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, 9 (1), 13894

Analysis of the Circadian Transcriptome of the Antarctic Krill Euphausia Superba

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Analysis of the Circadian Transcriptome of the Antarctic Krill Euphausia Superba

Alberto Biscontin et al. Sci Rep.

Abstract

Antarctic krill (Euphausia superba) is a high latitude pelagic organism which plays a central role in the Southern Ocean ecosystem. E. superba shows daily and seasonal rhythms in physiology and behaviour, which are synchronized with the environmental cycles of its habitat. Recently, the main components of the krill circadian machinery have been identified and characterized. However, the exact mechanisms through which the endogenous timing system operates the control and regulation of the overt rhythms remains only partially understood. Here we investigate the involvement of the circadian clock in the temporal orchestration of gene expression by using a newly developed version of a krill microarray platform. The analysis of transcriptome data from krill exposed to both light-dark cycles (LD 18:6) and constant darkness (DD), has led to the identification of 1,564 putative clock-controlled genes. A remarkably large proportion of such genes, including several clock components (clock, period, cry2, vrille, and slimb), show oscillatory expression patterns in DD, with a periodicity shorter than 24 hours. Energy-storage pathways appear to be regulated by the endogenous clock in accordance with their ecological relevance in daily energy managing and overwintering. Our results provide the first representation of the krill circadian transcriptome under laboratory, free-running conditions.

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Oscillation periods and expression peaks distribution of genes with sinusoidal expression patterns in LD, DD, and in both conditions. Classification of the genes showing sinusoidal oscillatory patterns on the basis of their oscillation period (τ: 12, 15, 18, 21 and 24 h) in LD (A), DD (D), and in both LD and DD (G). Different colours refer to different period lengths (see legend in the figure). Percentage of genes characterized by each period length are reported on each pie chart. Distribution of expression peaks of genes showing oscillatory profiles in LD (B), DD (E), and in both LD and DD (H). Distribution of expression peaks of genes showing oscillatory profiles characterized by a 24-hour period in LD (C), DD (F), and in both LD and DD (I). Proportion of genes showing a peak of expression at each time point is reported. Yellow and blue bars refer to light and dark intervals, respectively.
Figure 2
Figure 2
GO analysis of genes with sinusoidal expression patterns in LD, DD, and in both conditions. Classification of annotated genes with sinusoidal expression patterns throughout the 24-hour cycle in (A) LD (1,485 with GO annotation out of 2,743 annotated genes), (B) DD (802 out of 1,776 annotated genes), and C) in both LD and DD (376 out of 428 annotated genes) into 9 main GO terms. The diagrams show the proportion of each GO term. Percentage of genes belonging to each GO term are reported on each pie chart. Percentages of the significantly enriched GO terms are marked in bold typeface. See Supplementary Tables 4, 5, and 6 for further details.
Figure 3
Figure 3
Gene expression profiles of three core components of the krill circadian clock. Temporal expression profiles of cryptochrome 2, clock and period by using qRT-PCR performed on heads of krill sampled every 3 hours, starting from light-on (ZT0) or subjective light-on (CT0) in LD 16:8 and after 3 days of constant darkness. Relative quantification (RQ) is represented as mean ± SD (n = 3 pools of 7 individuals). Kruskal-Wallis p-value is reported (8 degrees of freedom), as well as the adjusted p-value, putative period (τ) and phase of the oscillation estimated using the RAIN algorithm. Yellow and blue bars refer to light and dark intervals, respectively.
Figure 4
Figure 4
Genes with rhythmic expression patterns in LD involved in energetic and metabolic processes. (A) Expression profiles of most relevant genes involved in “Energetic and metabolic process” in LD. Clock-controlled genes showing a sinusoidal expression pattern in both LD and DD, are marked in red. acyl-CoA dehydrogenase (ACAD, ID:N19130), acetyl-CoA carboxylase (ACAC, ID: N29097), acyl-CoA synthetase (ACS, ID:M101952), ATP synthase (ATP, ID:M87362), chitin synthase (CHS, ID:N19106), enoyl-CoA isomerase (ECI, ID:M1878), enolase (ENO, ID:N20765), glyceraldehyde-3-phosphate dehydrogenase (GAPDH, ID:M80754), glycogen branching enzyme (GBE, ID:M8882), glycogen debranching enzyme (GDE, ID:M17951), glycogen synthase (GYS, ID:M2029), pyruvate kinase (PK, ID:N18962), phosphoenolpyruvate carboxykinase (PCK, ID:N18402), phosphofructokinase (PFK, ID:N21844), glycogen phosphorylase (PYG, ID:M105964), and succinate-CoA ligase (SCS, ID:M18729). (B) Schematic representation of the daily distribution of metabolic processes resulting from the transcriptional signature of several genes through the 24-hour cycle. Different metabolic processes are marked by arrows shaded with a colour gradient showing the time of day corresponding to the higher expression levels of gene groups. The length of the arrows and darker colours indicate intervals and peaks of expression, respectively. ZTs are indicated at the bottom of each panel; yellow and blue bars refer to light and dark intervals.

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