Meeting the photosynthetic demand for inorganic carbon in an alga–invertebrate association: preferential use of CO
            <sub>2</sub>
            by symbionts in the giant clam
            <i>Tridacna gigas</i>

Leggat, William; Rees, Tom ap; Yellowlees, David

doi:10.1098/rspb.2000.1031

Cited by 24 publications

(20 citation statements)

References 26 publications

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“…Little is known about potential host‐factors influencing the holobiont response, but a number of species‐specific variables have been suggested whereby the coral host can alter the algal microenvironment through differences in the amount and type of light reaching symbionts in hospite, host‐based pigments (Dove, ), host skeletal morphology (Enríquez, Méndez, & Iglesias‐Prieto, ; Kaniewska, Anthony, & Hoegh‐Guldberg, ) and tissue thickness (Loya et al., ). Further, a potentially dissolved inorganic carbon (DIC) limited environment in hospite (Jarrold et al., ; Leggat, Rees, & Yellowlees, ; Marubini, Ferrier‐Pagès, Furla, & Allemand, ) could drive differences in photosynthesis between in vitro cultures that may be DIC replete. Alternatively, either the production of ROS by the host itself under heat stress or host antioxidant capacity could have been so high that the increase in ROS produced by WT symbionts at 31°C was relatively insignificant.…”

Section: Discussionmentioning

confidence: 99%

Rapid thermal adaptation in photosymbionts of reef‐building corals

Chakravarti

Beltran

Oppen

2017

Global Change Biology

146

207

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Climate warming is occurring at a rate not experienced by life on Earth for 10 s of millions of years, and it is unknown whether the coral-dinoflagellate (Symbiodinium spp.) symbiosis can evolve fast enough to ensure coral reef persistence. Coral thermal tolerance is partly dependent on the Symbiodinium hosted. Therefore, directed laboratory evolution in Symbiodinium has been proposed as a strategy to enhance coral holobiont thermal tolerance. Using a reciprocal transplant design, we show that the upper temperature tolerance and temperature tolerance range of Symbiodinium C1 increased after ~80 asexual generations (2.5 years) of laboratory thermal selection. Relative to wild-type cells, selected cells showed superior photophysiological performance and growth rate at 31°C in vitro, and performed no worse at 27°C; they also had lower levels of extracellular reactive oxygen species (exROS). In contrast, wild-type cells were unable to photosynthesise or grow at 31°C and produced up to 17 times more exROS. In symbiosis, the increased thermal tolerance acquired ex hospite was less apparent. In recruits of two of three species tested, those harbouring selected cells showed no difference in growth between the 27 and 31°C treatments, and a trend of positive growth at both temperatures. Recruits that were inoculated with wild-type cells, however, showed a significant difference in growth rates between the 27 and 31°C treatments, with a negative growth trend at 31°C. There were no significant differences in the rate and severity of bleaching in coral recruits harbouring wild-type or selected cells. Our findings highlight the need for additional Symbiodinium genotypes to be tested with this assisted evolution approach. Deciphering the genetic basis of enhanced thermal tolerance in Symbiodinium and the cause behind its limited transference to the coral holobiont in this genotype of Symbiodinium C1 are important next steps for developing methods that aim to increase coral bleaching tolerance.

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Section: Discussionmentioning

confidence: 99%

Rapid thermal adaptation in photosymbionts of reef‐building corals

Chakravarti

Beltran

Oppen

2017

Global Change Biology

146

207

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“…Haemolymph C i concentration (Leggat, Rees & Yellowlees 2000), pH (Fitt, Rees & Yellowlees 1995) and glucose (Rees et al 1993b) exhibit a diel cycle in giant clams. These cycles correlate directly with ambient light levels suggesting they are driven by zooxanthellae photosynthesis.…”

Section: Discussionmentioning

confidence: 99%

The impact of bleaching on the metabolic contribution of dinoflagellate symbionts to their giant clam host

Leggat

Buck

Grice

et al. 2003

Plant Cell & Environment

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Bleaching (loss of symbiotic dinoflagellates) is known to significantly decrease the fitness of symbiotic marine invertebrates resulting in reduced growth, fecundity and survival. This report is the first to quantify the effects of bleaching on inorganic carbon (C i ) and ammonium flux, fixation and export of photosynthate to the host, in this case the giant clam Tridacna gigas . The 1998 bleaching event was found to decrease the zooxanthellae population 30-fold when comparing bleached to non-bleached clams. This resulted in significant increases in haemolymph C i and decreases in haemolymph pH and glucose concentration, the predominant photosynthate exported from zooxanthellae in this symbiosis. There was also a decrease in the expression levels of host carbonic anhydrase, an enzyme involved in C i transport to the zooxanthellae, and although host glutamine synthase levels were unaffected, the clams ability to assimilate ammonium was eliminated in bleached individuals, suggesting that photosynthate from the zooxanthellae is required for ammonium assimilation. In an artificial bleaching experiment haemolymph C i ( r 2 = = = = 0.97), pH ( r 2 = = = = 0.94) and glucose levels ( r 2 = = = = 0.95) were correlated to zooxanthellae numbers during both bleaching and recovery. Recovery of the zooxanthellae population, was enhanced four-fold by the addition of organic and inorganic nutrients, as were related haemolymph characteristics. These results highlight the profound physiological changes that occur in symbiotic organisms during and after a bleaching event.

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“…The culture medium was replaced daily to minimize Ci uptake or loss to the atmosphere. Ci concentrations were determined as described in Leggat et al (2000). Dinoflagellates were grown under these conditions for 3 d before being harvested by centrifugation for mRNA isolation.…”

Section: Methodsmentioning

confidence: 99%

“…The culture medium was replaced daily to minimize Ci uptake or loss to the atmosphere. Ci concentrations were determined as described in Leggat et al. (2000).…”

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confidence: 99%

Analysis of an EST library from the dinoflagellate (Symbiodinium sp.) symbiont of reef‐building corals¹

Leggat

Høegh-Guldberg

Dove

et al. 2007

Journal of Phycology

118

120

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Dinoflagellates (Symbiodinium sp. Freud.) are an obligatory endosymbiont of the reef-building corals. Recent changes to the environment surrounding coral reefs (e.g., global warming) have demonstrated that this endosymbiotic relationship between corals and Symbiodinium is particularly sensitive to environmental changes. Therefore, understanding gene expression patterns of Symbiodinium is critical to understanding why coral reefs are susceptible to global climate change. This study identified 1456 unique expression sequence tags (ESTs) generated for Symbiodinium (clade C3) from the staghorn coral Acropora aspera following exposure to a variety of stresses. Of these, only 10% matched previously reported dinoflagellate ESTs, suggesting that the conditions used in the construction of the library resulted in a novel transcriptome. The function of 561 (44%) of these ESTs could be identified. The majority of these genes coded for proteins involved in posttranslational modification, protein turnover, and chaperones (12.3%); energy production and conversion (12%); or an unknown function (18.6%). The most common transcript found was a homologue to a bacterial protein of unknown function. This algal protein is targeted to the chloroplast and is present in those phototrophs that acquired plastids from the red algal lineage. An additional 48 prokaryote-like proteins were also identified, including the first glycerol-phosphate:phosphate antiporter from dinoflagellates. A protein with similarity to the fungi-archael-bacterial heme catalase peroxidases was also found. A variety of stress genes, in particular heat-shock proteins and proteins involved in ubiquitin cascades, were also identified. This study is the first transcriptome from the unicellular component of a eukaryote-eukaryote symbiosis.

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Meeting the photosynthetic demand for inorganic carbon in an alga–invertebrate association: preferential use of CO ₂ by symbionts in the giant clam Tridacna gigas

Cited by 24 publications

References 26 publications

Rapid thermal adaptation in photosymbionts of reef‐building corals

Rapid thermal adaptation in photosymbionts of reef‐building corals

The impact of bleaching on the metabolic contribution of dinoflagellate symbionts to their giant clam host

Analysis of an EST library from the dinoflagellate (Symbiodinium sp.) symbiont of reef‐building corals¹

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Meeting the photosynthetic demand for inorganic carbon in an alga–invertebrate association: preferential use of CO 2 by symbionts in the giant clam Tridacna gigas

Cited by 24 publications

References 26 publications

Rapid thermal adaptation in photosymbionts of reef‐building corals

Rapid thermal adaptation in photosymbionts of reef‐building corals

The impact of bleaching on the metabolic contribution of dinoflagellate symbionts to their giant clam host

Analysis of an EST library from the dinoflagellate (Symbiodinium sp.) symbiont of reef‐building corals1

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Product

Resources

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Meeting the photosynthetic demand for inorganic carbon in an alga–invertebrate association: preferential use of CO ₂ by symbionts in the giant clam Tridacna gigas

Analysis of an EST library from the dinoflagellate (Symbiodinium sp.) symbiont of reef‐building corals¹