Responses of the Mediterranean seagrass Cymodocea nodosa to combined temperature and salinity stress at the ionomic, transcriptomic, ultrastructural and photosynthetic levels

Soultana  Tsioli; Maria  Koutalianou; Georgios A.  Gkafas; Athanasios  Exadactylos; Vasilis  Papathanasiou; Christos I. Katsaros; Sotiris  Orfanidis; Frithjof Kuepper

doi:10.1016/j.marenvres.2021.105512

Responses of the Mediterranean seagrass Cymodocea nodosa to combined temperature and salinity stress at the ionomic, transcriptomic, ultrastructural and photosynthetic levels

Soultana Tsioli, Maria Koutalianou, Georgios A. Gkafas, Athanasios Exadactylos, Vasilis Papathanasiou, Christos I. Katsaros, Sotiris Orfanidis, Frithjof Kuepper^* (Corresponding Author)

^*Corresponding author for this work

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Abstract

The Little Neptune grass Cymodocea nodosa is a key seagrass species in the Mediterranean Sea, forming extensive and patchy meadows in shallow coastal and transitional ecosystems. In such habitats, high temperatures and salinities, separately and in combination, can be significant stressors in the context of climate change, particularly during heatwave events, and seawater desalination plant effluents.
Despite well-documented negative, macroscopic effects, the underlying cellular and molecular processes of the combined effects of increasing temperature and salinities have remained largely elusive in C. nodosa – which are addressed by the present study. High salinity and high temperature, alone and in combination, affected ion equilibrium in the plant cells. Non-synonymous mutations marked the transcriptomic response to salinity and temperature stress at loci related to osmotic stress. Cell structure, especially the nucleus, chloroplasts, mitochondria and organization of the MT cytoskeleton, was also altered. Both temperature and salinity stress negatively affected photosynthetic activity as evidenced by ΔF/Fm’, following an antagonistic interaction type.
Overall, this study showed that all biological levels investigated were strongly affected by temperature and salinity stress, however, with the latter having more severe effects. The results have implications for the operation of desalination plants and for assessing the impacts of marine heat waves.

Original language	English
Article number	105512
Number of pages	15
Journal	Marine Environmental Research
Volume	175
Early online date	15 Feb 2022
DOIs	https://doi.org/10.1016/j.marenvres.2021.105512
Publication status	Published - Mar 2022

Bibliographical note

Acknowledgements
We are particularly grateful to David E. Salt and John M.C. Danku (University of Aberdeen, now at the University of Nottingham) for providing facilities and guidance for the ionomics work within the framework of this study. This research was funded by the European Commission (European Social Fund – ESF; grant no. 375425) and Greek national funds through the Operational Program “Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF) - Research Funding Program: THALES - Investing in knowledge society through the European Social Funds (Project Acronym: MANTOLES). We would also like to thank the TOTAL Foundation (Project “Diversity of brown algae in the Eastern Mediterranean”), the European Commission under its Horizon 2021 Research and Innovation Programme (grants ZEROBRINE, grant agreement No. 730390, and WATERMINING, grant agreement No. 869474) and the UK Natural Environment Research Council for their Supplort to FCK (program Oceans 2025 – WP 4.5 and grants NE/D521522/1 and NE/J023094/1). The MASTS pooling initiative (Marine Alliance for Science and Technology for Scotland, funded by the Scottish Funding Council and contributing institutions; grant reference HR09011) is gratefully acknowledged.

Data Availability Statement

The data supporting the findings of this study are available from the corresponding author, Frithjof C. Küpper, upon request.

Keywords

Chlorophyll
Cymodocea
cytoskeleton
Little Neptune grass
photosynthesis
transcriptome
ultrastructure

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Cite this

Tsioli, S., Koutalianou, M., Gkafas, G. A., Exadactylos, A., Papathanasiou, V., Katsaros, C. I., Orfanidis, S., & Kuepper, F. (2022). Responses of the Mediterranean seagrass Cymodocea nodosa to combined temperature and salinity stress at the ionomic, transcriptomic, ultrastructural and photosynthetic levels. Marine Environmental Research, 175, Article 105512. https://doi.org/10.1016/j.marenvres.2021.105512

Responses of the Mediterranean seagrass Cymodocea nodosa to combined temperature and salinity stress at the ionomic, transcriptomic, ultrastructural and photosynthetic levels. / Tsioli, Soultana ; Koutalianou, Maria ; Gkafas, Georgios A. et al.
In: Marine Environmental Research, Vol. 175, 105512, 03.2022.

Research output: Contribution to journal › Article › peer-review

Tsioli, S, Koutalianou, M, Gkafas, GA, Exadactylos, A, Papathanasiou, V, Katsaros, CI, Orfanidis, S & Kuepper, F 2022, 'Responses of the Mediterranean seagrass Cymodocea nodosa to combined temperature and salinity stress at the ionomic, transcriptomic, ultrastructural and photosynthetic levels', Marine Environmental Research, vol. 175, 105512. https://doi.org/10.1016/j.marenvres.2021.105512

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abstract = "The Little Neptune grass Cymodocea nodosa is a key seagrass species in the Mediterranean Sea, forming extensive and patchy meadows in shallow coastal and transitional ecosystems. In such habitats, high temperatures and salinities, separately and in combination, can be significant stressors in the context of climate change, particularly during heatwave events, and seawater desalination plant effluents. Despite well-documented negative, macroscopic effects, the underlying cellular and molecular processes of the combined effects of increasing temperature and salinities have remained largely elusive in C. nodosa – which are addressed by the present study. High salinity and high temperature, alone and in combination, affected ion equilibrium in the plant cells. Non-synonymous mutations marked the transcriptomic response to salinity and temperature stress at loci related to osmotic stress. Cell structure, especially the nucleus, chloroplasts, mitochondria and organization of the MT cytoskeleton, was also altered. Both temperature and salinity stress negatively affected photosynthetic activity as evidenced by ΔF/Fm{\textquoteright}, following an antagonistic interaction type. Overall, this study showed that all biological levels investigated were strongly affected by temperature and salinity stress, however, with the latter having more severe effects. The results have implications for the operation of desalination plants and for assessing the impacts of marine heat waves.",

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author = "Soultana Tsioli and Maria Koutalianou and Gkafas, {Georgios A.} and Athanasios Exadactylos and Vasilis Papathanasiou and Katsaros, {Christos I.} and Sotiris Orfanidis and Frithjof Kuepper",

note = "Acknowledgements We are particularly grateful to David E. Salt and John M.C. Danku (University of Aberdeen, now at the University of Nottingham) for providing facilities and guidance for the ionomics work within the framework of this study. This research was funded by the European Commission (European Social Fund – ESF; grant no. 375425) and Greek national funds through the Operational Program “Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF) - Research Funding Program: THALES - Investing in knowledge society through the European Social Funds (Project Acronym: MANTOLES). We would also like to thank the TOTAL Foundation (Project “Diversity of brown algae in the Eastern Mediterranean”), the European Commission under its Horizon 2021 Research and Innovation Programme (grants ZEROBRINE, grant agreement No. 730390, and WATERMINING, grant agreement No. 869474) and the UK Natural Environment Research Council for their Supplort to FCK (program Oceans 2025 – WP 4.5 and grants NE/D521522/1 and NE/J023094/1). The MASTS pooling initiative (Marine Alliance for Science and Technology for Scotland, funded by the Scottish Funding Council and contributing institutions; grant reference HR09011) is gratefully acknowledged. ",

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AU - Koutalianou, Maria

AU - Gkafas, Georgios A.

AU - Exadactylos, Athanasios

AU - Papathanasiou, Vasilis

AU - Katsaros, Christos I.

AU - Orfanidis, Sotiris

AU - Kuepper, Frithjof

N1 - Acknowledgements We are particularly grateful to David E. Salt and John M.C. Danku (University of Aberdeen, now at the University of Nottingham) for providing facilities and guidance for the ionomics work within the framework of this study. This research was funded by the European Commission (European Social Fund – ESF; grant no. 375425) and Greek national funds through the Operational Program “Education and Lifelong Learning” of the National Strategic Reference Framework (NSRF) - Research Funding Program: THALES - Investing in knowledge society through the European Social Funds (Project Acronym: MANTOLES). We would also like to thank the TOTAL Foundation (Project “Diversity of brown algae in the Eastern Mediterranean”), the European Commission under its Horizon 2021 Research and Innovation Programme (grants ZEROBRINE, grant agreement No. 730390, and WATERMINING, grant agreement No. 869474) and the UK Natural Environment Research Council for their Supplort to FCK (program Oceans 2025 – WP 4.5 and grants NE/D521522/1 and NE/J023094/1). The MASTS pooling initiative (Marine Alliance for Science and Technology for Scotland, funded by the Scottish Funding Council and contributing institutions; grant reference HR09011) is gratefully acknowledged.

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N2 - The Little Neptune grass Cymodocea nodosa is a key seagrass species in the Mediterranean Sea, forming extensive and patchy meadows in shallow coastal and transitional ecosystems. In such habitats, high temperatures and salinities, separately and in combination, can be significant stressors in the context of climate change, particularly during heatwave events, and seawater desalination plant effluents. Despite well-documented negative, macroscopic effects, the underlying cellular and molecular processes of the combined effects of increasing temperature and salinities have remained largely elusive in C. nodosa – which are addressed by the present study. High salinity and high temperature, alone and in combination, affected ion equilibrium in the plant cells. Non-synonymous mutations marked the transcriptomic response to salinity and temperature stress at loci related to osmotic stress. Cell structure, especially the nucleus, chloroplasts, mitochondria and organization of the MT cytoskeleton, was also altered. Both temperature and salinity stress negatively affected photosynthetic activity as evidenced by ΔF/Fm’, following an antagonistic interaction type. Overall, this study showed that all biological levels investigated were strongly affected by temperature and salinity stress, however, with the latter having more severe effects. The results have implications for the operation of desalination plants and for assessing the impacts of marine heat waves.

AB - The Little Neptune grass Cymodocea nodosa is a key seagrass species in the Mediterranean Sea, forming extensive and patchy meadows in shallow coastal and transitional ecosystems. In such habitats, high temperatures and salinities, separately and in combination, can be significant stressors in the context of climate change, particularly during heatwave events, and seawater desalination plant effluents. Despite well-documented negative, macroscopic effects, the underlying cellular and molecular processes of the combined effects of increasing temperature and salinities have remained largely elusive in C. nodosa – which are addressed by the present study. High salinity and high temperature, alone and in combination, affected ion equilibrium in the plant cells. Non-synonymous mutations marked the transcriptomic response to salinity and temperature stress at loci related to osmotic stress. Cell structure, especially the nucleus, chloroplasts, mitochondria and organization of the MT cytoskeleton, was also altered. Both temperature and salinity stress negatively affected photosynthetic activity as evidenced by ΔF/Fm’, following an antagonistic interaction type. Overall, this study showed that all biological levels investigated were strongly affected by temperature and salinity stress, however, with the latter having more severe effects. The results have implications for the operation of desalination plants and for assessing the impacts of marine heat waves.

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KW - Cymodocea

KW - cytoskeleton

KW - Little Neptune grass

KW - photosynthesis

KW - transcriptome

KW - ultrastructure

U2 - 10.1016/j.marenvres.2021.105512

DO - 10.1016/j.marenvres.2021.105512

M3 - Article

SN - 0141-1136

VL - 175

JO - Marine Environmental Research

JF - Marine Environmental Research

M1 - 105512

ER -

Responses of the Mediterranean seagrass Cymodocea nodosa to combined temperature and salinity stress at the ionomic, transcriptomic, ultrastructural and photosynthetic levels

Abstract

Bibliographical note

Data Availability Statement

Keywords

UN SDGs

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