Effects of CO2-driven acidification of seawater on the calcification process in the calcareous hydrozoan Millepora alcicornis (Linnaeus, 1758)

Marangoni, Laura Fernandes de Barros; Calderón, Emiliano Nicolas; Marques, Joseane Aparecida; Duarte, Gabriela; Pereira, Cristiano Macedo; Castro, Clovis B.; Bianchini, Adalto

doi:10.1007/s00338-017-1605-6

Cited by 16 publications

(8 citation statements)

References 45 publications

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“…The role of carbonic anhydrase in the calcification process has been studied mainly in scleractinian corals; however, similar mechanisms have already been described in mollusks [2,29,30,31], sponges [32], octocorals [33], hydrocorals [34], gorgonian [35], crabs [36,37], algae [38], and foraminifera [39], exemplifying the essential role of carbonic anhydrase in the regulation of CaCO 3 precipitation in various biological systems.…”

Section: Carbonic Anhydrase and Its Biological Functionmentioning

confidence: 99%

“…Similarly, when the coral S. pistillata was cultivated for 1 year in low-pH water (pH 7.20), a reduction in carbonic anhydrase activity was also observed [86]. In contrast, Marangoni et al (2017) [34] demonstrated that the calcareous hydrozoan Millepora alcicornis elevated the activity of this enzyme following exposure to extreme water acidification (pH 7.20) for 30 days.…”

Section: Carbonic Anhydrase As a Biomarker In Calcifying Organismsmentioning

confidence: 99%

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Carbonic Anhydrase as a Biomarker of Global and Local Impacts: Insights from Calcifying Animals

Zebral

Fonseca

Marques

et al. 2019

IJMS

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The emission of greenhouse gases has grown in unprecedented levels since the beginning of the industrial era. As a result, global climate changes, such as heightened global temperature and ocean acidification, are expected to negatively impact populations. Similarly, industrial and urban unsustainable development are also expected to impose local impacts of their own, such as environmental pollution with organic and inorganic chemicals. As an answer, biomarkers can be used in environmental programs to assess these impacts. These tools are based in the quantification of biochemical and cellular responses of target species that are known to respond in a sensitive and specific way to such stresses. In this context, carbonic anhydrase has shown to be a promising biomarker candidate for the assessment of global and local impacts in biomonitoring programs, especially in marine zones, such as coral reefs, considering the pivotal role of this enzyme in the calcification process. Therefore, the aim of this review is to show the recent advances in the carbonic anhydrase research and the reasons why it can be considered as a promising biomarker to be used for calcifying organisms.

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Section: Carbonic Anhydrase and Its Biological Functionmentioning

confidence: 99%

Section: Carbonic Anhydrase As a Biomarker In Calcifying Organismsmentioning

confidence: 99%

Carbonic Anhydrase as a Biomarker of Global and Local Impacts: Insights from Calcifying Animals

Zebral

Fonseca

Marques

et al. 2019

IJMS

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“…These extracellular and secreted forms were observed to be specifically associated with mineralizing tissues in corals ( 7 , 18 ), sponges ( 16 ), mollusks ( 19 ), and sea urchins ( 20 ). Furthermore, pharmacological experiments using compounds (i.e., acetazolamide) that inhibit CAs demonstrated reductions in calcification rates in sponges ( 21 ), mollusks ( 19 , 22 ), corals ( 23 , 24 ), coccolithophores ( 25 ), and sea urchins ( 6 , 26 – 28 ). While these studies point toward a central role of CAs in the calcification process, their exact mechanism of promoting cellular carbon concentration remains largely hypothetical.…”

mentioning

confidence: 99%

Extracellular carbonic anhydrase activity promotes a carbon concentration mechanism in metazoan calcifying cells

Matt

Chang

2022

Proc. Natl. Acad. Sci. U.S.A.

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Many calcifying organisms utilize metabolic CO 2 to generate CaCO 3 minerals to harden their shells and skeletons. Carbonic anhydrases are evolutionary ancient enzymes that have been proposed to play a key role in the calcification process, with the underlying mechanisms being little understood. Here, we used the calcifying primary mesenchyme cells (PMCs) of sea urchin larva to study the role of cytosolic (iCAs) and extracellular carbonic anhydrases (eCAs) in the cellular carbon concentration mechanism (CCM). Molecular analyses identified iCAs and eCAs in PMCs and highlight the prominent expression of a glycosylphosphatidylinositol-anchored membrane-bound CA (Cara7). Intracellular pH recordings in combination with CO 2 pulse experiments demonstrated iCA activity in PMCs. iCA activity measurements, together with pharmacological approaches, revealed an opposing contribution of iCAs and eCAs on the CCM. H + -selective electrodes were used to demonstrate eCA-catalyzed CO 2 hydration rates at the cell surface. Knockdown of Cara7 reduced extracellular CO 2 hydration rates accompanied by impaired formation of specific skeletal segments. Finally, reduced pH i regulatory capacities during inhibition and knockdown of Cara7 underscore a role of this eCA in cellular HCO 3 − uptake. This work reveals the function of CAs in the cellular CCM of a marine calcifying animal. Extracellular hydration of metabolic CO 2 by Cara7 coupled to HCO 3 − uptake mechanisms mitigates the loss of carbon and reduces the cellular proton load during the mineralization process. The findings of this work provide insights into the cellular mechanisms of an ancient biological process that is capable of utilizing CO 2 to generate a versatile construction material.

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“…Direct comparisons between these findings and our results are challenging because gene expression patterns may not reflect the exact content and function of proteins, due to post-translational modifications. On the other hand, de Barros Marangoni et al (2017) observed a 1.6-fold increase in Ca-ATPase activity in the hydrocoral M. alcicornis exposed to acidified seawater (pH < 7.5) for 30 days but not for 16 days; likewise, Prazeres et al (2015) found that Ca- and Mg-ATPase activities of benthic foraminifera Amphistegina lessonii significantly increased (+50%) after 30 days at pH 7.6, while the 15-days exposure exerted no effect. However, another resistant species Marginopora vertebralis exhibited unaltered Ca-ATPase activity and a 30% inhibition of Mg-ATPase activity following 30-days exposure to lowered pH (Prazeres et al, 2015).…”

Section: Discussionmentioning

confidence: 93%

Diurnally Fluctuating pCO2 Modifies the Physiological Responses of Coral Recruits Under Ocean Acidification

et al. 2019

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Diurnal pCO2 fluctuations have the potential to modulate the biological impact of ocean acidification (OA) on reef calcifiers, yet little is known about the physiological and biochemical responses of scleractinian corals to fluctuating carbonate chemistry under OA. Here, we exposed newly settled Pocillopora damicornis for 7 days to ambient pCO2, steady and elevated pCO2 (stable OA) and diurnally fluctuating pCO2 under future OA scenario (fluctuating OA). We measured the photo-physiology, growth (lateral growth, budding and calcification), oxidative stress and activities of carbonic anhydrase (CA), Ca-ATPase and Mg-ATPase. Results showed that while OA enhanced the photochemical performance of in hospite symbionts, it also increased catalase activity and lipid peroxidation. Furthermore, both OA treatments altered the activities of host and symbiont CA, suggesting functional changes in the uptake of dissolved inorganic carbon (DIC) for photosynthesis and calcification. Most importantly, only the fluctuating OA treatment resulted in a slight drop in calcification with concurrent up-regulation of Ca-ATPase and Mg-ATPase, implying increased energy expenditure on calcification. Consequently, asexual budding rates decreased by 50% under fluctuating OA. These results suggest that diel pCO2 oscillations could modify the physiological responses and potentially alter the energy budget of coral recruits under future OA, and that fluctuating OA is more energetically expensive for the maintenance of coral recruits than stable OA.

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Effects of CO2-driven acidification of seawater on the calcification process in the calcareous hydrozoan Millepora alcicornis (Linnaeus, 1758)

Cited by 16 publications

References 45 publications

Carbonic Anhydrase as a Biomarker of Global and Local Impacts: Insights from Calcifying Animals

Carbonic Anhydrase as a Biomarker of Global and Local Impacts: Insights from Calcifying Animals

Extracellular carbonic anhydrase activity promotes a carbon concentration mechanism in metazoan calcifying cells

Diurnally Fluctuating pCO2 Modifies the Physiological Responses of Coral Recruits Under Ocean Acidification

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