The Antarctic Krill Euphausia superba Shows Diurnal Cycles of Transcription under Natural Conditions

Cristiano De Pittà,Alessandro Albiero,Cristiano Bertolucci,Caterina Millino,Rodolfo Costa,Gabriella M Mazzotta,Alberto Biscontin,Gabriele Sales

doi:10.1371/journal.pone.0068652

Cristiano De Pittà, Alessandro Albiero + Show 6 more

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https://doi.org/10.1371/journal.pone.0068652

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Abstract

BackgroundPolar environments are characterized by extreme seasonal changes in day length, light intensity and spectrum, the extent of sea ice during the winter, and food availability. A key species of the Southern Ocean ecosystem, the Antarctic krill (Euphausia superba) has evolved rhythmic physiological and behavioral mechanisms to adapt to daily and seasonal changes. The molecular organization of the clockwork underlying these biological rhythms is, nevertheless, still only partially understood.Methodology/Principal FindingsThe genome sequence of the Antarctic krill is not yet available. A normalized cDNA library was produced and pyrosequenced in the attempt to identify large numbers of transcripts. All available E. superba sequences were then assembled to create the most complete existing oligonucleotide microarray platform with a total of 32,217 probes. Gene expression signatures of specimens collected in the Ross Sea at five different time points over a 24-hour cycle were defined, and 1,308 genes differentially expressed were identified. Of the corresponding transcripts, 609 showed a significant sinusoidal expression pattern; about 40% of these exibithed a 24-hour periodicity while the other 60% was characterized by a shorter (about 12-hour) rhythm. We assigned the differentially expressed genes to functional categories and noticed that those concerning translation, proteolysis, energy and metabolic process, redox regulation, visual transduction and stress response, which are most likely related to daily environmental changes, were significantly enriched. Two transcripts of peroxiredoxin, thought to represent the ancestral timekeeping system that evolved about 2.5 billion years ago, were also identified as were two isoforms of the EsRh1 opsin and two novel arrestin1 sequences involved in the visual transduction cascade.ConclusionsOur work represents the first characterization of the krill diurnal transcriptome under natural conditions and provides a first insight into the genetic regulation of physiological changes, which occur around the clock during an Antarctic summer day.

Highlights

The Antarctic krill (Euphausia superba, Dana 1982), a crustacean species with a circumpolar distribution [1], plays a key role in the Antarctic ecosystem as it is an important link between primary producers and organisms at high trophic levels [2]
Our work represents the first characterization of the krill diurnal transcriptome under natural conditions and provides a first insight into the genetic regulation of physiological changes, which occur around the clock during an Antarctic summer day
Generation sequencing and reads assembly In order to better characterize the krill’s transcriptome and to increase the probability of identifying circadian clock or clock-controlled genes, total RNA was extracted from a variety of adult organs and tissues, including the head, the abdomen, and the thoracopods, of specimens sampled at different times of the day over a 24-hour cycle

Summary

Introduction

The Antarctic krill (Euphausia superba, Dana 1982), a crustacean species with a circumpolar distribution [1], plays a key role in the Antarctic ecosystem as it is an important link between primary producers and organisms at high trophic levels [2]. Krill abundance has declined by 80% over the past 30 years in concomitance with global temperature rises and the consequent decrease in the winter sea ice cover [6], a change which has had important implications with regard to krill stocks and to food interactions in the Southern Ocean [7,8] and to the fishing industry [9]. The polar pelagic environment is characterized by extreme seasonal changes causing considerable variations in day length, light intensity and spectrum, sea ice extent and food availability [4]. Polar environments are characterized by extreme seasonal changes in day length, light intensity and spectrum, the extent of sea ice during the winter, and food availability. A key species of the Southern Ocean ecosystem, the Antarctic krill (Euphausia superba) has evolved rhythmic physiological and behavioral mechanisms to adapt to daily and seasonal changes. The molecular organization of the clockwork underlying these biological rhythms is, still only partially understood

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