The Radiolarian species are a diverse group of marine microorganisms. They are known for their intricate and multi-functional silica skeletons. Due to rough oceanic conditions, the formation of a hard silica shell through biomineralization allows them to maintain their shape. The dissolution of their siliceous skeletons at higher ocean depths contributes to the amount of biogenic silica found in the oceans. Hence, they contribute significantly to biochemical ocean cycles such as the biogenic silica cycle. Additionally, studies have determined that polycystine radiolarians possess opaline silica skeletons that have high resistance to dissolution, making them useful at playing the role of environmental indicators. As single-celled organisms, they also communicate and catch their prey by means of bioluminescence. Furthermore, this paper sheds light on the mutualistic symbiotic relationship they have with microalgae, aiding these organisms in acquiring nutrients in low-nutrient ocean regions, while also collecting oxygen from their products of photosynthesis. Understanding the diversity and ecological roles of Radiolaria offers precious insights into paleoceanographic and paleoclimate research and recognizes their significance on marine ecosystems.
Belonging to the supergroup Rhizaria, Radiolarians are marine amoeboid protists that are separated into three major groups: Polycystina, Acantharia and Phaeodaria. These groups comprise several classes: Taxopodia, Acantharia, Spumellaria, Nassellaria and Collodoria (Fig. 1). Radiolarians have skeletons made primarily of amorphous opaline silica (SiO2⋅nH2O), with minor elements like magnesium, calcium, aluminum, and sodium, formed partly due to their uptake of silicic acid (Afanasieva & Amon, 2014).The only class that is excluded for this fact is Acantharia, known to be unique due to their base skeletal component being strontium sulfate (SrSO4) instead of opaline silica.
Figure. 1 The different known radiolarian orders and their general characteristics (Mansour, 2021).
The radiolarian cell structure is composed of a double layered cytoplasm that divides the endoplasm from the ectoplasm by a thin capsular membrane, as well as a central capsule and their pseudopodia (Mansour, 2021). The endoplasm and the central capsule combined contain organelles, food vacuoles, nuclei, ribosomes, mitochondria and, in the case of Acantharia, algal symbionts that makes photosynthesis possible (Fig.2). Pseudopodia are important cellular components that are used for feeding, buoyancy control and locomotion, all possible due to their contraction and elongation mechanisms (Mansour, 2021). In the case of Collodaria, they differ in their general morphology, being composed of a gelatinous matrix that contains multiple central capsules.
Figure 2 Schematic representation of a Acantharia radiolarian with strontium sulfate spicules, its endoplasm, ectoplasm and the thin capsular membrane (Perry et al., 1988).
Radiolaria are globally distributed in the ocean, but the abundance of their populations in certain depths and areas are determined by environmental factors, such as temperature, salinity, productivity and nutrient accessibility (Llopis Monferrer et al., 2020). Even though they are frequently encountered in the oceans, little is known regarding their feeding behavior. Generally, they are heterotrophic protists and usually carnivorous, in fact, ciliates tintinnids seem to be their preferred prey. Contrarily to the colonial Collodaria, the rest of the radiolarians ingest their prey by externally assimilating digested materials in food vacuoles found in the ectoplasm (Suzuki & Not, 2015). Aside from being heterotrophic feeders, various radiolarian species that live in the photic zones of the oceans develop symbiotic relationships with microalgae.
Biomineralization
A defining feature of Radiolaria is their intricate silica-based skeletons. The key process responsible for the formation of their skeleton is through biomineralization. It refers to how living organisms produce minerals, often to harden or stiffen existing tissues, offering structural support. Biomineralization involves a process by which living organisms deposit mineral crystals within their organic matrices. This mechanism leads to the formation of inorganic skeletal structures which provides support and shape to the body, while also playing a critical role in their metabolism. According to Banfield et al. (1999), the radiolarian skeleton itself can serve as a platform for enzymatic reactions involved in the organism’s metabolism. The extensive surface area provided by the skeletal structures can facilitate the attachment of enzymes that are involved in various biochemical pathways, including those involved in nutrient processing and waste management within the cell. This is analogous to the role of mineral surfaces in catalyzing reactions in geochemical environments, where the increased surface area enhances the interaction between reactants and catalytic sites, thus promoting faster reaction kinetics (Banfield et al., 1999).
The primary component of biomineralization in Radiolaria is hydrated silicon dioxide (SiO2), which is absorbed by radiolarians from the seawater in the form of dissolved orthosilicic acid monomers, Si(OH)4 (Afanasieva & Amon, 2014). They are stored in specialized vesicles within their cytoplasm, a process regulated by specific transporter proteins. As the concentration of silicic acid reaches a critical threshold within these vesicles, polymerization is initiated to form silica. Evidence for this is shown by the fine vacuoles with laminated membranes containing silica in the ectoplasm of living radiolarians, indicating that silica is deposited from the cytoplasm rather than being embedded in it (Cachon & Cachon, 1971; Afanasieva, 1990). The polymerization of this flexible and abundant building material is integrated into the polysaccharide plates of the organic matrix. Notably, like all organisms that undergo biomineralization, the organic matrix is crucial to the formation of the skeleton because it acts as a scaffold that provides a template to direct the deposition of the inorganic silica (Anderson, 1983). Additionally, the interaction between the organic matrix and the inorganic components dictates the final form, size, and patterning of the radiolarian skeleton (Afanasieva & Amon, 2014). According to Afanasieva (1990), the organic matrix framework is like a three-dimensional reticulum made up of protein fibrillae and polysaccharide plates, the latter being roughly 1.5 μm in length. (Fig. 3a). These plates are fragments of cellular membranes formed in the Golgi apparatus. When mineralization occurs, the polysaccharide plates become part of the organic matrix, playing a crucial role in guiding the initial orientation of the mineral particles and subsequent formation of the skeleton. This process, termed epitaxis, involves directed mineralization based on the stereochemical interaction between the organic matter of the plates and the mineral particles. However, current studies researching the exact mechanisms of the deposition of silica in the organic matrix are still lacking since cultivating Radiolaria in the laboratory is nearly impossible (Perry & Keeling-Tucker, 2000).
Figure 3 Stages and microstructure of radiolarian skeleton biomineralization: (a) Initial stage of biomineralization with protein fibrils and a polysaccharide plate attracting orthosilicic acid ions, (b) schematic of the silica deposition process within organic lamellae, (c) transmission electron microscopy image of the primary opal globules on ultra-thin sections of living radiolarians (d) scanning electron microscopy (SEM) image of silica globules aggregating into structural units, (e) SEM image of the assembly of globules into ultrastructural units, with an example from the radiolarian species, Bentonicosphaera triangulata (Afanasieva & Amon, 2014).
The product of the polymerization of orthosilicic acid are termed ‘SiO2 sols.’ According to Melnic et al. (1973) (as cited in Afanasieva, 1990), these silica sols are colloidal suspensions wherein the balance between colloidal and molecular-dissolved constituents of orthosilicic acid varies with pH. At a pH that ranges from 8.3-9.0, which is slightly alkaline, they are predominantly composed of colloidal globular particles. In the context of radiolarians, such conditions are presumed to be replicated within the primary organic matrix of their skeleton, allowing the formation of globular opal. These primary silica globules (E) as seen in Figure 3b then aggregate, forming ultrastructural units (D). The size of these (D) globules ranges from 0.2 to 0.3 μm. The formation of skeleton ultrastructure marks the interval between “the critical reaction yield” and the “point of gelatinization” (Afanasieva, 1990). Then, the individual (D) globules further associate into larger ultrastructural units, referred to as (C) globules, which range from 0.4 to 1 μm in size. This stage corresponds to the “point of gelatinization,” where the skeleton begins to take on a more solid form. During the slow silicification process, the intervals between C globules are filled with primary E globules. The silica globules, termed C, continue to aggregate into larger ultrastructural units known as B. These units take the shape of isometric plates, often hexagonal, which range from 1 to 3 micrometers in diameter and maintain the thickness of the smaller globules (C) (Fig. 3b). The largest structural elements within the radiolarian skeleton, designated as A, are between 3 and 10 μm in diameter. These A units encapsulate the entirety of the preceding units (B, C, D, E), representing the culmination of the hierarchical biomineralization process.
At the molecular level, the fundamental characteristics of the radiolarian skeleton are predominantly governed by the properties of silicon (Si) and oxygen (O) atoms, specifically the energetic properties of the Si–O bond (Afanasieva, 1990). Hydrated silicon dioxide’s unique crystallochemical properties dictate that its mineral substance consistently exhibits specific spatial formations in the forms of chains, bands, and layers, as visually represented in Figure 4 (Afanasieva & Amon, 2014).
Figure 4 Illustrations of Basic Silicate Tetrahedra and Various Complex Tetrahedral Groups. (a) represents the [SiO4]-4 tetrahedron, known as the orthogroup; (b) shows the dimer [Si2O7]-6, referred to as the diorthogroup; (c) is the [Si3O9]-6 trimer; (d) depicts the [Si4O12]-8 ring structure; (e) represents the [Si6O18]-12 chain structure; and (f) illustrates the densely packed tetrahedral groups surrounding a central Si+4 ion within a cubic arrangement, with silicon atoms indicated in black(Afanasieva & Amon, 2014).
Perry and Keeling-Tucker (2000) suggests that the polymerization process of Si(OH)4 monomers in Radiolaria can be described by a series of condensation reactions. The first reaction involves Si(OH)4 and Si(OH)3O– (the ionized form of Si(OH)4), which both have the form of a tetrahedral (Fig. 4a), and produces a dimer (disilicic acid, Fig. 4b) and OH–:
Si(OH)4 + Si(OH)3O–→ (OH)3(Si-O-Si)(OH)3 + OH–
Subsequently, these dimers can further react with Si(OH)3O– and monomeric orthosilicic acid to form a trimeric species (Fig. 4c):
Si(OH)3O– + Disilicic acid → Trisilicic acid + OH–
Si(OH)4 + [Disilicic acid]– → Trisilicic acid + OH–
Further polymerization can occur as trimers react with Si(OH)3O– or 2 dimers react with each other to create larger oligomeric structures like tetrameric silica (Fig. 4d):
Disilicilic acid + Disilicilic acid → Tetrasilicilic acid + OH–
Si(OH)3O– + Trisilicic acid → Tetrasilicilic acid + OH–
This process can continue with oligomers reacting with monomers to form even larger oligomeric chains, progressively releasing water as a byproduct:
Si(OH)4 + [Oligomer]– → (Larger Oligomer) + OH–
These reactions are catalyzed in the mildly alkaline conditions found within the microenvironment of the radiolarian cell, where the pH is conducive to silica polymerization. In these conditions, monomeric silica can penetrate the cell and undergo polymerization within the organic matrix to form colloidal silica (Afanasieva, 1990). Moreover, these polymerization reactions are driven by the decrease in the concentration of the monomeric silicic acid and the removal of the byproduct OH–, which shifts the equilibrium towards the formation of larger oligomers. Over time, as these particles aggregate to form dense three-dimensional networks, they create the solid structures characteristic of radiolarian skeletons (Perry & Keeling-Tucker, 2000).
Dissolution
Once radiolarians die, their silica-based skeletons undergo dissolution in seawater as they descend towards the ocean to settle and form radiolarite. Curiously, this dissolution isn’t uniform. Certain structures, possibly due to their unique compositions, disintegrate faster than others. This selective dissolution plays a part in determining which radiolarian remnants ultimately get embedded in marine sediments. This process of dissolution of silica-based skeletons is determined by water temperature, water concentration of silica, pH and pressure levels, as well as the specific surface area of the skeletons (Fig.1) (Erez et al., 1982). Concerning the overall silica concentration in ocean waters, it averages from 0.01µM to around 7.2 µM, however, the concentration according to sea depth vary, where silica is more concentrated at lower sea levels compared to surface levels (Kido & Nishimura, 1975). Absorption of inorganic or organic solutes may modify the surface reactivity of biogenic silica, for example, by polarizing Si-O-Si bonds in the surface lattice or blocking reactive surface sites.
More is known on the dependence of biogenic dissolution kinetics on temperature and the degree of undersaturation (Van Cappellen et al., 2002). In addition, these two variables show systematic differences between the euphotic zone and deep-sea sediments. Temperatures are generally lower at the seafloor, while degrees of undersaturation are highest at the sea surface. The latter reflects the very efficient removal of silicic acid by diatoms, and hence the very low concentrations of H4SiO4 in ocean surface waters. Both colder temperatures and lower degrees of undersaturation result in lower specific silica dissolution rates in deep-sea sediments.
Contribution of skeleton dissolution to the silica biogeochemical cycle
Importantly, along with other organisms in the supergroup of rhizarians, radiolarians are known to contribute to the marine organic carbon (C) and biogenic silica (bSi) pools. Concerning the silica pools, radiolarians highly impact this cycle due to their silica-based skeletal structures that are formed by extracting silicic acid from seawater. Their use of silicic acid from the water promotes a better skeletal structure, thus providing better mechanical protection, defense, more efficient pH buffering and better element uptake and storage (Llopis Monferrer et al., 2020). Polycystine radiolarians exhibit the ability to extract silicic acid at a rate of about 200-2000 pmol of Si per cell per day.
They also have a great impact on the biological carbon pump and the bSi production, because when radiolarians die, their skeletons sink to the bottom of the ocean, and their skeleton can become part of the sediment. This type of sediment is called radiolarite and it can also carry some organic matter (like carbon) into the ocean floor, entrapping the matter over time. However, like mentionned, during the process of the descent of their skeleton to the bottom, some of the silica (bSi) can also dissolve, forcing it to return as silicic acid in the water (Si(OH)4), while some organic matter (like carbon) can also be expelled back into the water (Llopis Monferrer et al., 2020).
Overall, it is thought that siliceous radiolarians significantly contribute to the production and the amount of biogenic silica in the oceans. Contributing to the marine stock of bSi by 0.2 to 2.2 mmol Si per m2 and the overall production of bSi by 2 to 58 Tmol Si per year, equivalent to 1 % to 19 % of the total production each year (Llopis Monferrer et al., 2020).
Like many other marine organisms, siliceous radiolarians can emit light through bioluminescence. Such luminescence is a result of a natural chemical reaction that allows species living in deep waters to produce light, and for some, this is the only source accessible. Furthermore, bioluminescence also plays a significant role in terms of communication, impacting how the organisms interact, defend themselves, and reproduce. This natural production of light typically relies on the oxidation of a luciferin, a light-emitting molecule, for which only four different types were discovered, although it is certain that more exist (Haddock, 2010). To control the reaction rate, an enzyme is involved in the reaction. The enzyme is either a luciferase or a photoprotein, the latter being a variant of luciferase, but with different light emitting factors bounded together, like luciferin and oxygen. In a case involving a photoprotein, the production of light is triggered when the photoprotein binds an ion or a cofactor (such as Ca2+or Mg2+), causing the protein to undergo a conformational change and emit energy (Haddock, 2010).
Radiolaria rely on coelenterazine as their type of luciferin (Fig. 4). Structurally, coelenterazine is formed by a combination of 5- and 6-membered rings that contains nitrogen, which is believed to biosynthesize through the cyclization of a precursor such as Phe-Tyr-Tyr (Fig.5). More particularly, radiolarians use coelenterazine in combination with photoproteins, like aequorin, Mitrocoma, Clytia, Obelia and symplectin (Haddock, 2010). The more common order of radiolarians known to be bioluminescent are the Collodaria. They are known to use coelenterazine that is bound to Ca2+ activated photoproteins, which are remarkably obtained through their diets, by consuming larger preys.
Figure 5 Molecular structure of coelenterazine (Haddock, 2010).
Figure 6. Molecular structure of the tripeptide phenylalanine-tyrosine-tyrosine (FYY) (Francis et al., 2015).
Photosymbiosis
One of the greatest examples of evolution at work is mutualistic symbiosis. In order to survive, organisms of different species have adapted to rely on each other in ways that result in a net benefit for all parties (Dimijian G. G., 2000). These symbiotic relationships are seen all around us, wasps and fig fruit plants, corals and sponges, even mammals and gut bacteria. In the case of Radiolaria, symbiosis can be observed between them and certain types of algae (Anderson, O. R., 2001). More specifically, these two organisms provide an example of both endosymbiosis and photosymbiosis. Endosymbiosis involves one organism acting as a host for a smaller organism (Mansour, J., 2021). Photosymbiosis occurs specifically when the smaller organism is a photoautotroph, meaning an organism that carries out photosynthesis (Stanley, G. D., 2006). Radiolaria fill the role of host organism for algal symbionts that live in the peripheral cytoplasm of the Radiolaria’s central body (Anderson, O. R., 2001). These species heavily differ in taxonomy and physiology but are able to live in lifelong harmony in order to provide necessary gains to both organisms.
Not all types of Radiolaria are able to live in photosymbiotic relationships. Since the endosymbiont (smaller organism living within the host) requires daily exposure to sunlight, only surface-dwelling radiolarians exhibit photosymbiosis (Anderson, O. R., 2001). Specifically, the taxa Arthracanthida and Symphiacanthida of the Acantharean class of Radiolaria are commonly observed in surface waters of the tropical oligotrophic regions, making them ideal photosymbiotic hosts (Biard, T., 2022). In fact, due to the size of Acantharia, they can host an average of 6 symbionts each. Remarkably, the larger hosts may contain up to 40 symbionts. Based on their sarcodine-symbiont production rates, host acanthareans can account for up to 20% of carbon fixation in the oligotrophic region’s euphotic zone (Michaels, A.F., 1988). This specific oceanic region is low in nutrients and biomass. Contrastingly, the peripheral cytoplasm of the Acantharia’s core that the microalgal symbionts call home is nutrient rich. The products of photosynthesis carried out by the endosymbionts are called photosynthates and are used by the host Radiolaria to supplement food ingestion in order to sustain metabolic activity and growth. This mutual nutritional need is the driving force behind the highly beneficial photosymbiotic relationship between acanthareans and the specific genus of algae Phaeocystis (Biard, T., 2022).
Chemistry of Photosynthesis
In general, photosynthesis is a process that takes in carbon and water to produce carbohydrates (commonly glucose) and oxygen with the equation below.
6CO2 + 6H2O → C6H12O6 + 6O2 (1)
This equation is a simplification of the multitude of biochemically complex processes that make up photosynthesis. There are two main steps in photosynthesis, the light dependent reactions, and the light independent reactions.
Light Dependent Reactions
The light dependent reactions come first, which occur in the thylakoid membrane of the chloroplast (a photosynthesis specialized organelle). The thylakoid membrane is a phospholipid bilayer, which is highly efficient at maintaining ionic concentration gradients. To begin, a photon of light, which is produced by fusion reactions in our sun, is absorbed by pigments within the thylakoid membrane. There are various pigments involved, however the most abundant in Phaeocystis algae is chlorophyll 
(van Leeuwe, M. A., & Stefels, J., 2007). Chlorophyll is an organic molecule, specifically called a porphyrin. The molecular structure of chlorophyll has an array of rings that all converge to a magnesium cation at the center. The rings themselves have various double bonds which, in tandem with the molecule’s long hydrocarbon chain, allows for a high number of delocalized electrons, which in turn means the molecule is able to more efficiently absorb photons.
Figure 7. The molecular structure of chlorophyll The structure exhibits a central magnesium cation with four surrounding nitrogen atoms. The cluster of carbon rings is attached to a long hydrocarbon tail with an ester group (American Chemical Society, 2023).
Chlorophyll absorbs most visible light, except green light. This is why chlorophyll pigments appear green and can be understood by the chlorophyll absorption spectrum represented by the blue curve below.
Figure 8 The absorption spectrum of chlorophyll a and chlorophyll b on an absorbance over wavelength graph (Milne et al., 2015).
The chlorophyll molecules are organized in photosystems that are imbedded in the thylakoid membrane. Photosystem II (also known as plastoquinone oxidoreductase) comes first and contains around 30 chlorophyll molecules which, with the help of the antenna light harvesting complexes, absorb wavelengths of light around 680nm. When a photon is absorbed by a chlorophyll dimer molecule, it is oxidized, which induces a conformation change that leads to the excitation of a delocalized electron in the molecule (Jean-David, R., 2016). The electron then falls back down to ground state, releasing energy in the process. This energy then excites a neighboring chlorophyll. This process is called resonance energy transfer and is repeated until the energy reaches the reaction center of the photosystem (Schöck, 2023). The reaction center is where the central, final chlorophyll exists. The final chlorophyll is excited, and the electron once again jumps up to a higher energy state. This excited electron is taken by the mobile electron receiver pheophytin. Pheophytin then shuttles the electron to the first round of electron transport chain (ETC). This leaves the reaction center of Photosystem II electron deficient. So, Photosystem II performs hydrolysis, which is the splitting of a stable H2O molecule. The splitting releases an electron that is then taken by the chlorophyll in order to replenish the photosystem’s electron supply. Additionally, hydrogen ions and oxygen are produced as byproducts of hydrolysis. The hydrogen ions continue to contribute to the concentration gradient created in the electron transport chain. The oxygen molecules are released. This step is crucial for the algae/Radiolaria symbiosis since they require oxygen to perform cellular respiration.
Pheophytin carries the electrons to the thylakoid membrane protein complex, cytochrome b6f complex (Cyt b6f). This complex acts as an intermediary between Photosystem II and Photosystem I, it uses the energy from pheophytins electrons to pump another hydrogen proton across the lipid bilayer and into the thylakoid. The energy from this reaction is then used to fuel the electron transport chain.
In overview, the electron transport chain (ETC) is a series of redox reactions that occur within protein complexes that are imbedded in the thylakoid membrane. The goal of ETC is to convert the energy from the electrons from photosystem II into energy that is usable by the algae. These reactions generate a proton gradient across the membrane that is used to power the production of ATP during oxidative phosphorylation by ATP synthase.
Figure 9 A schematic showing the electron transport chain process in photosynthesis. The red arrows show linear electron flow, and the blue show cyclic electron flow (Najafpour, M., 2016).
After the synthesis of ATP has been carried out, the electrons are in a much lower energy state than when they entered the ETC. To combat this, the electron is reenergized in Photosystem I. This photosystem is very similar to the Photosystem II as it uses the same proteins and chlorophylls. However, this time, when the energy from an absorbed photon reaches the reaction center, all the energy of the excited electron is used by the enzyme NADP+ reductase to combine two electrons, one hydrogen ion, and NADP+ to produce NADPH. When all is said and done, the light dependent reactions have produced energy carriers NADPH and ATP, as well as oxygen.
Figure 10 A Z schematic of the light dependent reactions. Specifically, the double excitation via
Photosystems II and I, as well as the generation of ATP after PSII and the generation of NADPH after PSI I (Wang et al., 2018).
Light Independent Reaction: The Calvin Cycle
The Calvin Cycle is the final step in photosynthesis and occurs in the stroma, which is the empty space within chloroplasts. In general, the Calvin Cycle is a system that algae use to create necessary sugars from carbon dioxide. The system is driven by the ATP and NADPH created as products of the light dependent reactions. This essential cycle can be broken down into three stages. The first stage is carbon fixation, which is the attachment of a ribulose biphosphate onto a carbon from carbon dioxide with the help of the enzyme 1,5-biphosphate carboxylase oxidase (RuBisCo). The product of this reaction is a six-carbon molecule that is highly unstable and thus immediately separates into two 3 carbon molecules: 3-phosphoglycerate. The second stage is reduction, which is the conversion of 3-phosphoglycerate into the high energy molecule, glyceraldehyde-3-phosphate. This is done by ATP adding a phosphate group, followed by NADPH adding electrons. This product is the end goal since glyceraldehyde-3-phosphate is taken out of the cycle to create various carbohydrates, including glucose, cellulose, and starch. However, the cycle requires five glyceraldehyde-3-phosphate molecules to replenish the ribulose biphosphate supply in order to keep the cycle running. Since the reduction stage produces six glyceraldehyde-3-phosphate molecules, only one gets to leave the cycle to be made into a carbohydrate. To create the most common carbohydrate, glucose, six carbon atoms are needed. So, the cycle only produces a glucose molecule every six cycles. After reduction comes the regeneration stage. This stage is where another series of reactions uses the five glyceraldehyde-3-phosphate molecules to regenerate the ribulose biphosphate supply. Then, the cycle can be repeated. These photosynthetic processes were first developed 2.5 billion years ago and have stood the evolutionary test of time, being observed in many of the Earth’s organisms (Olson, J. M., & Blankenship, R. E., 2004).
Adapting to Light Conditions
To adapt to different conditions, algae have evolved a variety of mechanisms to account for their changing environment. In particular, algae must adapt to varying light quantity conditions in their environments. To solve this problem, organisms use the photosystem complexes as funnels for sunlight into the reaction centers to increase their absorption cross-section. There are further regulatory controls that are used by algae in order to manage the flux of energy received by the reaction centers. Under limited sunlight conditions, light absorption is optimized by the reversible relocation of part of the light harvesting complex between the two photosystems in order to adjust the organization of the antenna system within the photosystems. This process is known as a state transition. The change in absorption properties is especially relevant to aquatic algae since the penetration of light waves through water lowers the intensity of light due to scattering by the medium. State transitions are programed to not occur during high light conditions by the inactivation of the light harvesting complex kinase, which is the enzyme responsible for the phosphorylation reaction that leads to state transitions.
Figure 11 Schematic of the two states of the photosystems. The basis for the transition from state 1 to 2 is the redox activation of LHCII kinase when sunlight is limited. The basis for the transition back to state 1 is the redox inactivation of LHCII kinase (Allen, J. F., 2003).
For algae, sudden changes in ocean conditions can bring the organism into a much more illuminated environment. In excess sunlight conditions, the surplus of energy is dissipated via nonphotochemical quenching in the form of heat. More specifically, the mechanism works by an increase in electron flow along the ETC which generates a proton gradient and thus the acidification of the thylakoid lumen. This leads to the de-excitation of chlorophyll molecules within the photosystems. The energy emitted by the de-excitation is then dissipated as heat. Since excess energy in the photosynthetic apparatus would cause photodamage, nonphotochemical quenching is an imperative evolutionary solution.
Photodamage is of major concern to photosynthesizing organisms. Since the water splitting oxidation reaction is one of the strongest of its kind found in nature, photodamage is exceedingly relevant to photosystem II (Jean-David, R., 2016). To combat this, the system has come up with a repair cycle. The reaction center experiences the most concentrated energy during resonance energy transfer. As such, the protein within it must be replaced by a new copy after it isdamaged by light radiation. Photosystem II consists of a dimer whose monomers contain 28 subunits. The replacement occurs through the phosphorylation of these subunits by a specialized enzyme. The phosphorylation allows for the disassembly of the photosystem, the degradation of the existing reaction center protein, the addition of the newly synthesized version and reassembly of the photosystem. Additionally, the photosynthetic apparatus has a multitude of complex responses to other changes in the algae’s environment. These include responses to nutrient depletion, and long-term chloroplast gene expression changes.
With the help of the skeletons of Radiolaria acting to focus light for the absorption by algae, the efficiency of photosynthetic process has been greatly improved through evolutionary adaptation. Since Radiolaria relies on algae to obtain photosynthates to supplement their own nutrient intake and carry out cellular respiration, efficient algal photosynthesis is imperative. If photosynthesis is no longer efficient, then neither organism is benefiting from the symbiotic relationship. As such, these various algae mechanisms and photosynthetic procedures have been fine-tuned by evolutionary pressures both for its own benefit and to prolong its endosymbiosis with Radiolaria.
Radiolaria is an amazing organism that demonstrates potential for new scientific advancements. In fact, they are already used in paleontological discovery. These organisms have biogenic silica structures that are well preserved in surface sediment (Fig.11). Polycystine radiolarians such as Collodaria, Spumellaria, Orodaria, and Nassellaria have skeletons made of opaline silica. Their skeletons are fairly affected by the dissolution in the water column, And these organisms have been shown to reach the bottom of the ocean with minimal change in their composition (Qu et al., 2020). They show great resistance to dissolution on the seafloor where dissolution is more prone to occur due to the formation of thin Alrich opal coating over their skeletons. Thus, an abundance of Polycystine skeletons have been found in the sediments of the North Pacific oceans (amongst others). Contrary to Radiolaria, foraminifera shells dissolve completely when they vertically drop below the calcite compensation depth. Fossilized radiolarians can be utilized in paleoenvironmental reconstructions in high-altitude and open ocean areas, where many microfossil groups struggle with problems regarding dissolution and low density. Due to their planktonic life cycle, their relative abundance is primarily correlated with surface water mass characteristics such as temperature, salinity, productivity, and nutrients. A study was done on the abundance of different species in the southwest Pacific/Southern Ocean and found that surface hydrography was influenced by the degree of abundance of radiolarians (Qu et al., 2020).
Figure 12 Diversity of the different polycystine Radiolaria orders. E-F. Spumellaria, G-H. Nassellaria, I-J. Orodaria, K-L. Collodaria (Biard, 2022).
Keep in mind, the distribution of radiolarian depends on ocean currents as well. Research from sediments in the East China seas used Q-mode factor analysis to determine that the distribution of Radiolaria fauna is highly influenced by the Kuroshio and Oyashio Currents. The Kuroshio Current is responsible for bringing warm and saline waters from the western tropical North Pacific (Qu et al., 2020). However, it was found that the Kuroshio Current has very minimal control over this phenomenon in the Northern South China seas. The Oyashio Current is responsible for bringing cold, high in nutrients, and low salinity waters southward along the Eastern coast of Japan (Yasudomi et al., 2014).
Radiolaria are most abundant in upper sea layers (0-100 m) (Qu et al., 2020). Although there are some Radiolaria species that live in deeper ocean depths, they account for a small percentage of the total assemblage. Therefore, the analysis of those species would be associated with large uncertainty as they don not offer accurate results (Hernández‐Almeida et al., 2017). On the other hand, those on surface sea layers could be used as environmental indicators of surface conditions such as salinity and temperature.
Figure 13 Relative abundance of the total samples, SCS (South China Sea), ECS (East China Sea), NECB (Nothern East China Bay), and NEC (North East China) samples individually (Qu et al., 2020).
A study was done by retrieving surface sediments samples in the marginal seas of the Western North Pacific, which includes the South China Sea, the East China Sea, and the Philippine Sea, to determine seasonal values of sea surface temperature and salinity (Fig.13). In the study, Spumellaria were found to be predominant in many regions of the SCS and ECS. For example, species that prefer warmer environments, such as Didymocyrtis tetrathalamus, the Euchitonia group, the Phorticium group, and the Tetrapyle group, all belonging to the Nassellaria order, were found to be tracers of Kuroshio Current. Didymocyrtis tetrathalamus were related to low Winter Sea surface temperature (SSTw), high winter sea surface water salinity (SSSw), and low annual silicate (Sia) (Qu et al., 2020). Thus, this species of Radiolaria is suggested to prefer higher salinity and relatively low temperature and silicate concentration. Previously, studies have shown that they are located in warmer waters (low in nutrients) in the tropical and subtropical regions. However, new findings have demonstrated their ability to withstand lower temperatures as well, making them indicators of high salinity in ocean waters. The Tetrapyle group was negatively correlated with SSTw and SSSw and weakly connected with Sia. The abundance of the Tetrapyle group mostly happens in subtropical regions with a lower concentration of salts. Just like D. tetrathalamus, they have adapted to survive in lower temperatures. The Phosticium group was determined to be surface dwellers with temperatures varying between 13–19 °C (resistance to lower temperatures) and high seawater salinity. The Euchitonia group were located in abundance among regions controlled by the Kuroshio Current, however, no results were computed or found regarding their preference of salinity and temperature.
Figure 14 Sea surface oceanographic conditions on annual, winter, and summer timelines in the marginal sea of the Western North Pacific, where (a) Temperature, (b) Salinity, (c) Chlorophyll a, (d) Dissolved Oxygen, (e) Phosphate, (f) Nitrate, (g) Silicate (Qu et al., 2020).
Radiolaria has amazing properties that are beneficial for paleontological research. Their high resistance opaline silica skeletons (found in most species) prevent high levels of dissolution and allow the radiolarian skeleton to stay intact. Thus, these fossilized organisms can be later used for environmental reconstructions and paleoclimatology (Hernández‐Almeida et al., 2017). Their abundance in surface water layers gives the opportunity to use them to research and determine key the properties of surface waters such as temperature and salinity. Moreover, their distribution is partially controlled by different currents such as the Oyashio Current and Kuroshio Current. Hence, they have adapted to tolerate different temperature waters.
Radiolaria are marine amoeboid protists that demonstrate complex chemical processes that allow them to thrive in their changing environments. Ocean conditions are often rough, and as such, Radiolaria require a sturdy structure to keep their shape. This is achieved by biomineralization which is carried out by regulated reactions that occur within specialized vesicles to form organic silica. The organic silica is then embedded, along with polysaccharide plates, into an organic matrix. This matrix acts as the scaffold for the deposition of inorganic silica that governs the final form of Radiolaria’s skeletal structure. The process creates a hardened skeleton that is necessary for structural support and whose fundamental characteristics are governed by the energy properties of silicon-oxygen bonds and enhanced using silicic acid,which promotes better mechanical protection, defense, more efficient pH buffering and better element uptake and storage. Additionally, the biomineralized skeleton can increase surface area available for the attachment of enzymes that regulated metabolic and waste management reactions. This highly specialized formation of skeletal structures demonstrates efficient use of environmental resources and solves radiolarian problems ranging from the need of strong structural support and to raising rate of enzymic reactions.
Remarkably, bioluminescence is used to communicate by the order of Radiolaria Collodaria. It is a reaction that consists of the oxidation of coelenterazine, catalysed by activated photoproteins obtained through their diet. Communication through bioluminescence is essential for organisms living in dark environments (like the deep sea) in order to scare off predators, attract prey, and interact with mates to reproduce. This allows the Radiolaria to obtain nutrients and prolong the survival of both individual Radiolaria and the entire species. Due to these facts, bioluminescence is an exceedingly efficient solution that fills the role of an indispensable communication method for Radiolaria.
Photosymbiosis is an evolutionary adaptation that allows for the prosperity of two species through the quid pro quo of commodities necessary for survival. For the order of Radiolaria Acanthareans, algae Phaeocystis act as photosymbionts that live within the cytoplasm of the Radiolaria’s core. The algae carry out photosynthesis that produces oxygen necessary for Radiolaria. In exchange, the Radiolaria provides a nutrient rich environment (its cytoplasm) for the algae to take habitat. Since photosynthesis is the basis for this evolutionarily favourable relationship, both organisms contribute to its efficiency. The Radiolaria assures the optimization of sunlight exposure by adjusting their vertical position in the water as well as having skeletons that focus light into their core. The algae have various mechanisms to modify photosynthesis and accommodate for varying light/nutrient conditions to avoid photodamage. These optimization techniques have been developed through evolutionary trial and error in order to benefit both parties.
The distribution of Radiolaria is highly impacted by ocean currents, which forces them to adapt in new environments efficiently and according to the conditions. Considering this, and the fact that skeletons from dead Radiolaria fossilize in deep-sea sediment, it emphasizes their potential as environmental indicators. In fact, the non-uniform and low dissolution of organic matter from the skeletons is dictated by colder temperatures and lower degrees of undersaturation. As such, Radiolaria skeletons have acted as valuable environmental indicators for the study of paleoclimatology.
Afanasieva, Marina S. (1990). Experimental evidence for changes during fossilization of radiolarian tests and implications for a model of biomineralization. Marine Micropaleontology, 15(3–4), 233–248. https://doi.org/10.1016/0377-8398(90)90013-c
Afanasieva, M. S., & Amon, E. O. (2014). Biomineralization of radiolarian skeletons. Paleontological Journal, 48(14), 1473-1486. https://doi.org/10.1134/S0031030114140020
Allen, J. F. (2003). State Transitions–a Question of Balance. Science, 299(5612), 1530-1532. https://doi.org/doi:10.1126/science.1082833
American Chemical Society. (2023). 479-61-8. SciFinder.https://scifinder-n.cas.org/searchDetail/substance/654e605b3fddae18b89f7567/substanceDetails
Anderson, O. R. (1983). Radiolaria. https://doi.org/10.1007/978-1-4612-5536-9
Anderson, O. R. (2001). Protozoa, Radiolarians*. Encyclopedia of Ocean Sciences (Second Edition). J. H. Steele. Oxford, Academic Press: 613-617.
Banfield, J. F., Welch, S. A., Zhang, H., Ebert, T. T., & Penn, R. L. (2000). Aggregation-based crystal growth and microstructure development in natural iron oxyhydroxide biomineralization products. Science, 289(5480), 751–754. https://doi.org/10.1126/science.289.5480.751
Biard, T. (2022). Diversity and ecology of Radiolaria in modern oceans. Environmental Microbiology, 24(5), 2179-2200. https://doi.org/10.1111/1462-2920.16004
Bruce F. Milne, Y. T., Angel Rubio, and Steen Brøndsted Nielsen. (2015). “Unraveling the Intrinsic Color of Chlorophyll”. Max Planck Institue for the Structure and Dynamics of Matter, Angewandte Chemie International Edition. https://doi.org/10.1002/anie.201410899
Erez, J., Takahashi, K., & Honjo, S. (1982). In-situ dissolution experiment of radiolaria in the central North Pacific ocean. Earth and Planetary Science Letters, 59(2), 245-254. https://doi.org/https://doi.org/10.1016/0012-821X(82)90129-7
Dimijian G. G. (2000). Evolving together: the biology of symbiosis, part 1.Proceedings (Baylor
University. Medical Center),13(3), 217–226.
Francis, W.,Shaner, N., Christianson, L., Powers, M., & Haddock, S. (2015). Occurrence of Isopenicillin-N-Synthase hom*ologs in Bioluminescent Ctenophores and
Implications for Coelenterazine Biosynthesis. PloS one, 10, e0128742. https://doi.org/10.1371/journal.pone.0128742
Haddock, S.H. D. S. S. H. D. (2010). Bioluminescence in the sea. Annual Review of Marine Science, 2(1), 443-493. Kido, K., & Nishimura, M. (1975). Silica in the sea — its forms and dissolution rate. Deep Sea Research and Oceanographic Abstracts, 22(5), 323-338. https://doi.org/https://doi.org/10.1016/0011-7471(75)90073-X
Hernández‐Almeida, I., Cortese, G., Yu, P. S., Chen, M. T., & Kucera, M. (2017). Environmental determinants of radiolarian assemblages in the western Pacific since the last deglaciation. Paleoceanography, 32(8), 830-847.
Jean-David, R. (2016). The Dynamics of the Photosynthetic Apparatus in Algae. In N.MohammaMahdi
(Ed.), Applied Photosynthesis (pp. Ch. 2). IntechOpen. https://doi.org/10.5772/62261
Kido, K., & Nishimura, M. (1975). Silica in the sea — its forms and dissolution rate. Deep Sea Research and Oceanographic Abstracts, 22(5), 323-338. https://doi.org/https://doi.org/10.1016/0011-7471(75)90073-X
Llopis Monferrer, N., Boltovskoy, D., Tréguer, P., Sandin, M. M., Not, F., & Leynaert, A. (2020). Estimating Biogenic Silica Production of Rhizaria in the Global Ocean [Article]. Global Biogeochemical Cycles, 34(3), Article e2019GB006286. https://doi.org/10.1029/2019GB006286
Mansour, J. (2021). Mixotrophy of photosymbiotic Radiolaria
Étude de la mixotrophie chez les radiolaires photosymbiotiques (Publication Number 2021SORUS425)
Sorbonne Université]. https://theses.hal.science/tel-03696691
Michaels, A.F. (1988). Vertical distribution and abundance of Acantharia and their symbionts.Marine Biology97, 559–569. https://doi-org.proxy3.library.mcgill.ca/10.1007/BF00391052
Najafpour, M. (2016). Applied Photosynthesis: New Progress. BoD–Books on Demand.
Olson, J. M., & Blankenship, R. E. (2004). Thinking about the evolution of photosynthesis. Photosynthesis Research, 80, 373-386.
Perry, C. C., & Keeling-Tucker, T. (2000). Biosilicification: The role of the Organic Matrix in Structure Control. JBIC Journal of Biological Inorganic Chemistry, 5(5), 537–550. https://doi.org/10.1007/s007750000130
Perry, C. C., Wilco*ck, J. R., & Williams, R. J. P. (1988). A physico-chemical approach to
morphogenesis: the roles of inorganic ions and crystals. Experientia, 44(8), 638-650. https://doi.org/10.1007/BF01941024
Qu, H., Wang, J., Xu, Y., & Li, X. (2020). Radiolarian assemblage as an indicator of environmental conditions in the marginal seas of the Western North Pacific. Marine Micropaleontology, 157, 101859.
Yasudomi, Y., Motoyama, I., Oba, T., & Anma, R. (2014). Environmental fluctuations in the northwestern Pacific Ocean during the last interglacial period: evidence from radiolarian assemblages. Marine Micropaleontology, 108, 1-12.
Hernández‐Almeida, I., Cortese, G., Yu, P. S., Chen, M. T., & Kucera, M. (2017). Environmental determinants of radiolarian assemblages in the western Pacific since the last deglaciation. Paleoceanography, 32(8), 830-847.
Suzuki, N., & Not, F. (2015). Biology and ecology of radiolaria. Marine protists: Diversity and dynamics, 179-222.
Stanley, G. D. (2006). Photosymbiosis and the Evolution of Modern Coral Reefs. Science, 312(5775), 857-858. https://doi.org/doi:10.1126/science.1123701
Van Cappellen, P., Dixit, S., & van Beusekom, J. (2002). Biogenic silica dissolution in the oceans: Reconciling experimental and field-based dissolution rates. Global Biogeochemical Cycles, 16(4), 23-21-23-10. https://doi.org/https://doi.org/10.1029/2001GB001431
Van Leeuwe, M. A., & Stefels, J. (2007). Photosynthetic responses in Phaeocystis antarctica towards varying light and iron conditions. Biogeochemistry, 83(1), 61-70. https://doi.org/10.1007/s10533-007-9083-5
Wang, Y., Suzuki, H., Xie, J., Tomita, O., Martin, D. J., Higashi, M., Kong, D., Abe, R., & Tang, J. (2018). Mimicking natural photosynthesis: solar to renewable H2 fuel synthesis by Z-scheme water splitting systems. Chemical reviews, 118(10), 5201-5241.
