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Review
.2016 Dec;186(8):947-968.
doi: 10.1007/s00360-016-1000-6. Epub 2016 Jun 4.

Life in a dark biosphere: a review of circadian physiology in "arrhythmic" environments

Affiliations
Review

Life in a dark biosphere: a review of circadian physiology in "arrhythmic" environments

Andrew David Beale et al. J Comp Physiol B.2016 Dec.

Abstract

Most of the life with which humans interact is exposed to highly rhythmic and extremely predictable changes in illumination that occur with the daily events of sunrise and sunset. However, while the influence of the sun feels omnipotent to surface dwellers such as ourselves, life on earth is dominated, in terms of biomass, by organisms isolated from the direct effects of the sun. A limited understanding of what life is like away from the sun can be inferred from our knowledge of physiology and ecology in the light biosphere, but a full understanding can only be gained by studying animals from the dark biosphere, both in the laboratory and in their natural habitats. One of the least understood aspects of life in the dark biosphere is the rhythmicity of physiology and what it means to live in an environment of low or no rhythmicity. Here we describe methods that may be used to understand rhythmic physiology in the dark and summarise some of the studies of rhythmic physiology in "arrhythmic" environments, such as the poles, deep sea and caves. We review what can be understood about the adaptive value of rhythmic physiology on the Earth's surface from studies of animals from arrhythmic environments and what role a circadian clock may play in the dark.

Keywords: Arrhythmic; Cave; Circadian clock; Evolution; Physiology; Subterranean.

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Figures

Fig. 1
Fig. 1
Article publication rate on topics associated with circadian physiology (source: PubMed, http://www.ncbi.nlm.nih.gov/pubmed).a andb present publication rates on different scales
Fig. 2
Fig. 2
The circadian clock core feedback loops interact with cellular metabolism.a In the core feedback loops, rhythmic expression of PERIOD (PER1, PER2 and PER3) and CRYPTOCHROME (CRY1 and CRY2) proteins are produced from the rhythmic activation ofPeriod (Per1,Per2 andPer3) andCryptochome (Cry1 andCry2) by CLOCK and BMAL1. PER and CRY proteins form complexes that subsequently translocate back to the nucleus to inhibit the CLOCK:BMAL1 activity, thus closing the loop. CLOCK and BMAL1 also activate the rhythmic expression of many other genes within the cell imparting rhythmicity on many aspects of cellular physiology, such asNampt, the rate limiting enzyme in the NAD salvage pathway.b The NAD salvage pathway has a direct influence on the NAD+-dependent deacetylase, SIRT1. SIRT1 directly interacts with the core circadian clock elements in three major ways: (1) through deacetylating PER2, promoting its degredation (Asher et al. 2008); (2) through its effect on circadian chromatin remodelling through its deactylase action on H3K9 and H3K14 in preferential sites of CLOCK’s own acetylase activity (Doi et al. ; Nakahata et al. 2008). (3) Through deacetylating, modifying CRY1-mediated repression of the CLOCK/BMAL1 complex (Hirayama et al. ; Nakahata et al. 2008). SIRT1 also influences H3K4 trimethylation through circadian deacetylation of MLL1, causing a reduction in transcriptionally active chromatin (Aguilar-Arnal et al. 2015). Since one CLOCK target isNampt, in this way, the NAD-CLOCK accessory loop via SIRT1 is closed (Nakahata et al. ; Ramsey et al. 2009)
Fig. 3
Fig. 3
E-box reporter activity in zebrafish larvae. Luciferase expression fromtg(4xE-box:Luc), detected by immunohistochemistry with an anti-luciferase antibody and an Alexa Fluor 488-labelled secondary antibody, shows diurnal (a) and circadian (b) rhythms across all tissues of a 5 dpf larvae. Relative fluorescence intensity is showncolour coded. Larvae were sampled at five different time points during LD (ZT3-ZT3′;a) or DD (CT3-CT3′;b) after a 4-day entrainment period.Scale bar 1.0 mm. Taken from Weger et al. (2013). Reprinted from Developmental Biology, 380/2, Weger et al., Real-time in vivo monitoring of circadian E-box enhancer activity: a robust and sensitive zebrafish reporter line for developmental, chemical and neural biology of the circadian clock, 259–273, Copyright (2013), with permission from Elsevier
Fig. 4
Fig. 4
a Sample actograms showing patterns of activity over 1 year in sub-adult reindeer inleft, northern Norway at 70°N (R. t. tarandus), andright, Svalbard at 78°N (R. t. platyrhynchus).Lines indicating the beginning and end of civil twilight (when light intensity is 10 lx,orange) and sunrise and sunset (yellow) are superimposed on each actogram (van Oort et al. 2005). Reprinted by permission from Macmillan Publishers Ltd: Nature, van Oort et al. , copyright 2005.b Hints of rhythmicity in a deep-sea decapod at 1178–1240 m below sea level,Pontophilus norvegicus, as indicated by the variation in stomach fullness of fish caught at different times of day, however ANOVA reveals no significant difference between samples (Maynou and Cartes 1998). Copyright © 1998 Inter-Research.c Core clock gene rhythms in peripheral tissues of the mole rat,Spalax ehrenbergi, on a light–dark cycle. Here, RT-PCR reveals thatPer2 shows a high amplitude rhythm in both the harderian gland (Hard) and the liver (Avivi et al. 2002). Copyright © 2002, The National Academy of Sciences
Fig. 5
Fig. 5
a The cave fish,Schistura jaruthanini, shows pronounced free-running locomotor rhythms after 6 months in 12:12 LD cycle. Activity was measured as the number of movements per 30 min period (y-axis) and was plotted over the full period of observation. Lomb-Scargle periodogram (right) shows pronounced rhythmicity in circadian range, typical of all but one species in Duboué et al.’s study (Duboué and Borowsky 2012).b A second cavefish,Phreatichys andruzzii, shows an absence of circadian rhythms during 12:12 LD cycles. Fish were maintained at 27 °C during recording and locomotor activity, measured by infra-red beam crossing, is double plotted on thex-axis (Cavallari et al. 2011).c Two independent populations of cavefish demonstrate an absence of circadian rhythms of activity in constant darkness after LD entrainment inAstyanax mexicanus, though the sister surface population is rhythmic under the same protocol. The cavefish of this species show rhythmic activity under 12:12 LD cycles (Beale et al. 2013).dPhreatichthys andruzzii cavefish, arrhythmic after LD entrainment, show circadian rhythms of locomotor activity under entrainment by an alternative zeitgeber, feeding. Fish were maintained under constant darkness and fed once a day at ZT0 and show a clear response to this daily zeitgeber. However, entrainment was not tested under constant conditions, i.e., the absence of feeding (Cavallari et al. 2011).e Though Pachón and Chica populations ofA. mexicanus do not show rhythms of locomotor activity in DD after LD entrainment, an underlyingPer1 gene expression rhythm is present. Its damped profile is indicative of an unpregulation of the repressive light-input pathway (Beale et al. 2013).f Timed feeding entrains the peripheral core clocks ofP. andruzzii, asPer1 andClk1a rhythms persist in the absence of the zeitgeber (Cavallari et al. 2011)
Fig. 6
Fig. 6
The Mexican tetraAstyanax mexicanus is a useful model for studying chronobiology as several distinct phenotypes are found within the same species complex.a Eyeless Pachón cave morph andb eyed surface morph
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