Marine biogenic calcification

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. Their robust calcification abilities have resulted in extensive calcium carbonate deposits, some housing significant hydrocarbon reserves. However, this group only accounts for about 10% of the global production of calcium carbonate.

Corals undergo extracellular calcification and first develop an organic matrix and skeleton on top of which they will form their calcite structures. 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⁺). This process circumvents the kinetic barriers to CaCO₃precipitation that exist naturally in seawater.

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. The resulting minerals exhibit complex shapes and sizes along with being formed within a confined space. 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. 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. 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. 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.

Crustaceans

Crustaceans have a hard outer shell formed from calcium carbonate. These organisms form a network of chitin-protein fibers and then precipitate calcium carbonate within this matrix. The chitin-protein fibers are first hardened by sclerotization, or crosslinking of protein and polysaccharides, followed by the crosslinking of proteins with other proteins. The presence of a hard, calcified exoskeleton means that the crustacean has to molt and shed the exoskeleton as its body size increases. This links molting cycles to calcification processes, making access to a regular source of calcium and carbonate ions crucial for the growth and survival of crustaceans. Various body parts of the crustacean will have a different mineral content, varying the hardness at these locations with the harder areas being generally stronger. This calcite shell provides protection for the crustaceans, meaning between molting cycles the crustacean must avoid predators while it waits for its calcite shell to form and harden.

Foraminifera

Foraminifera, or forams, are single-celled protists that form chambered shells (tests) from calcium carbonate. Forams first appeared approximately 170 million years ago, and populate oceans globally. Forams are microscopic organisms, typically no larger than 1 mm in length. The calcification and dissolution of their shells causes changes both in the surface seawater carbonate chemistry, and in deep-water chemistry. 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. Unlike their benthic counterparts, more of these species have algal symbionts.

Coccolithophores

Phytoplankton, especially haptophytes such as coccolithophores, are also well known for their calcium carbonate production. It is estimated that these phytoplankton may contribute up to 70% of the global calcium carbonate precipitation, and coccolithophores are the largest phytoplankton contributors, along with diatoms and dinoflagellates. Contributing between 1 and 10% of total ocean primary productivity, 200 species of coccolithophores live in the ocean, and under the right conditions they can form large blooms. These large bloom formations are a driving force for the export of calcium carbonate from the surface to the deep ocean in what is sometimes called "Coccolith rain". As the coccolithophores sink to the seafloor they contribute to the vertical carbon dioxide gradient in the water column.

Great Calcite Belt of the Southern Ocean

Coccolithophores produce calcite plates termed coccoliths which together cover the entire cell surface forming the coccosphere. The coccoliths are formed using the intracellular strategy where the plates are formed in a coccoliths vesicle, but the product forming within the vesicle varies between the haploid and diploid phases. A coccolithophore in the haploid phase will produce what is called a holococcolith, while one in the diploid phase will produce heterococcoliths. Holococcoliths are small calcite crystals held together in an organic matrix, while heterococcoliths are arrays are larger, more complex calcite crystals. These are often formed over a pre-existing template, giving each plate its particular structure and forming complex designs. Each coccolithophore is a cell surrounded by the exoskeleton coccosphere, but there exists a wide range of sizes, shapes and architectures between different cells. Advantages of these plates may include protection against infection by viruses and bacteria, as well as protection from grazing zooplankton. The calcium carbonate exoskeleton enhances the amount of light the coccolithophore can uptake, increasing the level of photosynthesis. Finally, the coccoliths protect the phytoplankton from photodamage by UV light from the sun.

The coccolithophores are also important in the geological history of Earth. The oldest coccolithophore fossil records are more than 209 million years old, placing their earliest presence in the Late Triassic period. Their calcium carbonate formation may have been the first deposition of carbonate on the seafloor.

Corallinales (red algae)

Calcifying rhodophytes stock their filamentous cell walls with calcium carbonate and magnesium. Corallinales is the one genus of red algae exists but their distribution ranges across the world's oceans. Examples include Corallina, Neogoniolithon, and Harveylithon. The magnesium-rich calcium carbonate of Corallinales cell wall provides shelter from predators and structural integrity in the intertidal zone. The CaCO₃ production in Coralline also plays a role in habitat formation and provides resources for benthic invertebrates.

Calcifying bacteria

Evidence shows that some calcifying cyanobacteria strains have existed for millions of years and contributed to large land formations. About 70 strains of cyanobacteria can precipitate calcium carbonate, including some strains of Synechococcus, Bacillus sphaericus, Bactilus subtilus, and Sporosarcina psychrophile.

Morphological variations in calcium carbonate skeletons

Structural adaptations in different marine organisms

Diverse algae exhibit distinct mechanisms of CaCO₃ formation, with calcification occurring internally or externally. Calcification may play a role in producing CO₂ or supporting processes that need H+, based on the observed partial reaction. Phytoplankton species relying on CO₂ diffusion for photosynthesis may face limitations due to CO₂ concentration and diffusion to the chloroplast's Rubisco site. Calcifying macroalgae like Halimeda and Corallina also produce CaCO₃ in alkaline extracellular spaces.

Coccolithophorid phytoplankton form CaCO₃ in crystalline structures known as coccoliths, with holococcoliths formed externally and heterococcoliths produced intracellularly. 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. 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. 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. 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.

Calcification rates in coccolithophores often correlate with photosynthesis, implying a potential metabolic role. 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.

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. 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).

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. Five out of the eight major clades feature species with mineralized skeletons, and all five clades involve organisms that precipitate calcite or aragonite. Skeletal evolution occurred independently in foraminiferans and echinoderms, suggesting two separate origins of CaCO₃ skeletons. The common ancestry for echinoderm and ascidian skeletons is less clear, but a conservative estimate indicates that carbonate skeletons evolved at least twenty-eight times within Eukarya.

Phylogenetic insights highlight repeated innovations in carbonate skeleton evolution, raising questions about homology in underlying molecular processes. 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. While skeletons may not share structural homology, underlying physiological pathways are common, reflecting multiple cooptations of molecular and physiological processes across eukaryotic organisms.

The Cambrian Period marks a significant watershed in skeletal evolution, with the appearance of mineralized skeletons in various groups. Skeletal diversity increased during this period, driven by predation pressure favoring protective armor evolution. The Cambrian radiation of mineralized skeletons was likely part of a broader animal diversity expansion.

The evolution of mineralized skeletons during the Cambrian did not occur instantly, with a gradual increase in abundance and diversity over 25 million years. 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. 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. Skeletal organisms that precipitate massive skeletons under limited physiological control show stratigraphic patterns corresponding to shifts in seawater chemistry. 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. Alternatively, CaCO₃ can dissolve or be remineralized within the water column prior to reaching the seafloor.

Upon reaching the seafloor, CaCO₃ undergoes a diagenetic process that ends in either dissolution or burial. The distribution of sediments consisting of calcium carbonate is fairly even across the global oceans, but specific locations are determined by the solubility and saturation level of calcium carbonate.

The "biological carbon pump" is a colloquial term coined by scientists to summarize the global carbon cycle in the ocean and its relationship to the biological processes that occur throughout the ocean. The calcium carbonate cycle is inherently linked to the biological pump. The formation of biogenic calcium carbonate by marine calcifiers is one way to add ballast to sinking particles and enhance transport of carbon to the deep ocean and seafloor. The calcium carbonate counter pump refers to the biological process of precipitation of carbonate and the sinking of particulate inorganic carbon. This process releases CO₂ into the surface ocean and atmosphere across timescales spanning 100 to 1,000 years. Its crucial role in regulating atmospheric pCO2 significantly influences global changes in atmospheric CO₂ concentration.

Inorganic sources of calcium carbonate

Of all the metals important to biogeochemical cycles in the ocean, calcium is one of the most significant in both its mobility and the role it plays in regulating climate over millions of years through its presence in calcium carbonate. Calcium has the ability to migrate relatively easily between the hydrosphere, the biosphere, and the crust of the Earth.

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. Weathering accounts for approximately 60-90% of solute calcium within the global calcium cycle. 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. The formation of biogenic calcium carbonate is the primary mechanism of removal of calcium in the ocean water column.

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. When sea surface temperatures exceed the local summer maximum monthly mean, coral bleaching and mortality occur as a result of the breakdown in symbiosis with Symbiodiniaceae. Predicted increases in summer-time temperatures, coupled with ocean warming, are expected to impact coral health and overall rates of calcification, particularly in tropical regions where many corals already live close to their upper thermal limits.

Corals are highly adapted to their local seasonal temperature and light conditions, influencing their physiology and calcification rates. 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. 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. 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.

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. 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. 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. Other organisms are particularly vulnerable in the early stages of their life cycle. Bivalves for instance are particularly susceptible during early larval stages during initial shell formation since these early stages have a high energetic cost to the individual's development. In contrast, adult bivalves are considerably more resilient to reduced pH.

Human interactions and applications

Economic importance

Shellfish industry

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. 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.

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%. 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. 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. Adding to the challenges, rapid climate-induced ocean warming and acidification exacerbate the threats to these vital ecosystems. 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. 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 Hawaiʻi'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. In the St. Martin region, coral reefs contribute significantly, emphasizing the need for prioritized conservation and protection efforts. 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.