Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont <i>Breviolum minutum</i> (Symbiodiniaceae)

Maor-Landaw, Keren; Oppen, Madeleine J. H. van; McFadden, Geoffrey I.

doi:10.1002/ece3.5910

Cited by 49 publications

(63 citation statements)

References 126 publications

(201 reference statements)

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“…The completeness of coral transcriptome was similar with previous research but not the Symbiodiniaceae transcriptome [33,34]. This is because coral larvae were used for RNA extraction, not Symbiodiniaceae pure culture and some Symbiodiniaceae transcripts were discarded if they can be found in coral database.…”

Section: De Novo Assembly Of Reference Transcriptome For Coral and Sysupporting

confidence: 74%

Nutrient gradients simulate different adjustments of coral-algal symbiosis

Tong¹,

Zhou²,

Zhang³

et al. 2020

Preprint

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Background: Eutrophication is one of the major causes of coral reef degradation but the effect of eutrophication on coral and its symbiont algae remains unclear, particularly for the larval stage of coral. In the present study, the physiological and transcriptomic responses of the larvae of an ecologically important scleractinian coral Pocillopora damicornis were analyzed after a 5-day exposure to elevated nitrate in order to assess the survival and adaptation of coral-algal symbiosis under elevated nutrients. Results: The results showed that multiple larval transcripts were significantly correlated with Symbiodiniaceae transcripts. The major differentially expressed transcripts in coral/Symbiodiniaceae included those responsible for energy synthesis/comsumption, nitrogen metabolism and stressor response. Slightly elevated nitrate concentration could in fact promote the health of coral meta-organism. With increase in nitrate concentrations, coral larvae showed significant stress response to maintain the coral-algal symbiosis and coral-algal symbiosis was impaired, while Symbiodiniaceae switched photosynthetic states for ATP synthesis, material transport and nitrogen metabolism for symbiosis maintenance under the control of the coral hosts.Conclusions: Our results suggest that adjustment of coral-algal symbiosis via coral control and a shift in Symbiodiniaceae photosynthetic states serves as the basis of coral meta-organism adaptation under eutrophication stresses. The larvae of P. damicornis and Symbiodiniaceae displayed different transcriptomic responses to nitrate enrichment. Coral larva meta-organism can adapt to moderately elevated nutrient concentration while extreme eutrophication can impair coral-algal symbiosis and affect coral larvae survival ultimately.

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Section: De Novo Assembly Of Reference Transcriptome For Coral and Sysupporting

confidence: 74%

Nutrient gradients simulate different adjustments of coral-algal symbiosis

Tong¹,

Zhou²,

Zhang³

et al. 2020

Preprint

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“…In contrast, genes responsible for ammonia assimilation (GS-GOGAT, CPS1) were upregulated ( Fig. 2D), indicating that ammonium may be readily available to symbionts, as has been shown in several other photosymbioses (36)(37)(38). Together, these results suggest that acantharian hosts may rely on a nutrient-independent mechanism to inhibit symbiont cell division and manage intracellular symbiont populations, a strategy that would give hosts finer control over symbionts while ensuring maximal symbiont productivity.…”

Section: Phaeocystissupporting

confidence: 56%

Cytoklepty in the plankton: a host strategy to optimize the bioenergetic machinery of endosymbiotic algae

Uwizeye

Margaret

Gallet

et al. 2020

Preprint

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Endosymbioses have shaped the evolutionary trajectory of life and remain widespread and ecologically important. Investigating modern oceanic photosymbioses can illuminate how algal endosymbionts are energetically exploited by their heterotrophic hosts, and inform on putative initial steps of plastid acquisition in eukaryotes. By combining 3D subcellular imaging with photophysiology, carbon flux imaging and transcriptomics, we show that cell division of algal endosymbionts (Phaeocystis) is blocked within hosts (Acantharia), and that their cellular architecture and bioenergetic machinery are radically altered. Transcriptional evidence indicates that a nutrient-independent mechanism prevents symbiont cell division and decouples nuclear and plastid division. As endosymbiont plastids proliferate, the volume of the photosynthetic machinery volume increases 100-fold in correlation with expansion of a reticular mitochondrial network in close proximity to plastids. Photosynthetic efficiency tends to increase with cell size and photon propagation modeling indicates that the networked mitochondrial architecture enhances light capture. This is accompanied by 150-fold higher carbon uptake and upregulation of genes involved in photosynthesis and carbon fixation, which, in conjunction with a ca.15-fold size increase of pyrenoids demonstrates enhanced primary production in symbiosis. NanoSIMS analysis revealed major carbon allocation to plastids and transfer to the host cell. Invagination of the symbiosome into endosymbionts to optimize metabolic exchanges is strong evidence that the algal metamorphosis is irreversible. Hosts therefore trigger and unambiguously benefit from major bioenergetic remodeling of symbiotic microalgae with important consequences for the oceanic carbon cycle. Unlike other photosymbioses, this interaction represents a so-called cytoklepty, which is a putative initial step towards plastid acquisition.

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“…Carbon fixation is carried out by a type II Rubisco which is characterized by a low CO 2 -O 2 selectivity factor, and requires the presence of an efficient CO 2 concentrating mechanism 24 , 25 largely controlled by the host 26 , 27 that limits the occurrence of the photorespiratory pathway 24 . After accomplishing carbohydrate synthesis, an important amount of photosynthetic products is transported to the host 28 thanks to the expression of membrane transporters 29 . The photosynthetic activity of corals is dynamic at different levels of time and space scales in coral reefs 30 , and it has been shown to be highly coupled with nutrients 31 and water flow 7 .…”

Section: Introductionmentioning

confidence: 99%

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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Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae)

Cited by 49 publications

References 126 publications

Nutrient gradients simulate different adjustments of coral-algal symbiosis

Nutrient gradients simulate different adjustments of coral-algal symbiosis

Cytoklepty in the plankton: a host strategy to optimize the bioenergetic machinery of endosymbiotic algae

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

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