Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora

Abstract Coral reefs across the globe are threatened by warming oceans. The last few years have seen the worst mass coral bleaching events recorded, with more than one quarter of all reefs irreversibly impacted. Considering the widespread devastation, we need to increase our efforts to understanding...

Full description

Bibliographic Details
Main Authors: K. Petrou, B. L. Nunn, M. P. Padula, D. J. Miller, D. A. Nielsen
Format: Article
Language:English
Published: Nature Portfolio 2021-09-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-021-98548-x
_version_ 1823960840952348672
author K. Petrou
B. L. Nunn
M. P. Padula
D. J. Miller
D. A. Nielsen
author_facet K. Petrou
B. L. Nunn
M. P. Padula
D. J. Miller
D. A. Nielsen
author_sort K. Petrou
collection DOAJ
description Abstract Coral reefs across the globe are threatened by warming oceans. The last few years have seen the worst mass coral bleaching events recorded, with more than one quarter of all reefs irreversibly impacted. Considering the widespread devastation, we need to increase our efforts to understanding the physiological and metabolic shifts underlying the breakdown of this important symbiotic ecosystem. Here, we investigated the proteome (PRIDE accession # PXD011668) of both host and symbionts of the reef-building coral Acropora millepora exposed to ambient (~ 28 °C) and elevated temperature (~ 32 °C for 2 days, following a five-day incremental increase) and explored associated biomolecular changes in the symbiont, with the aim of gaining new insights into the mechanisms underpinning the collapse of the coral symbiosis. We identified 1,230 unique proteins (774 host and 456 symbiont) in the control and thermally stressed corals, of which 107 significantly increased and 125 decreased in abundance under elevated temperature relative to the control. Proteins involved in oxidative stress and proteolysis constituted 29% of the host proteins that increased in abundance, with evidence of impairment to endoplasmic reticulum and cytoskeletal regulation proteins. In the symbiont, we detected a decrease in proteins responsible for photosynthesis and energy production (33% of proteins decreased in abundance), yet minimal signs of oxidative stress or proteolysis. Lipid stores increased > twofold despite reduction in photosynthesis, suggesting reduced translocation of carbon to the host. There were significant changes in proteins related to symbiotic state, including proteins linked to nitrogen metabolism in the host and the V-ATPase (-0.6 fold change) known to control symbiosome acidity. These results highlight key differences in host and symbiont proteomic adjustments under elevated temperature and identify two key proteins directly involved in bilateral nutrient exchange as potential indicators of symbiosis breakdown.
first_indexed 2024-12-17T16:55:45Z
format Article
id doaj.art-7985aae22b5741aa9bb5977c63ac9aca
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-12-17T16:55:45Z
publishDate 2021-09-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-7985aae22b5741aa9bb5977c63ac9aca2022-12-21T21:40:27ZengNature PortfolioScientific Reports2045-23222021-09-0111111610.1038/s41598-021-98548-xBroad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora milleporaK. Petrou0B. L. Nunn1M. P. Padula2D. J. Miller3D. A. Nielsen4School of Life Sciences, University of Technology SydneyDepartment of Genome Sciences, University of WashingtonSchool of Life Sciences, University of Technology SydneyARC Centre of Excellence for Coral Reef Studies, James Cook UniversitySchool of Life Sciences, University of Technology SydneyAbstract Coral reefs across the globe are threatened by warming oceans. The last few years have seen the worst mass coral bleaching events recorded, with more than one quarter of all reefs irreversibly impacted. Considering the widespread devastation, we need to increase our efforts to understanding the physiological and metabolic shifts underlying the breakdown of this important symbiotic ecosystem. Here, we investigated the proteome (PRIDE accession # PXD011668) of both host and symbionts of the reef-building coral Acropora millepora exposed to ambient (~ 28 °C) and elevated temperature (~ 32 °C for 2 days, following a five-day incremental increase) and explored associated biomolecular changes in the symbiont, with the aim of gaining new insights into the mechanisms underpinning the collapse of the coral symbiosis. We identified 1,230 unique proteins (774 host and 456 symbiont) in the control and thermally stressed corals, of which 107 significantly increased and 125 decreased in abundance under elevated temperature relative to the control. Proteins involved in oxidative stress and proteolysis constituted 29% of the host proteins that increased in abundance, with evidence of impairment to endoplasmic reticulum and cytoskeletal regulation proteins. In the symbiont, we detected a decrease in proteins responsible for photosynthesis and energy production (33% of proteins decreased in abundance), yet minimal signs of oxidative stress or proteolysis. Lipid stores increased > twofold despite reduction in photosynthesis, suggesting reduced translocation of carbon to the host. There were significant changes in proteins related to symbiotic state, including proteins linked to nitrogen metabolism in the host and the V-ATPase (-0.6 fold change) known to control symbiosome acidity. These results highlight key differences in host and symbiont proteomic adjustments under elevated temperature and identify two key proteins directly involved in bilateral nutrient exchange as potential indicators of symbiosis breakdown.https://doi.org/10.1038/s41598-021-98548-x
spellingShingle K. Petrou
B. L. Nunn
M. P. Padula
D. J. Miller
D. A. Nielsen
Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora
Scientific Reports
title Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora
title_full Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora
title_fullStr Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora
title_full_unstemmed Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora
title_short Broad scale proteomic analysis of heat-destabilised symbiosis in the hard coral Acropora millepora
title_sort broad scale proteomic analysis of heat destabilised symbiosis in the hard coral acropora millepora
url https://doi.org/10.1038/s41598-021-98548-x
work_keys_str_mv AT kpetrou broadscaleproteomicanalysisofheatdestabilisedsymbiosisinthehardcoralacroporamillepora
AT blnunn broadscaleproteomicanalysisofheatdestabilisedsymbiosisinthehardcoralacroporamillepora
AT mppadula broadscaleproteomicanalysisofheatdestabilisedsymbiosisinthehardcoralacroporamillepora
AT djmiller broadscaleproteomicanalysisofheatdestabilisedsymbiosisinthehardcoralacroporamillepora
AT danielsen broadscaleproteomicanalysisofheatdestabilisedsymbiosisinthehardcoralacroporamillepora