Algae and the Silicon Cycle

The biogeochemical cycle of silicon (Si) might be interpreted as those processes that link sources and sinks of silicic acid [Si(OH)₄]. Silicic acid is the only precursor in the processing and deposition of silicon in biota. The biogeochemical cycle of silicon does not facilitate a high biospheric abundance of the element, in fact silicon cycle differs from the cycles of carbon, nitrogen, and sulfur and it is similar to phosphorus in that there is no atmospheric reservoir. The silicon cycle, like those for phosphorus and the divalent metals calcium and magnesium, has a significant abiotic drain. It actually consists of two parts: the terrestrial or freshwater cycle and the marine cycle, the former feeding the latter. However, its replenishment can only occur via the marine sedimentary cycle. This is dependent on geotectonic processes, such as mountain building and subduction, and, as such, will incur delays of tens to hundreds of millions years before marine silicon is returned to the terrestrial environment.

The substantial losses of biospheric silicic acid to abiotic sinks may be compensated for in nature by its overall abundance in the Earth’s crust. It is the second most abundant element in the lithosphere (28%), the iron being the first one (35%). It is found in the Earth’s crust in silicate minerals; the most prevalent of which are quartz, the alkali feldspars, and plagioclase. The latter two minerals are aluminosilicates and contribute significantly to the aluminium content of the crust. All of these minerals are broken down by the process of weathering. Important feedbacks exist between autotrophs (algae and plants), weathering, and CO₂.

The dominant form of weathering is the carbonation reaction involving carbonic acid (H₂CO₃), which results in enhanced removal of CO₂ from the atmosphere, because the net effect of silicate mineral weathering is to convert soil carbon, derived ultimately from photosynthesis, into dissolved HCO₃^-. On a geological timescale, this transfer is an important control on the CO₂ content of the atmosphere and hence the global climate. Weathering is a complex function of rainfall, runoff, lithology, temperature, topography, vegetation, and magnitudes. Algae, plants, and their associate microbiota directly affect silicate mineral weathering in several ways: by the generation of organic substances, known as chelates, that have the ability to decompose minerals and rocks by the removal of metallic cations; by modifying pH through the production of CO₂ or organic acids such as acetic, citric, phenolic, etc., and by altering the physical properties of the soil, particularly the exposed surface areas of minerals and the residence time of water.

The significance of this natural process for biota can be found in the detailed geochemistry of the weathering reactions and, in particular, in the rates at which these reactions occur. The rate of mineral weathering is dependent on a number of factors including the temperature, pH, ionic composition of the solvent (or leachate), and hydrogeological parameters such as water flow.

Silicification occurs in three clades of photosynthetic heterokonts: Chrysophyceae (Parmales), Bacillariophyceae, and Dictyochophyceae, with diatoms being the world’s largest contributors to biosilicification. Because amorphous silica is an essential component of the diatom cell wall, silicon availability is a key factor in the regulation of diatom growth in nature; in turn, the use of silicon by diatoms dominates the biogeochemical cycling of silicon in the sea, with each atom of silicon weathered from land passing through a diatom on an average of 39 times before burial in the sea bed.

Several thousand million years ago little if any of the life on Earth was involved in the processing of silicic acid to amorphous silica (SiO_{2 *} nH₂O). The concentration of silicic acid in the aqueous environment was high, of the order of millimolar, and reflected equilibration according to the dominant mineral weathering reactions at that time. The prevalence of these environments rich in silicic acid is indicated in the fossil record by evidence of blue-green algae found encased in silica cherts. It is important to recognize that implicit in this observation is the acceptance that early biochemical evolution proceeded within environments that, relative to the conditions which prevail today, were extremely rich in silicic acid. Concomitant with the advent of dioxygen, and its subsequent gradual increase in atmospheric concentration from approximately 1% towards the level of 21% which is characteristic of today, an increasing number of organisms occurred within which silicic acid was processed to silica. The most important of these, in the terms of their diversity, ubiquity (both freshwater and marine species) and biomass, were the diatoms. The diatoms are characterized by a silica frustule that surrounds their cell wall. Silicic acid is freely diffusible across the cell walls and membranes and, in most cell types of most organisms, the intracellular concentration of silicic acid equilibrates with the extracellular environment according to a Donnan equilibrium (the equilibrium characterized by an unequal distribution of diffusible ions between two ionic solutions separated by a membrane, which is impermeable to at least one of the ionic species present). However, while the intracellular concentration of the silicic acid in the diatom has not been measured it is likely that it is under kinetic as opposed to thermodynamic control and that it is maintained at an extremely low level, probably less than 1 µmol dm^-3. This kinetic control of the intracellular silicic acid concentration may be achieved through the condensation and polymerization of silicic acid in a number of chemical (e.g., pH controlled) and physical (e.g., membrane-bound) compartments eventually resulting in amorphous silica. This biogenic silica is then deposited in a controlled manner to form the intricate and elaborate silica frustules. How all of these remarkable feats of chemistry are achieved within the diatom remains largely unknown. However, what is known, and is becoming more apparent, is the formative role played by diatoms and other silica-forming organisms, such as silicoflagellates, radiolarian, and sponges, in the biogeochemical cycle of silicon.

The reactions of condensation of silicic acid and subsequent polymerization to form biogenic silica eventually (i.e., upon the death of the organism) result in a net loss of silicic acid to the biosphere. The rate of the forward reaction (condensation and polymerization) is several orders of magnitude higher than that of the reverse (regeneration of silicic acid pool) with the result that concomitant with the rise of the diatoms and other silica-forming organisms was a significant reduction in the environmental silicic acid concentration. Silica frustules are formed in a matter of hours to days whereas the rate at which silicic acid is returned to the biosphere through the dissolution of the frustules of dead diatoms as they sink in the water column is of the order of 10^-9µmol m^-2 sec^-1. In addition, the dissolution of these sinking frustules can be greatly influenced by the chemistry of the water column. For example, the frustule is a highly adsorptive surface and is implicated in the removal of metal ions, for example, aluminium, from the water column. These adsorptive processes tend to stabilize the frustule surface towards dissolution and thereby reduce the amount of silicic acid returned to the biosphere during sedimentation. Once the silica frustules have settled to the bottom their silica enters the sedimentary cycle whereupon it is unlikely to reappear in the biosphere for tens of millions of years.

The biologically induced dramatic decline in the environmental silicic acid concentration had the effect of accelerating the rate of mineral weathering. This, in turn, consumed more carbon dioxide and precipitated a gradual reduction in the atmospheric concentration of this “greenhouse” gas. The impact of the emergence of diatoms and other silica-forming organisms, and latterly the spread of rooted vascular plants, on the biogeochemical cycle of silicon contributed significantly to the global cooling, which has resulted in the climate of today. The diatoms, in particular, are extremely successful organisms and will continue to deposit silica frustules of varying silica content at micromolar concentrations of environmental silicic acid. In this way they are a continuous accelerant of mineral weathering almost regardless of how low the environmental silicic acid concentration may fall. From the advent of the silica-forming organisms the process of biochemical evolution has continued in silicon-replete, though no longer of millimolar concentration, environments. Diatoms in sedimentary deposits of marine and continental, especially lacustrine, origin belong to different geologic ranges and physiographic environments. Marine diatoms range in age from Early Cretaceous to Holocene, and continental diatoms range in age from Eocene to Holocene; however, most commercial diatomites, both marine and lacustrine, were deposited during the Miocene. Marine deposits of commercial value generally accumulated along continental margins with submerged coastal basins and shelves where wind-driven boundary currents provided the nutrient-rich upwelling conditions capable of supporting a productive diatom habitat. Commercial freshwater diatomite deposits occur in volcanic terrains associated with events that formed sediment-starved drainage basins. Marine habitats generally are characterized by stable conditions of temperature, salinity, pH, nutrients, and water currents, in contrast to lacustrine habitats, which are characterized by wide variations in these conditions. Marine deposits generally are of higher quality and contain larger resources, owing to their greater areal extent and thickness, whereas most of the world’s known diatomites are of lacustrine origin.

Unlike many other algae, whose division cycles are strongly coupled to the diel light cycle, diatoms are capable of dividing at any point of the diel cycle. This light independence extends to their nutrient requirements, with nitrate and silicic acid uptake and storage continuing during the night through the use of excess organic carbon synthesized during the day. Moreover, the silica frustule has recently been shown to play a role in CO₂ acquisition, which indicates that Si limitation can induce CO₂ limitation in diatoms. Specifically, the silica frustule facilitates the enzymatic conversion of bicarbonate to CO₂ at the cell surface by serving as a pH buffer thus enabling more efficient photosynthesis. This control by diatoms and the reduction in silicate input from rivers due to cooling and drying of the climate offers a feedback mechanism between climate variability, diatom productivity, and CO₂ exchange. These features of diatom physiology almost certainly contribute to the in situ observation that diatoms have greater maximum growth rates relative to comparable algae. Further, so long as silicic acid is abundant (and other nutrients non-limiting), diatoms are found to dominate algal communities. Diatoms are estimated to contribute up to 45% of total oceanic primary production, making them major players in the cycling of all biological elements. They globally uptake and process 240 Tmol Si yr^-1. Currently, risk to diatoms comes from both climate forced impacts and anthropogenic sources. Reduced input of silicate due to damming of rivers and changes in water use patterns, and increased input of inhibitory levels of ammonium to estuaries and adjacent coastal waters affect diatom success. The high ammonium concentrations prevalent in some estuaries, a result of anthropogenic inputs from sewage treatment plants and agricultural runoff inhibit the uptake of nitrate by diatoms which draw primarily on nitrate for high growth rates.

Aside from their role in the silicon cycle, the diatoms have also attracted attention because of their importance to the export of primary production to the ocean’s interior. Aggregation and sinking is an important aspect in the life history of many diatom species, and high sinking velocities, whether as individuals, aggregates, or mats, allow diatoms to rapidly transport material out of the surface mixed layer. Additionally, mesozooplankton grazers that consume diatoms produce large, fast-sinking faecal pellets. These processes remove nutrients and carbon from the productive surface waters before they can be remineralized, making the diatoms crucial to “new” (or export) production. So long as silicic acid is available, diatoms act as a conduit for nutrients and carbon to deep waters, contrasting with the production of other algae, which “traps” nutrients in a regeneration loop at the surface.

Though diatoms are by far the most important organisms that take up silicic acid to form their encasing structures, silicoflagellates also deserve mentioning. These unicellular heterokont algae belong to a small group of siliceous marine phytoplankton. Silicoflagellates live in the upper part of the water column, and are adapted for life in tropical, temperate, and frigid waters. Silicoflagellates have a multi-stage life-cycle, not all stages of which are known. The best-known stage consists of a naked cell body with a single anterior flagellum and numerous plastids contained within an external lateral skeleton. This skeleton is composed of hollow beams of amorphous silica, forming a network of bars and spikes arranged to form an internal basket. The siliceous skeleton of silicoflagellates is very susceptible to dissolution, and therefore their preservation is often hindered by diagenetic processes; moreover, their abundance is relatively low compared with that of other siliceous microfossils, because they form a small component of marine sediments; both these reasons make their presence rare in the sedimentary record.