling day at each station. during PolarNight. Since circadian clocks ofmost organisms use Sampling at JR85 started 3 days before the summer solstice, on the daily light/dark cycles as a Zeitgeber (literally, time giver)to 18th June at 11.00 and ended on 19th June at 11.00 (all times maintain synchrony with the environment (entrainment), the noted in local time (UTC + 2). Sampling at B13 started 9 days capacity of the mechanism to persist under Midnight Sun con- after the summer solstice, on 30th June at 14.00 and ended on ditions remains uncertain [4,5]. Climate change-induced 1st July at 14.00. For each timepoint, the water column was sampled between 200 m depth to the surface with a WP2 plank- latitudinal range shifts displace zooplankton such as C. finmarch- ton net (200 µm mesh size). Net contents were preserved in icus to higher latitudes [6] yet the impact of high-latitude RNAlater (Ambion, UK) for later analysis post cruise. photoperiods on the endogenous timing systems of non- Measurements of photosynthetically active radiation (PAR, i.e. endemic species is currently unknown. Indeed, the northward the range of wavelengths available to photosynthesis, 400 to expansion of organisms may be limited by the adaptive capacity 700 nm) were taken byPQS1 PAR sensors (Kipp & Zonen, The Neth- of the clock to entrain to such extreme photoperiods [7,8]. erlands) from the ship’s meteorological platform. Modelled data of The persistence of zooplankton DVM during the high Arctic sun altitude were obtained from the United States Naval Observatory Midnight Sun period is still debatable [9–13] and therefore (https://aa.usno.navy.mil/data/docs/AltAz.php, USNO, USA) raises the question whether associated clock gene oscillations and the keisan.casio website (https://keisan.casio.com/exec/ are maintained at this time or whether the clock stops ‘ticking’ system/1224682331). Information on the tidal dynamics have and only reinitiates once clear light/dark cycles resume? been drawn from the TPX08 model [14] by using the OTPS package (Tidal Prediction Software, http://www-po.coas.oregonstate.edu/ Here we address this by determining circadian clock gene ~poa/www-po/research/po/research/tide/index.html), via the expression in C. finmarchicus during the Midnight Sun period. mbotps program (MB-System; [15]). Additional methodological information and physical characteristics of the water column are available in the electronic supplementary material. 2. Material and methods (b) Copepod sorting and clock gene expression (a) Study area, field sampling and data collection For each replicate (n =3–5 per time point), 15 C. finmarchicus Sampling was conducted during Cruise JR17006 of the RRS James CV stage copepods were sorted from the samples using morpholo- Clark Ross in summer 2018 at two stations along a latitudinal gical characteristics. Since there is considerable morphological gradient, from the Nansen Basin (JR85; 82.5° N, 30.85° E, sea overlap between congeners C. finmarchicus and C. glacialis,species ice-covered) to the southern Barents Sea (B13; 74.5° N, 30° E, identification was corroborated molecularly (see electronic sup- sea ice-free, figure 1a). Sampling covered a complete 24 h cycle plementary material S1). Copepod total RNA was obtained by a at 4 h intervals, resulting in seven timepoints per station. combination of TRIzol-based extraction and the Direct-zol™ clock cycle period1 timeless 3 21 5.5 40 D * 4.0 D ** U ** D * D * 0.4 19 30 royalsocietypublishing.org/journal/rsbl 8 5.0 0.2 17 3.0 20 0 JR85 6 15 4.5 –0.2 expression 2.0 10 relative gene relative 13 tidal height (m) 4 4.0 0 solar altitude (°) –0.4 12.5 4.0 40 0.4 D *** D *** U * D *** 8 D *** 3.5 24 10.0 7 30 0.2 3.0 B13 6 20 7.5 2.5 20 0 5 expression 10 –0.2 relative gene relative 2.0 5.0 16 4 tidal height (m) 1.5 3 0 –0.4 12 18 00 06 12 12 18 00 06 12 12 18 00 06 12 12 18 00 06 12 cryptochrome2 vrille doubletime2 cryptochrome1 50 15 40 0.4 U ** U ** U *** D *** 45 20 15.0 13 30 0.2 Biol. Lett. 40 12.5 JR85 15 11 20 0 35 10.0 9 expression 10 –0.2 relative gene relative 10 7.5 30 7 tidal height (m) 0 solar altitude (°)–0.4 solar altitude (°) 16 12 : 20200257 70 D *** D ** D *** 9 40 0.4 10 60 8 30 15 7 0.2 50 8 B13 6 20 0 40 10 6 5 10 –0.2 expression 30 4 relative gene relative 4 tidal height (m) 20 5 2 0 solar altitude (°) –0.4 12 18 00 06 12 12 18 00 06 12 12 18 00 06 12 12 18 00 06 12 local time (UTC + 2) Figure 2.
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