Different levels of energetic coupling between photosynthesis and respiration do not determine the occurrence of adaptive responses of Symbiodiniaceae to global warming

Pierangelini, Mattia; Thiry, Marc; Cardol, Pierre

doi:10.1111/nph.16738

Cited by 16 publications

(16 citation statements)

References 93 publications

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“…66 ). The capacity of the AOX pathway measured in S. pistillata was 24% of Rd and is in the range as values previously reported for different species of Symbiodiniaceae grown in culture 20,65 . The observed lack of effect of the AOX inhibitor (i.e.…”

Section: Discussionsupporting

confidence: 86%

In vivo assessment of mitochondrial respiratory alternative oxidase activity and cyclic electron flow around photosystem I on small coral fragments

Luna

Córdoba-Granados

Dang

et al. 2020

Sci Rep

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The mutualistic relationship existing between scleractinian corals and their photosynthetic endosymbionts involves a complex integration of the metabolic pathways within the holobiont. Respiration and photosynthesis are the most important of these processes and although they have been extensively studied, our understanding of their interactions and regulatory mechanisms is still limited. In this work we performed chlorophyll-a fluorescence, oxygen exchange and time-resolved absorption spectroscopy measurements on small and thin fragments (0.3 cm2) of the coral Stylophora pistillata. We showed that the capacity of mitochondrial alternative oxidase accounted for ca. 25% of total coral respiration, and that the high-light dependent oxygen uptake, commonly present in isolated Symbiodiniaceae, was negligible. The ratio between photosystem I (PSI) and photosystem II (PSII) active centers as well as their respective electron transport rates, indicated that PSI cyclic electron flow occurred in high light in S. pistillata and in some branching and lamellar coral species freshly collected in the field. Altogether, these results show the potential of applying advanced biophysical and spectroscopic methods on small coral fragments to understand the complex mechanisms of coral photosynthesis and respiration and their responses to environmental changes.

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Section: Discussionsupporting

confidence: 86%

In vivo assessment of mitochondrial respiratory alternative oxidase activity and cyclic electron flow around photosystem I on small coral fragments

Luna

Córdoba-Granados

Dang

et al. 2020

Sci Rep

Self Cite

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“…This phenomenon could be explained by a relatively higher proportion of "light-418 dependent O2 consumption" through processes such as photorespiration and chlororespiration 419 that can serve as photoprotective electron sinks to dissipate excess excitation energy (Hughes et al 2018). Such a photosynthetic strategy has been observed for Symbiodiniaceae taxa that are inherently more tolerant of heat and/or light stress (Suggett et al 2008;Roberty et al 2014, Pierangelini et al 2020). This strategy is conducive to a higher overall PSII electron flow (Gorbunov et al 2011), yet would result in a smaller proportion of electrons that flow linearly to Ci fixation (Cardol et al 2011).…”

Section: Reliance Of Mangrove P Acuta On Photochemical Quenchingmentioning

confidence: 99%

Symbiont shuffling across environmental gradients aligns with changes in carbon uptake and translocation in the reef-building coral Pocillopora acuta

Ros

Suggett

Edmondson³

et al. 2021

Coral Reefs

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Symbiosis between reef-building corals and unicellular algae (Symbiodiniaceae) fuels the growth and productivity of corals reefs. Capacity for Symbiodiniaceae to fix inorganic carbon (Ci) and translocate carbon compounds to the host is central to coral health, but how these processes change for corals thriving in environmental extremes remains largely unresolved. We investigate how a model coral -Pocillopora acuta -persists from a reef habitat into an adjacent extreme mangrove lagoon on the Great Barrier Reef. We combine respirometry and photophysiology measurements, Symbiodiniaceae genotyping, and 13 C labelling to compare P. acuta metabolic performance across habitats, in relation to the Ci uptake and 27 translocation capacity by symbionts' autotrophy. We show that differences in P. acuta 28 metabolic strategies across habitats align with a shift in dominant host-associated 29 Symbiodiniaceae taxon, from Cladocopium in the reef to Durusdinium in the mangroves. This 30 shift corresponded with a change in 'photosynthetic strategy', with P. acuta in the mangroves 31 utilising absorbed light for photochemistry over non-photochemical quenching. Mangrove 32 corals translocated similar proportions of carbon compared to the reefs, despite a lower Ci uptake. These trends indicate that coral survival in mangrove environments occurs through sustained translocation rate of organic compounds from coral symbionts to host. Introduction 36The ecological success of reef-building corals resides on their ability to establish and 37 maintain metabolic exchanges through an effective symbiotic association with dinoflagellates 38 from the family Symbiodiniaceae. Symbiodiniaceae fuel their hosts with organic carbon by fixing inorganic carbon (Ci) through photosynthesis (Davy et al. 2012). While Ci uptake rates by the algal symbionts have rarely been measured, they appear strongly regulated by environmental factors, such as availability of CO2 (pCO2) (Suggett et al. 2012b; Brading et al. 42 2013) and temperature (Oakley et al. 2014). Recent work on cultured Symbiodiniaceae 43 revealed that different environmental optima primarily drive variation in Ci uptake rates (Ros 44 et al. 2020). Within reef systems where Symbiodiniaceae are hosted within cnidarian tissues, symbiont cells are typically carbon-limited (Smith and Muscatine 1999; Doherty 2009; Towanda and Thuesen 2012); as such, cnidarians can exhibit a stimulated carbon metabolism under naturally higher pCO2 (more acidic) environments (Suggett et al. 2012b). The efficiency 48 of Symbiodiniaceae carbon metabolism across environments thus appears an important trait in 49 supporting their host's survival, and a means to cope with stressful conditions. 50 51 Associations between the cnidarian host and specific genera, species or strains of 52 Symbiodiniaceae profoundly influence the stress resilience of their coral host (Berkelmans and 53

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“…CCMP827 lost 50% of its initial pigment content at 34 • C (Takahashi et al, 2013), but Symbiodinium sp. (Avir) tolerated a wide range (10-35 • C) of temperatures (Pierangelini et al, 2020). These results indicated that Symbiodiniaceae taxa exhibited different photobleaching threshold temperatures, which caused a dramatic loss of photosynthetic pigments and/or plastid photobleaching.…”

Section: Photobleaching Of E Voratum Scs01 Cells Under Thermal Stressmentioning

confidence: 80%

Photobleaching and Recovery of Symbiodiniaceae Effrenium voratum SCS01 Reveals Life Form Transformation Under Thermal Stress

Gong

Jin

et al. 2021

Front. Mar. Sci.

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Dinoflagellates in the family Symbiodiniaceae contain a number of species and play an important role in the establishment of coral reef ecosystems in oligotrophic marine waters. Effrenium voratum is likely an exclusively free-living and heterotrophic species of Symbiodiniaceae. How this species responds and acclimates to warming is largely unknown. The present study experimentally established the phenotypic landscapes related to the photobleaching and recovery processes of Effrenium voratum SCS01 following thermal stress. We found that thermal stress bleached the plastids of E. voratum SCS01 and caused the cells to become lighter in color. Thereafter, the bleached cells recovered rapidly when they returned to the optimal temperature. The dominant life form of E. voratum SCS01 shifted from mastigote cells to coccoid cells then returned to mastigote cells. Transcriptome analysis revealed that the photobleaching of E. voratum SCS01 was due to increased degradation and decreased biosynthesis of photosynthetic pigments. The thermally induced life form changes were related to the downregulation of genes for cell motility. Our results revealed the mechanism of photobleaching in E. voratum SCS01 and indicated life form transformation as a newly identified survival strategy of Effrenium voratum SCS01 under thermal stress.

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Different levels of energetic coupling between photosynthesis and respiration do not determine the occurrence of adaptive responses of Symbiodiniaceae to global warming

Cited by 16 publications

References 93 publications

In vivo assessment of mitochondrial respiratory alternative oxidase activity and cyclic electron flow around photosystem I on small coral fragments

In vivo assessment of mitochondrial respiratory alternative oxidase activity and cyclic electron flow around photosystem I on small coral fragments

Symbiont shuffling across environmental gradients aligns with changes in carbon uptake and translocation in the reef-building coral Pocillopora acuta

Photobleaching and Recovery of Symbiodiniaceae Effrenium voratum SCS01 Reveals Life Form Transformation Under Thermal Stress

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