Differential localization of ion transporters suggests distinct cellular mechanisms for calcification and photosynthesis between two coral species

Barott, Katie L.; Perez, Sidney O.; Linsmayer, Lauren B.; Tresguerres, Martín

doi:10.1152/ajpregu.00052.2015

Cited by 56 publications

(84 citation statements)

References 57 publications

(60 reference statements)

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“…Two membrane transport proteins are modeled: a Ca-ATPase pump (McConnaughey and Whelan, 1997;Allemand et al, 2004;Barott et al, 2015a) that exchanges 1 mol Ca 2+ for 2 mol H + at the cost of 1 mol ATP (Gattuso et al, 1999) between coelenteron and ECM, and a bicarbonate anion transport [ (Furla et al, 2000;Zoccola et al, 2015); BAT, (Barott et al, 2015a)] that exchanges 1 mol HCO − 3 between coelenteron and ECM. BAT functioning does not require an ATP supply and may be driven by the co-transport of other ions such as Cl − or Na + (Barott et al, 2015a;Zoccola et al, 2015), though those have been neglected as they are not relevant for skeletogenesis and unlikely to be rate-limiting due to high seawater concentrations.…”

Section: Membrane Transport Processesmentioning

confidence: 99%

“…BAT functioning does not require an ATP supply and may be driven by the co-transport of other ions such as Cl − or Na + (Barott et al, 2015a;Zoccola et al, 2015), though those have been neglected as they are not relevant for skeletogenesis and unlikely to be rate-limiting due to high seawater concentrations.…”

Section: Membrane Transport Processesmentioning

confidence: 99%

“…Recent studies uncovered several energy demanding physiological processes involved in coral calcification. There is evidence that Ca 2+ ions are supplied to the ECM via an active transcellular pathway involving Ca-ATPase active membrane transport proteins that would simultaneously remove protons from the ECM (Barott et al, 2015a;Zoccola et al, 2015). Alternatively, protons may be removed from the ECM by an independent proton pumping mechanism (Jokiel, 2011;Ries, 2011), possibly an H-ATPase of the same kind used to acidify the medium where zooxanthellae are located (Barott et al, 2015b).…”

Section: Introductionmentioning

confidence: 99%

“…Alternatively, protons may be removed from the ECM by an independent proton pumping mechanism (Jokiel, 2011;Ries, 2011), possibly an H-ATPase of the same kind used to acidify the medium where zooxanthellae are located (Barott et al, 2015b). Carbon, on the other hand, may reach the ECM trough passive bicarbonate anion transports (BAT) of the SLC4 family (Barott et al, 2015a;Zoccola et al, 2015). Barott et al (2015a) however, also suggest that HCO − 3 transport trough BATs may be driven by the co-transport of Sodium that may reach the ECM through an active Na/K-ATPase pump, thus making also carbon delivery costly.…”

Section: Introductionmentioning

confidence: 99%

“…Carbon, on the other hand, may reach the ECM trough passive bicarbonate anion transports (BAT) of the SLC4 family (Barott et al, 2015a;Zoccola et al, 2015). Barott et al (2015a) however, also suggest that HCO − 3 transport trough BATs may be driven by the co-transport of Sodium that may reach the ECM through an active Na/K-ATPase pump, thus making also carbon delivery costly. However, there is also evidence that not all corals may have evolved the same physiological pathways and mechanisms to control calcification (Barott et al, 2015a;Le Goff et al, 2017), so a complete description of all the processes involved in calcification in corals is still missing.…”

Section: Introductionmentioning

confidence: 99%

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ATP Supply May Contribute to Light-Enhanced Calcification in Corals More Than Abiotic Mechanisms

Galli

Solidoro

2018

Front. Mar. Sci.

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Zooxanthellate corals are known to increase calcification rates when exposed to light, a phenomenon called light-enhanced calcification that is believed to be mediated by symbionts' photosynthetic activity. There is controversy over the mechanism behind this phenomenon, with hypotheses coarsely divided between abiotic and biologically-mediated mechanisms. At the same time, accumulating evidence shows that calcification in corals relies on active ion transport to deliver the skeleton building blocks into the calcifying medium, making it is an energetically costly activity. Here we build on generally accepted conceptual models of the coral calcification machinery and conceptual models of the energetics of coral-zooxanthellae symbiosis to develop a model that can be used to isolate the biologically-mediated and abiotic effects of photosynthesis, respiration, temperature, and seawater chemistry on coral calcification rates and related metabolic costs. We tested this model on data from the Mediterranean scleractinian Cladocora caespitosa, an acidification resistant species. We concluded that most of the variation in calcification rates due to photosynthesis, respiration and temperature can be attributed to biologically-mediated mechanisms, in particular to the ATP supplied to the active ion transports. Abiotic effects are also present but are of smaller magnitude. Instead, the decrease in calcification rates caused by acidification, albeit small, is sustained by both abiotic and biologically-mediated mechanisms. However, there is a substantial extra cost of calcification under acidified conditions. Based on these findings and on a literature review we suggest that the energy aspect of coral calcification might have been so far underappreciated.

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Section: Membrane Transport Processesmentioning

confidence: 99%

Section: Membrane Transport Processesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

ATP Supply May Contribute to Light-Enhanced Calcification in Corals More Than Abiotic Mechanisms

Galli

Solidoro

2018

Front. Mar. Sci.

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Evolutionary links between intra‐ and extracellular acid–base regulation in fish and other aquatic animals

et al. 2020

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The acid-base relevant molecules carbon dioxide (CO2), protons (H + ), and bicarbonate (HCO3 -) are substrates and end products of some of the most essential physiological functions including aerobic and anaerobic respiration, ATP hydrolysis, photosynthesis, and calcification. The structure and function of many enzymes and other macromolecules are highly sensitive to changes in pH, and thus maintaining acidbase homeostasis in the face of metabolic and environmental disturbances is essential for proper cellular function. On the other hand, CO2, H + and HCO3have regulatory effects on various proteins and processes, both directly through allosteric modulation and indirectly through signal transduction pathways. Life in aquatic environments 2 presents organisms with distinct acid-base challenges that are not found in terrestrial environments. These include a relatively high CO2 relative to O2 solubility that prevents internal CO2/HCO3accumulation to buffer pH, a lower O2 content that may favor anaerobic metabolism, and variable environmental CO2, pH and O2 levels that require dynamic adjustments in acid-base homeostatic mechanisms. Additionally, some aquatic animals purposely create acidic or alkaline microenvironments that drive specialized physiological functions. For example, acidifying mechanisms can enhance O2 delivery by red blood cells, lead to ammonia trapping for excretion or buoyancy purposes, or lead to CO2 accumulation to promote photosynthesis by endosymbiotic algae. On the other hand, alkalinizing mechanisms can serve to promote calcium carbonate skeletal formation. This non-exhaustive review summarizes some of the distinct acid-base homeostatic mechanisms that have evolved in aquatic organisms to meet the particular challenges of this environment.

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Changes in gill and air‐breathing organ characteristics during the transition from water‐ to air‐breathing in juvenile Arapaima gigas

et al. 2021

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The obligate air‐breathing Amazonian fish, Arapaima gigas, hatch as water‐breathing larvae but with development, they modify their swim bladder to an air‐breathing organ (ABO) while reducing their gill filaments to avoid oxygen loss. Here, we show that significant changes already take place between 4 weeks (1.6 g) and 11 weeks (5 g) post hatch, with a reduction in gill lamellar surface area, increase in gill diffusion distance, and proliferation of the parenchyma in the ABO. By using a variety of methods, we quantified the surface area and diffusion distances of the gills and skin, and the swim bladder volume and anatomical complexity from hatch to 11‐week‐old juveniles. In addition, we identified the presence of two ionocyte types in the gills and show how these change with development. Until 1.6 g, A. gigas possess only the H+‐excreting/Na+‐absorbing type, while 5‐g fish and adults have an additional ionocyte which likely absorbs H+ and Cl− and excretes HCO3−. The ionocyte density on the gill filaments increased with age and is likely a compensatory mechanism for maintaining ion transport while reducing gill surface area. In the transition from water‐ to air‐breathing, A. gigas likely employs a trimodal respiration utilizing gills, skin, and ABO and thus avoid a respiratory–ion regulatory compromise at the gills.

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Differential localization of ion transporters suggests distinct cellular mechanisms for calcification and photosynthesis between two coral species

Abstract: Barott KL, Perez SO, Linsmayer LB, Tresguerres M. Differential localization of ion transporters suggests distinct cellular mechanisms for calcification and photosynthesis between two coral species.

Cited by 56 publications

References 57 publications

ATP Supply May Contribute to Light-Enhanced Calcification in Corals More Than Abiotic Mechanisms

ATP Supply May Contribute to Light-Enhanced Calcification in Corals More Than Abiotic Mechanisms

Evolutionary links between intra‐ and extracellular acid–base regulation in fish and other aquatic animals

Changes in gill and air‐breathing organ characteristics during the transition from water‐ to air‐breathing in juvenile Arapaima gigas

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