Dim artificial light at night alters gene expression rhythms and growth in a key seagrass species (Posidonia oceanica)

Abstract Artificial light at night (ALAN) is a globally spreading anthropogenic stressor, affecting more than 20% of coastal habitats. The alteration of the natural light/darkness cycle is expected to impact the physiology of organisms by acting on the complex circuits termed as circadian rhythms. O...

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Main Authors: L. Dalle Carbonare, A. Basile, L. Rindi, F. Bulleri, H. Hamedeh, S. Iacopino, V. Shukla, D. A. Weits, L. Lombardi, A. Sbrana, L. Benedetti-Cecchi, B. Giuntoli, F. Licausi, E. Maggi
Format: Article
Language:English
Published: Nature Portfolio 2023-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-37261-3
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author L. Dalle Carbonare
A. Basile
L. Rindi
F. Bulleri
H. Hamedeh
S. Iacopino
V. Shukla
D. A. Weits
L. Lombardi
A. Sbrana
L. Benedetti-Cecchi
B. Giuntoli
F. Licausi
E. Maggi
author_facet L. Dalle Carbonare
A. Basile
L. Rindi
F. Bulleri
H. Hamedeh
S. Iacopino
V. Shukla
D. A. Weits
L. Lombardi
A. Sbrana
L. Benedetti-Cecchi
B. Giuntoli
F. Licausi
E. Maggi
author_sort L. Dalle Carbonare
collection DOAJ
description Abstract Artificial light at night (ALAN) is a globally spreading anthropogenic stressor, affecting more than 20% of coastal habitats. The alteration of the natural light/darkness cycle is expected to impact the physiology of organisms by acting on the complex circuits termed as circadian rhythms. Our understanding of the impact of ALAN on marine organisms is lagging behind that of terrestrial ones, and effects on marine primary producers are almost unexplored. Here, we investigated the molecular and physiological response of the Mediterranean seagrass, Posidonia oceanica (L.) Delile, as model to evaluate the effect of ALAN on seagrass populations established in shallow waters, by taking advantage of a decreasing gradient of dim nocturnal light intensity (from < 0.01 to 4 lx) along the NW Mediterranean coastline. We first monitored the fluctuations of putative circadian-clock genes over a period of 24 h along the ALAN gradient. We then investigated whether key physiological processes, known to be synchronized with day length by the circadian rhythm, were also affected by ALAN. ALAN influenced the light signalling at dusk/night in P. oceanica, including that of shorter blue wavelengths, through the ELF3–LUX1–ZTL regulatory network, and suggested that the daily perturbation of internal clock orthologs in seagrass might have caused the recruitment of PoSEND33 and PoPSBS genes to mitigate the repercussions of a nocturnal stress on photosynthesis during the day. A long-lasting impairment of gene fluctuations in sites characterised by ALAN could explain the reduced growth of the seagrass leaves when these were transferred into controlled conditions and without lighting during the night. Our results highlight the potential contribution of ALAN to the global loss of seagrass meadows, posing questions about key interactions with a variety of other human-related stressors in urban areas, in order to develop more efficient strategies to globally preserve these coastal foundation species.
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spelling doaj.art-a1995af523db4f4e8119366cfca6765e2023-07-02T11:15:33ZengNature PortfolioScientific Reports2045-23222023-06-0113111410.1038/s41598-023-37261-3Dim artificial light at night alters gene expression rhythms and growth in a key seagrass species (Posidonia oceanica)L. Dalle Carbonare0A. Basile1L. Rindi2F. Bulleri3H. Hamedeh4S. Iacopino5V. Shukla6D. A. Weits7L. Lombardi8A. Sbrana9L. Benedetti-Cecchi10B. Giuntoli11F. Licausi12E. Maggi13Institute of Life Sciences, Scuola Superiore Sant’AnnaInstitute of Life Sciences, Scuola Superiore Sant’AnnaDipartimento di Biologia, Universita’ di Pisa, CoNISMaDipartimento di Biologia, Universita’ di Pisa, CoNISMaInstitute of Life Sciences, Scuola Superiore Sant’AnnaInstitute of Life Sciences, Scuola Superiore Sant’AnnaInstitute of Life Sciences, Scuola Superiore Sant’AnnaInstitute of Life Sciences, Scuola Superiore Sant’AnnaDipartimento di Biologia, Universita’ di Pisa, CoNISMaDipartimento di Biologia, Universita’ di Pisa, CoNISMaDipartimento di Biologia, Universita’ di Pisa, CoNISMaInstitute of Life Sciences, Scuola Superiore Sant’AnnaDepartment of Biology, University of OxfordDipartimento di Biologia, Universita’ di Pisa, CoNISMaAbstract Artificial light at night (ALAN) is a globally spreading anthropogenic stressor, affecting more than 20% of coastal habitats. The alteration of the natural light/darkness cycle is expected to impact the physiology of organisms by acting on the complex circuits termed as circadian rhythms. Our understanding of the impact of ALAN on marine organisms is lagging behind that of terrestrial ones, and effects on marine primary producers are almost unexplored. Here, we investigated the molecular and physiological response of the Mediterranean seagrass, Posidonia oceanica (L.) Delile, as model to evaluate the effect of ALAN on seagrass populations established in shallow waters, by taking advantage of a decreasing gradient of dim nocturnal light intensity (from < 0.01 to 4 lx) along the NW Mediterranean coastline. We first monitored the fluctuations of putative circadian-clock genes over a period of 24 h along the ALAN gradient. We then investigated whether key physiological processes, known to be synchronized with day length by the circadian rhythm, were also affected by ALAN. ALAN influenced the light signalling at dusk/night in P. oceanica, including that of shorter blue wavelengths, through the ELF3–LUX1–ZTL regulatory network, and suggested that the daily perturbation of internal clock orthologs in seagrass might have caused the recruitment of PoSEND33 and PoPSBS genes to mitigate the repercussions of a nocturnal stress on photosynthesis during the day. A long-lasting impairment of gene fluctuations in sites characterised by ALAN could explain the reduced growth of the seagrass leaves when these were transferred into controlled conditions and without lighting during the night. Our results highlight the potential contribution of ALAN to the global loss of seagrass meadows, posing questions about key interactions with a variety of other human-related stressors in urban areas, in order to develop more efficient strategies to globally preserve these coastal foundation species.https://doi.org/10.1038/s41598-023-37261-3
spellingShingle L. Dalle Carbonare
A. Basile
L. Rindi
F. Bulleri
H. Hamedeh
S. Iacopino
V. Shukla
D. A. Weits
L. Lombardi
A. Sbrana
L. Benedetti-Cecchi
B. Giuntoli
F. Licausi
E. Maggi
Dim artificial light at night alters gene expression rhythms and growth in a key seagrass species (Posidonia oceanica)
Scientific Reports
title Dim artificial light at night alters gene expression rhythms and growth in a key seagrass species (Posidonia oceanica)
title_full Dim artificial light at night alters gene expression rhythms and growth in a key seagrass species (Posidonia oceanica)
title_fullStr Dim artificial light at night alters gene expression rhythms and growth in a key seagrass species (Posidonia oceanica)
title_full_unstemmed Dim artificial light at night alters gene expression rhythms and growth in a key seagrass species (Posidonia oceanica)
title_short Dim artificial light at night alters gene expression rhythms and growth in a key seagrass species (Posidonia oceanica)
title_sort dim artificial light at night alters gene expression rhythms and growth in a key seagrass species posidonia oceanica
url https://doi.org/10.1038/s41598-023-37261-3
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