How Symbiodiniaceae meets the challenges of life during coral bleaching

Jiang, Jiaoyun; Wang, Aoqi; Deng, Xiangzi; Zhou, Wenxu; Gan, Qinhua; Lu, Yandu

doi:10.1007/s00338-021-02115-9

Cited by 18 publications

(12 citation statements)

References 152 publications

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“…While previous studies have established a connection between elevated temperature and ROS production in coral symbionts 70 , the data presented here suggests that, under the environmental conditions employed in this study, the symbionts are able to cope with increased ROS or at least manage it by reducing activity. As such, it is likely that damage in the host is primarily a result of host-produced ROS as opposed to ROS generated by the symbiont, as is frequently proposed 89 .…”

Section: Resultsmentioning

confidence: 98%

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

Petrou

Nunn

Padula

et al. 2021

Sci Rep

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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.

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Section: Resultsmentioning

confidence: 98%

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

Petrou

Nunn

Padula

et al. 2021

Sci Rep

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“…We thus probed the possible effects of abiotic stresses on the synthesis of GAs in dinoflagellate endosymbionts. For reef-building corals, the bleaching process is induced by environmental stimuli, such as high light, high temperature, and acidification ( Lu et al, 2020 ; Jiang et al, 2021 ). Therefore, to probe the physiological relevance of GAs in microalgae, we monitored the transcriptional activities of the committed GA biosynthetic gene GA 20-oxidase ( GA 20 ox1 ) and GA profiles under the high light, high temperature, and acidification conditions.…”

Section: Resultsmentioning

confidence: 99%

“…Although reef-building corals provide numerous socio-economic and ecological benefits in addition to high biodiversity ( inter alia , tourist and recreational attractions, shoreline protection and fisheries), the global populations of reef systems are declining, partly due to rapid climatic changes, including global warming, ocean acidification, and ultraviolet radiation ( Roth, 2014 ). The loss of algal symbionts or algal pigments is always assumed as critical steps for coral bleaching ( Jiang et al, 2021 ). Therefore, understanding of the stress response and mechanisms underlying these traits of dinoflagellate endosymbionts is critical to the symbiosis stability and the health of the coral systems.…”

Section: Introductionmentioning

confidence: 99%

A Functional Genomics View of Gibberellin Metabolism in the Cnidarian Symbiont Breviolum minutum

Yang²,

Gu³

et al. 2022

Front. Plant Sci.

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Dinoflagellate inhabitants of the reef-building corals exchange nutrients and signals with host cells, which often benefit the growth of both partners. Phytohormones serve as central hubs for signal integration between symbiotic microbes and their hosts, allowing appropriate modulation of plant growth and defense in response to various stresses. However, the presence and function of phytohormones in photosynthetic dinoflagellates and their function in the holobionts remain elusive. We hypothesized that endosymbiotic dinoflagellates may produce and employ phytohormones for stress responses. Using the endosymbiont of reef corals Breviolum minutum as model, this study aims to exam whether the alga employ analogous signaling systems by an integrated multiomics approach. We show that key gibberellin (GA) biosynthetic genes are widely present in the genomes of the selected dinoflagellate algae. The non-13-hydroxylation pathway is the predominant route for GA biosynthesis and the multifunctional GA dioxygenase in B. minutum has distinct substrate preference from high plants. GA biosynthesis is modulated by the investigated bleaching-stimulating stresses at both transcriptional and metabolic levels and the exogenously applied GAs improve the thermal tolerance of the dinoflagellate. Our results demonstrate the innate ability of a selected Symbiodiniaceae to produce the important phytohormone and the active involvement of GAs in the coordination and the integration of the stress response.

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“…Sterols are vital membrane components in all eukaryotic cells [ 60 ]. In corals, it has been suggested that sterols are originally synthesized by the symbiotic Symbiodiaceae and not by the host corals [ 33 , 61 ]. Indeed, sterols play an important role in the bleaching process of cnidarians [ 33 , 49 ].…”

Section: Discussionmentioning

confidence: 99%

Adaptive Responses of the Sea Anemone Heteractis crispa to the Interaction of Acidification and Global Warming

Tian

Chen

et al. 2022

Animals

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Ocean acidification and warming are two of the most important threats to the existence of marine organisms and are predicted to co-occur in oceans. The present work evaluated the effects of acidification (AC: 24 ± 0.1 °C and 900 μatm CO2), warming (WC: 30 ± 0.1 °C and 450 μatm CO2), and their combination (CC: 30 ± 0.1 °C and 900 μatm CO2) on the sea anemone, Heteractis crispa, from the aspects of photosynthetic apparatus (maximum quantum yield of photosystem II (PS II), chlorophyll level, and Symbiodiniaceae density) and sterol metabolism (cholesterol content and total sterol content). In a 15-day experiment, acidification alone had no apparent effect on the photosynthetic apparatus, but did affect sterol levels. Upregulation of their chlorophyll level is an important strategy for symbionts to adapt to high partial pressure of CO2 (pCO2). However, after warming stress, the benefits of high pCO2 had little effect on stress tolerance in H. crispa. Indeed, thermal stress was the dominant driver of the deteriorating health of H. crispa. Cholesterol and total sterol contents were significantly affected by all three stress conditions, although there was no significant change in the AC group on day 3. Thus, cholesterol or sterol levels could be used as important indicators to evaluate the impact of climate change on cnidarians. Our findings suggest that H. crispa might be relatively insensitive to the impact of ocean acidification, whereas increased temperature in the future ocean might impair viability of H. crispa.

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How Symbiodiniaceae meets the challenges of life during coral bleaching

Cited by 18 publications

References 152 publications

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

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

A Functional Genomics View of Gibberellin Metabolism in the Cnidarian Symbiont Breviolum minutum

Adaptive Responses of the Sea Anemone Heteractis crispa to the Interaction of Acidification and Global Warming

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