Marine biogenic calcification

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Marine biogenic calcification is the production of calcium carbonate by organisms in the global ocean.

Marine biogenic calcification is the biologically mediated process by which marine organisms produce and deposit calcium carbonate minerals to form

Calcium carbonate plays a fundamental role in the skeletal formation of marine calcifiers. The skeletal structures of these organisms are predominantly composed of calcium carbonate minerals, specifically aragonite and calcite. These structures provide support, protection, and housing for marine calcifiers and are formed through the biochemical processes of biomineralization to precipitate the crystal structures that form the hard tissues of these organisms.

The biogenic formation of calcium carbonate structures is the result of a combination of biological and physical processes such as genetics, cellular activity, crystal competition, growth in confined spaces, and self-organization processes. The composition of these structures, and the mechanisms involved in building them, are highly diverse. For example, some corals can incorporate both calcite and aragonite polymorphs into their skeletons. Some species, like corals and byrozoans, can incorporate other minerals to form complex protein matrices that perform specific functions.^[2][3]

The key steps involved in marine biogenic calcification include the uptake of dissolved calcium ions (Ca²⁺) and carbonate ions (CO₃^2-) from seawater, the precipitation of calcium carbonate crystals, and the controlled formation of skeletal structures through biomineralization processes. These organisms often regulate the calcification process through the secretion of organic molecules and proteins that influence the nucleation and growth of crystalline structures.

A range of biochemical calcification (biocalcification) mechanisms exist, indicated by the fact that marine calcifiers use several different forms of calcium carbonate minerals.^[4] Within this range of mechanisms, there are two broad categories of biogenic calcification in marine organisms: extracellular mineralization and intracellular mineralization.^[4] In particular, mollusks and corals use the extracellular strategy in which ion exchange pumps actively pump ions out of a cell into the extracellular space, where environmental conditions, such as pH, can be tightly controlled.^[4] In contrast, during intracellular mineralization the calcium carbonate is formed within the organism and can either be kept within the organism as an internal structure or is later moved to the outside while retaining the cell membrane covering.^[4] Broadly, the intracellular mechanism pumps ions into a vesicle within the cell.^[4] This vesicle can then be secreted to the outside of the organism. Often, cells will fuse their membranes and combine these vesicles in order to build very large calcium carbonate structures that would not be possible within a single cell.^[4]

Forms of calcium carbonate

The three most common calcium carbonate minerals are

The surface ocean engages in air-sea interactions and absorbs carbon dioxide (CO₂) from the atmosphere, making the ocean the Earth's largest sink for atmospheric CO₂. Carbon dioxide dissolves in and reacts with seawater to form carbonic acid. Subsequent reactions then produce carbonate (CO₃²⁻), bicarbonate (HCO₃⁻), and hydrogen (H⁺) ions. Carbonate and bicarbonate are also deposited into the global ocean by rivers through the weathering of rock formations. The three species of carbon in seawater, carbon dioxide, bicarbonate, and carbonate, make up the total concentration of dissolved organic carbon (DIC) in the ocean. Approximately 90% of DIC is bicarbonate ions, 10% is carbonate ions, and <1% is dissolved carbon dioxide, with some spatial variation. The equilibria reactions between these species result in the buffering of seawater in terms of the concentrations of hydrogen ions present.^[8]

The following chemical reactions exhibit the dissolution of carbon dioxide in seawater and its subsequent reaction with water:

CO₂(g) + H₂O(l) ⥨ H₂CO₃(aq)

H₂CO₃(aq) ⥨ HCO₃^-(aq) + H⁺(aq)

HCO₃^-(aq) ⥨ CO₃²⁻(aq) + H⁺(aq)

This series of reactions governs the pH levels in the ocean and also dictates the saturation state of seawater, indicating how saturated or unsaturated the seawater is with carbonate ions. Consequently, the saturation state significantly influences the balance between the dissolution and calcification processes in marine biogenic calcifiers. When seawater is oversaturated with calcium carbonate, the concentration of calcium ions and carbonate ions exceed the saturation point for a particular mineral, such as aragonite or calcite, which make up the skeletons of many marine organisms. Such conditions are favorable to marine calcifiers for the formation of calcium carbonate skeletons or shells. When seawater is undersaturated, meaning the concentration of calcium and carbonate ions is below the saturation point, it becomes challenging for marine calcifiers to build and maintain their skeletal structures, as the equilibrium conditions favor dissolution of calcium carbonate.^[6] As a general rule, seawater that is undersaturated (Ω < 1) can dissolve the structures of calcifying organisms.^[9] However, many organisms see negative effects on growth at saturation states above Ω = 1. For example, a saturation state of  Ω = 3 is optimal for coral growth, so a saturation state Ω < 3 can potentially have negative effects on coral growth and survival.^[10]

Calcium carbonate saturation can be determined using the following equation:

Ω = ([Ca²⁺][CO₃²⁻])/K_sp

where the numerator ([Ca²⁺][CO₃²⁻]) denotes the concentration of calcium and carbonate ions and the denominator (K_sp) refers to the mineral (solid) phase stoichiometric solubility product of calcium carbonate.^[8]

When saturation is high, organisms can extract calcium and carbonate ions from seawater, forming solid crystals of calcium carbonate:

Ca²⁺(aq) + 2HCO₃⁻(aq) → CaCO₃(s) + CO₂ + H₂O

For marine calcifiers to build and maintain calcium carbonate structures, CaCO₃ production must be greater than CaCO₃ loss through physical, chemical, and biological processes. This net production can be thought of as follows:

CaCO₃ accretion = CaCO₃ production – CaCO₃ dissolution – physical loss of CaCO₃

The decreasing saturation of seawater with respect to calcium carbonate, associated with

The widespread use of calcification by marine organisms has relied on the ability of calcium carbonate to readily form in seawater, where the saturation states (Ω) of aragonite and calcite minerals have consistently surpassed Ω = 1 (indicating oversaturation) in surface waters for hundreds of millions of years.[13] The impacts of reduced calcium carbonate saturation on marine calcifiers have broader ecological implications, as these organisms play vital roles in marine ecosystems. For example, coral reefs, which are built by coral polyps secreting calcium carbonate skeletons, are particularly vulnerable to changes in calcium carbonate saturation.^[14]

There is much debate in the scientific community on whether calcification rates correlate more with carbonate ions and saturation state or with pH. Some researchers state that a correlation exists between calcification and the Ω of carbonate ions in seawater.^[15] Meanwhile, others state that from a physiological standpoint there are numerous marine organisms, and their calcification control is attributed more so to the concentrations of seawater bicarbonate (HCO3−) and protons (H+) rather than the Ω.^[16] Further research is essential to gain a comprehensive understanding of the intricate connections between Ω, ocean acidification, and their impacts on the calcification rates of marine biogenic calcifiers, elucidating the distinct roles played by each.

Marine Calcifying Organisms

Corals

Coral reefs, physical structures formed from calcium carbonate, are important on biological and ecological scales to the regions they are endemic to.^[12] Their robust calcification abilities have resulted in extensive calcium carbonate deposits, some housing significant hydrocarbon reserves.^[17] However, this group only accounts for about 10% of the global production of calcium carbonate.^[18]

Corals undergo extracellular calcification and first develop an organic matrix and skeleton on top of which they will form their calcite structures.^[19] It is proposed that calcification via pH upregulation of the coral's extracellular calcifying fluid occurs at least in part via Ca²⁺-ATPase. Ca²⁺-ATPase is an enzyme in the calicoblastic epithelium that pumps Ca²⁺ ions into the calcifying region and ejects protons (H⁺).^[20] This process circumvents the kinetic barriers to CaCO₃precipitation that exist naturally in seawater.^[20]

Molluscs

Mollusks are a diverse group including slugs, oysters, limpets, snails, scallops, mussels, clams, cephalopods and others. Mollusks employ a strategic approach to protect their soft tissues and deter predation by developing an external calcified shell. This process involves specialized cells following genetic instructions to synthesize minerals under non-equilibrium conditions.^[21] The resulting minerals exhibit complex shapes and sizes along with being formed within a confined space.^[21] These organisms also pump hydrogen out of the calcifying area so that it will not bond to the carbonate ions, which prevents crystallization of calcium carbonate.

Echinoderms

Echinoderms, of the phylum Echinodermata, include organisms such as sea stars, sea urchins, sand dollars, crinoids, sea cucumbers and brittle stars. These organisms form extensive  endoskeletons consisting of magnesium-rich calcite.^[22] Magnesium-rich calcite maintains the chemical composition of CaCO3, yet features substitutions of Mg for Ca as calcite and aragonite are mineral forms or polymorphs of CaCO3. Adult echinoderm skeletons consist of teeth, spines, tests, tubule feet, and in some cases, spicules.^[23] Echinoderms serve as excellent blueprints for biomineralization. Adult sea urchins are a particularly popular species studied to better understand the molecular and cellular processes that the calcification and biomineralization of their skeletal structures requires.^[22] Unlike many other marine calcifiers, echinoderm tests are not formed purely from calcite; instead, their structures also heavily consist of organic matrices that increases the toughness and strength of their endoskeletons.^[23]

Crustaceans

Foraminifera

Foraminifera, or forams, are single-celled protists that form chambered shells (tests) from calcium carbonate.^[25] Forams first appeared approximately 170 million years ago, and populate oceans globally. Forams are microscopic organisms, typically no larger than 1 mm in length.^[25]  The calcification and dissolution of their shells causes changes both in the surface seawater carbonate chemistry, and in deep-water chemistry.^[25] These organisms are excellent paleo-proxies as they record ambient water chemistry during shell formation and are well-preserved in the sedimentary fossil record. Planktonic foraminifera, found in large numbers in the ocean, contribute significantly to oceanic carbonate production.^[26] Unlike their benthic counterparts, more of these species have algal symbionts.

Coccolithophores

Coccolithophorid phytoplankton form CaCO3 in crystalline structures known as coccoliths, with holococcoliths formed externally and heterococcoliths produced intracellularly.[37] Various coccolithophores produce two coccolith types: Heterococcoliths, from diploid cells, are complex, while holococcoliths, from haploid stages, are less studied. Factors influencing life cycle phase transitions and the role of specific proteins like GPA in coccolith morphology are explored.^[37] Polysaccharides, particularly coccolith-associated polysaccharides (CAPs), emerge as key regulators of calcite growth and morphology. CAPs' diverse roles, including nucleation promotion and inhibition, vary between species.^[37] External polysaccharides also influence coccolith adhesion and organization. Recent findings link cellular transport processes, carbonate saturation conditions, and regulatory processes determining calcite precipitation rate and morphology.^[37] Unexpectedly, silicon's role in coccolith morphology regulation is species-dependent, highlighting physiological distinctions among coccolithophore groups. These revelations raise questions about ecological implications, evolutionary adaptations, and the impact of changing ocean silicate levels on coccolithogenesis.^[37]

Calcification rates in coccolithophores often correlate with photosynthesis, implying a potential metabolic role.^[36] Heterococcoliths develop inside intracellular vesicles, with coccolith formation showing a unity ratio with photosynthetic carbon fixation under high calcification rates. The variability in isotope fractionation and calcification mechanisms underscores these organisms' adaptability and complexity in responding to environmental factors.^[36]

For corals, DIC from the seawater is absorbed and transferred to the coral skeleton. An anion exchanger will then be used to secrete DIC at the site of calcification. This DIC pool is also used by algal symbionts (dinoflagellates) that live in the coral tissue.^[38] These algae photosynthesize and produce nutrients, some of which are passed to the coral. The coral in turn will emit ammonium waste products which the algae uptake as nutrients. There has been an observed tenfold increase in calcium carbonate formation in corals containing algal symbionts compared with corals that do not have this symbiotic relationship. The coral algal symbionts, Symbiodinium, show decreased populations with increased temperatures, often leaving the coral colorless and unable to photosynthesize and losing pigments (known as coral bleaching).^[39]

Evolution of biogenic calcification

The evolution of biogenic calcification and carbonate structures within the eukaryotic domain is complex, highlighted by the distribution of mineralized skeletons across major clades.

Phylogenetic insights highlight repeated innovations in carbonate skeleton evolution, raising questions about homology in underlying molecular processes.[40] Skeleton formation involves controlled mineral precipitation in specific biological environments, requiring directed calcium and carbonate transport, molecular templates, and growth inhibitors. Biochemical similarities, including the synthesis of acidic proteins and glycoproteins guiding mineralization, suggest an ancient capacity for carbonate formation in eukaryotes.^[40] While skeletons may not share structural homology, underlying physiological pathways are common, reflecting multiple cooptations of molecular and physiological processes across eukaryotic organisms.^[40]

The

The evolution of mineralized skeletons during the Cambrian did not occur instantly, with a gradual increase in abundance and diversity over 25 million years.[42] Environmental changes and predation pressure played key roles in shaping skeletal evolution. The diversity of minerals and skeletal architectures during this period challenges explanations solely based on changing ocean chemistry. The interplay between genetic possibility and environmental opportunity, influenced by factors like increased oxygen tensions, likely contributed to Cambrian diversification.^[42] Later Cambrian oceans witnessed a decline in mineralized skeletons, potentially influenced by high temperatures and pCO₂ associated with a super greenhouse. Skeletal physiological responses to environmental conditions remain an area of study. Large-scale variations in carbonate chemistry suggest a connection between ocean chemistry and the mineralogy of carbonate precipitation.^[40] Skeletal organisms that precipitate massive skeletons under limited physiological control show stratigraphic patterns corresponding to shifts in seawater chemistry.^[43] This interplay between physiology, evolution, and environment underscores the complexity of mineralized skeleton evolution across geological time.

Calcium carbonate cycling and the biological carbon pump

The calcium carbonate cycle in the global ocean is of great significance to the biological, chemical, and physical state of the ocean. Mineral calcium carbonate most commonly presents as calcite in the ocean, and the majority of calcite is produced biologically in the upper layer of the ocean. CaCO₃ material is exported from the upper ocean to sediments on the ocean floor where it either dissolves or is buried.^[44] Alternatively, CaCO₃ can dissolve or be remineralized within the water column prior to reaching the seafloor.

Upon reaching the seafloor, CaCO₃ undergoes a

Calcium and bicarbonate ions are largely deposited into the ocean from the weathering of rock formations and are transported via riverine input. This process occurs on very long timescales.^[44] Weathering accounts for approximately 60-90% of solute calcium within the global calcium cycle.^[49] Limestone rock, which consists mostly of calcite, is a prime example of a rich source of calcium to the ocean. The source of the majority of inorganic calcium present in the ocean is due to riverine deposition, though volcanic activity interacting with seawater does provide some calcium as well. The distribution of calcium sources described above is the case for both the present day oceanic calcium budget, and the historical budget over the last 25 million years.^[50] The formation of biogenic calcium carbonate is the primary mechanism of removal of calcium in the ocean water column.^[49]

Impact of environmental factors on calcification

Rising temperature and light exposure

Marine biogenic calcifiers, such as corals, are facing challenges due to increasing ocean temperatures, leading to prolonged warming events.

Corals are highly adapted to their local seasonal temperature and light conditions, influencing their physiology and calcification rates.[15] While increased temperature or light levels typically stimulate calcification up to a certain optimum, beyond which rates decline, the effects of temperature and light on the calcifying fluid chemistry are less clear.^[15] Coral calcification is a biologically mediated process influenced by the regulation of internal calcifying fluid chemistry, including pH and dissolved inorganic carbon. The impacts of temperature and light on these factors remain a knowledge gap, with laboratory studies yielding contrasting results.^[15] Decoupling the effects of temperature and light on calcification processes is challenging due to their seasonal co-variation, highlighting the need for further research to address this gap and enhance our understanding of how marine biogenic calcifiers respond to future climate change.^[15]

Ocean Acidification

Calcifying organisms are particularly at risk due to changes in the chemical composition of ocean water associated with ocean acidification. As pH decreases due to ocean acidification, the availability of carbonate ions (CO₃^2-) in seawater also decreases. Therefore, calcifying organisms experience difficulty building and maintaining their skeletons or shells in an acidic environment. There has been considerable debate in the literature regarding whether organisms are responding to reduced pH or reduced mineral saturation state as both variables decline with ocean acidification.^[18][52][53] However, recent studies that have isolated the effects of saturation state independent of pH changes point toward saturation state as the most important factor impacting shell formation development.^[51][54] However, we still need to fully constrain the carbonate chemistry to better interpret the ecological responses around ocean acidification.

Responses of marine calcifiers to reduced carbonate ion availability are seen in different ways. For example, coral reefs experience inhibited growth at decreased pH, and live calcium carbonate structures experience weakening of existing structures.

Ocean acidification (OA) presents a formidable threat to global shellfish production, particularly exerting its impact on calcification processes. Projections indicate that by the end of the century, mussel and oyster calcification could witness substantial reductions of 25% and 10%, respectively, as outlined in the IPCC IS92a scenario, which has an emissions trajectory that results in atmospheric CO2 reaching approximately 740 ppm in 2100.[57] These species, integral to coastal ecosystems and representing a significant portion of global aquaculture, play crucial roles as ecosystem engineers. The anticipated decline in calcification due to OA not only jeopardizes coastal biodiversity and ecosystem functioning but also carries the potential for considerable economic losses. For example, global aquaculture production for shellfish contributed US$29.2 billion to the world economy.^[58]

Damaged shell surfaces, primarily resulting from reduced calcification rates, contribute to a significant decrease in sale prices, marking a critical economic concern. Economic assessments reveal that such damages, particularly impacting culture quasi-profits or applied cultural value, can lead to reductions ranging from 35% to 70%.^[59] Furthermore, when accounting for assumed pH-driven changes occurring concurrently, quasi-profits diminish even more substantially, reaching levels of 49% to 84% across diverse OA scenarios. Consequently, the economic fallout is substantial, with the UK facing potential direct losses of £3 to £6 billion in GDP by 2100, and globally, costs exceeding US$100 billion.^[60] These findings emphasize the urgent need for proactive measures to mitigate OA's impact on bivalve farming and underscore the importance of comprehensive climate policies to address these multifaceted challenges.

Coral reef tourism

For organisms relying on calcified structures (e.g. such as reef-associated organisms), OA can potentially disrupt entire ecosystems. As calcifiers play crucial roles in maintaining marine biodiversity, the repercussions of coral reef decline extend beyond economic considerations, emphasizing the urgency of comprehensive conservation efforts. Extensive degradation is occurring in the Caribbean and Western Atlantic region's coral reefs, stemming from issues like disease, overfishing, and a range of human activities.^[61] Adding to the challenges, rapid climate-induced ocean warming and acidification exacerbate the threats to these vital ecosystems.^[62] Tourism is integral to the Caribbean region with the sector contributing to over 15 percent of GDP and sustaining 13 percent of jobs in the region as a whole.^[63] In the face of these challenges, the worldwide combined economic value of coral reefs is an estimated average of US$490 per hectare annually. Specific regions showcase the economic significance of coral reefs, with Hawai'i's contributing US$360 million annually to its economy, and the Philippine economy receiving at least US$1.06 billion each year from coral reefs.^[61] In the St. Martin region, coral reefs contribute significantly, emphasizing the need for prioritized conservation and protection efforts.^[61] Proposed solutions encompass ecological measures such as water quality management, sustainable fishing practices, ecological engineering, and marine spatial planning. Additionally, socio-economic strategies involve establishing a regional reef secretariat, integrating reef health into blue economy plans, and initiating a reef labeling program to foster corporate partnerships.^[61]

See also

• Ocean acidification - a threat for marine biogenic calcification
• Protist shell
• Seashell
• Shell growth in estuaries

References