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Lipidome analysis of Symbiodiniaceae reveals possible mechanisms of heat stress tolerance in reef coral symbionts

Lipidome analysis of Symbiodiniaceae reveals possible mechanisms of heat stress tolerance in reef coral symbionts
Lipidome analysis of Symbiodiniaceae reveals possible mechanisms of heat stress tolerance in reef coral symbionts
Climate change-induced global warming threatens the survival of key ecosystems including shallow water coral reefs. Elevated temperatures can disrupt the normal physiological functioning of photosynthetic organisms by altering the fluidity and permeability of chloroplast membranes that is defined and regulated by their lipid composition. Since the habitat-forming reef corals rely on the obligatory symbiosis with dinoflagellates of the family Symbiodiniaceae, their heat stress response can be expected to be strongly influenced by the symbiont's lipid metabolism. However, in contrast to the steady increase in the knowledge of the functioning of coral symbionts at the genomic and transcriptomic level, the understanding of their membrane lipid composition and regulation in response to temperature stress is lagging behind. We have utilised mass spectrometry-based lipidomic analyses to identify the key polar lipids that form the biological membranes of reef coral symbionts, comparing the thermotolerant species Durusdinium trenchii with the thermosensitive taxon Cladocopium C3, both hosted by Acropora valida. Our results indicate that the superior thermotolerance D. trenchii inside the host corals could be achieved through (1) the amount and saturation of sulfoquinovosyldiacylglycerols, in particular through putative photosystem II interactions, (2) the increased digalactosyldiacylglycerol to monogalactosyldiacylglycerol ratio with the potential to stabilise thylakoid membranes and integrated proteins, and (3) the chaperone-like function of lyso-lipids. Thereby, our study provides novel insights into the heat tolerance of coral symbionts, contributing to the understanding of the potential of coral reef ecosystems to respond and adjust to heat stress events that are becoming more frequent due to climate change. Finally, our identification of multiple mechanisms of heat tolerance in Symbiodiniaceae furthers the knowledge of the general stress physiology of photosynthetic organisms.
0722-4028
1241-1253
Rosset, S.
22555676-237a-498b-8252-c8c7cb9dca08
Koster, G.
e404c38a-6f48-430a-adf0-5208228cb9e7
Brandsma, J.
b4c553dc-9444-466a-b352-25fd8fa25ee7
Hunt, A. N.
0e8ebb1c-89bf-46fc-a4f6-d5dc4fa08456
Postle, A. D.
0fa17988-b4a0-4cdc-819a-9ae15c5dad66
D'Angelo, C. (Maria Cecilia)
0d35b03b-684d-43aa-a57a-87212ab07ee1
Rosset, S.
22555676-237a-498b-8252-c8c7cb9dca08
Koster, G.
e404c38a-6f48-430a-adf0-5208228cb9e7
Brandsma, J.
b4c553dc-9444-466a-b352-25fd8fa25ee7
Hunt, A. N.
0e8ebb1c-89bf-46fc-a4f6-d5dc4fa08456
Postle, A. D.
0fa17988-b4a0-4cdc-819a-9ae15c5dad66
D'Angelo, C. (Maria Cecilia)
0d35b03b-684d-43aa-a57a-87212ab07ee1

Rosset, S., Koster, G., Brandsma, J., Hunt, A. N., Postle, A. D. and D'Angelo, C. (Maria Cecilia) (2019) Lipidome analysis of Symbiodiniaceae reveals possible mechanisms of heat stress tolerance in reef coral symbionts. Coral Reefs, 38 (6), 1241-1253. (doi:10.1007/s00338-019-01865-x).

Record type: Article

Abstract

Climate change-induced global warming threatens the survival of key ecosystems including shallow water coral reefs. Elevated temperatures can disrupt the normal physiological functioning of photosynthetic organisms by altering the fluidity and permeability of chloroplast membranes that is defined and regulated by their lipid composition. Since the habitat-forming reef corals rely on the obligatory symbiosis with dinoflagellates of the family Symbiodiniaceae, their heat stress response can be expected to be strongly influenced by the symbiont's lipid metabolism. However, in contrast to the steady increase in the knowledge of the functioning of coral symbionts at the genomic and transcriptomic level, the understanding of their membrane lipid composition and regulation in response to temperature stress is lagging behind. We have utilised mass spectrometry-based lipidomic analyses to identify the key polar lipids that form the biological membranes of reef coral symbionts, comparing the thermotolerant species Durusdinium trenchii with the thermosensitive taxon Cladocopium C3, both hosted by Acropora valida. Our results indicate that the superior thermotolerance D. trenchii inside the host corals could be achieved through (1) the amount and saturation of sulfoquinovosyldiacylglycerols, in particular through putative photosystem II interactions, (2) the increased digalactosyldiacylglycerol to monogalactosyldiacylglycerol ratio with the potential to stabilise thylakoid membranes and integrated proteins, and (3) the chaperone-like function of lyso-lipids. Thereby, our study provides novel insights into the heat tolerance of coral symbionts, contributing to the understanding of the potential of coral reef ecosystems to respond and adjust to heat stress events that are becoming more frequent due to climate change. Finally, our identification of multiple mechanisms of heat tolerance in Symbiodiniaceae furthers the knowledge of the general stress physiology of photosynthetic organisms.

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Accepted/In Press date: 25 September 2019
e-pub ahead of print date: 16 October 2019
Published date: December 2019

Identifiers

Local EPrints ID: 437132
URI: http://eprints.soton.ac.uk/id/eprint/437132
ISSN: 0722-4028
PURE UUID: d36ff230-5b9b-4814-b725-379636ec1989
ORCID for A. D. Postle: ORCID iD orcid.org/0000-0001-7361-0756

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Date deposited: 17 Jan 2020 17:35
Last modified: 26 Nov 2021 02:32

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Contributors

Author: S. Rosset
Author: G. Koster
Author: J. Brandsma
Author: A. N. Hunt
Author: A. D. Postle ORCID iD

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