Environmental and Circadian Regulation Combine to Shape the Rhythmic Selenoproteome

The circadian clock orchestrates an organism’s endogenous processes with environmental 24 h cycles. Redox homeostasis and the circadian clock regulate one another to negate the potential effects of our planet’s light/dark cycle on the generation of reactive oxygen species (ROS) and attain homeostasi...

Full description

Bibliographic Details
Main Authors: Holly Kay, Harry Taylor, Gerben van Ooijen
Format: Article
Language:English
Published: MDPI AG 2022-01-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/11/3/340
_version_ 1827661202413584384
author Holly Kay
Harry Taylor
Gerben van Ooijen
author_facet Holly Kay
Harry Taylor
Gerben van Ooijen
author_sort Holly Kay
collection DOAJ
description The circadian clock orchestrates an organism’s endogenous processes with environmental 24 h cycles. Redox homeostasis and the circadian clock regulate one another to negate the potential effects of our planet’s light/dark cycle on the generation of reactive oxygen species (ROS) and attain homeostasis. Selenoproteins are an important class of redox-related enzymes that have a selenocysteine residue in the active site. This study reports functional understanding of how environmental and endogenous circadian rhythms integrate to shape the selenoproteome in a model eukaryotic cell. We mined quantitative proteomic data for the 24 selenoproteins of the picoeukaryote <i>Ostreococcus tauri</i> across time series, under environmentally rhythmic entrained conditions of light/dark (LD) cycles, compared to constant circadian conditions of constant light (LL). We found an overrepresentation of selenoproteins among rhythmic proteins under LL, but an underrepresentation under LD conditions. Rhythmic selenoproteins under LL that reach peak abundance later in the day showed a greater relative amplitude of oscillations than those that peak early in the day. Under LD, amplitude did not correlate with peak phase; however, we identified high-amplitude selenium uptake rhythms under LD but not LL conditions. Selenium deprivation induced strong qualitative defects in clock gene expression under LD but not LL conditions. Overall, the clear conclusion is that the circadian and environmental cycles exert differential effects on the selenoproteome, and that the combination of the two enables homeostasis. Selenoproteins may therefore play an important role in the cellular response to reactive oxygen species that form as a consequence of the transitions between light and dark.
first_indexed 2024-03-10T00:05:11Z
format Article
id doaj.art-4a5a23d30b77469f8099f0b7cf5b51be
institution Directory Open Access Journal
issn 2073-4409
language English
last_indexed 2024-03-10T00:05:11Z
publishDate 2022-01-01
publisher MDPI AG
record_format Article
series Cells
spelling doaj.art-4a5a23d30b77469f8099f0b7cf5b51be2023-11-23T16:10:15ZengMDPI AGCells2073-44092022-01-0111334010.3390/cells11030340Environmental and Circadian Regulation Combine to Shape the Rhythmic SelenoproteomeHolly Kay0Harry Taylor1Gerben van Ooijen2School of Biological Sciences, University of Edinburgh, Max Born Crescent, Edinburgh EH9 3BF, UKSchool of Biological Sciences, University of Edinburgh, Max Born Crescent, Edinburgh EH9 3BF, UKSchool of Biological Sciences, University of Edinburgh, Max Born Crescent, Edinburgh EH9 3BF, UKThe circadian clock orchestrates an organism’s endogenous processes with environmental 24 h cycles. Redox homeostasis and the circadian clock regulate one another to negate the potential effects of our planet’s light/dark cycle on the generation of reactive oxygen species (ROS) and attain homeostasis. Selenoproteins are an important class of redox-related enzymes that have a selenocysteine residue in the active site. This study reports functional understanding of how environmental and endogenous circadian rhythms integrate to shape the selenoproteome in a model eukaryotic cell. We mined quantitative proteomic data for the 24 selenoproteins of the picoeukaryote <i>Ostreococcus tauri</i> across time series, under environmentally rhythmic entrained conditions of light/dark (LD) cycles, compared to constant circadian conditions of constant light (LL). We found an overrepresentation of selenoproteins among rhythmic proteins under LL, but an underrepresentation under LD conditions. Rhythmic selenoproteins under LL that reach peak abundance later in the day showed a greater relative amplitude of oscillations than those that peak early in the day. Under LD, amplitude did not correlate with peak phase; however, we identified high-amplitude selenium uptake rhythms under LD but not LL conditions. Selenium deprivation induced strong qualitative defects in clock gene expression under LD but not LL conditions. Overall, the clear conclusion is that the circadian and environmental cycles exert differential effects on the selenoproteome, and that the combination of the two enables homeostasis. Selenoproteins may therefore play an important role in the cellular response to reactive oxygen species that form as a consequence of the transitions between light and dark.https://www.mdpi.com/2073-4409/11/3/340selenocysteinecircadian clockselenoproteomeseleniumcellular rhythms
spellingShingle Holly Kay
Harry Taylor
Gerben van Ooijen
Environmental and Circadian Regulation Combine to Shape the Rhythmic Selenoproteome
Cells
selenocysteine
circadian clock
selenoproteome
selenium
cellular rhythms
title Environmental and Circadian Regulation Combine to Shape the Rhythmic Selenoproteome
title_full Environmental and Circadian Regulation Combine to Shape the Rhythmic Selenoproteome
title_fullStr Environmental and Circadian Regulation Combine to Shape the Rhythmic Selenoproteome
title_full_unstemmed Environmental and Circadian Regulation Combine to Shape the Rhythmic Selenoproteome
title_short Environmental and Circadian Regulation Combine to Shape the Rhythmic Selenoproteome
title_sort environmental and circadian regulation combine to shape the rhythmic selenoproteome
topic selenocysteine
circadian clock
selenoproteome
selenium
cellular rhythms
url https://www.mdpi.com/2073-4409/11/3/340
work_keys_str_mv AT hollykay environmentalandcircadianregulationcombinetoshapetherhythmicselenoproteome
AT harrytaylor environmentalandcircadianregulationcombinetoshapetherhythmicselenoproteome
AT gerbenvanooijen environmentalandcircadianregulationcombinetoshapetherhythmicselenoproteome