Silicon: requirements, uptake, deployment in phytoplankton
All phytoplankton have a requirement for the small amounts of silicon involved in protein synthesis (<0.1% of dry mass; see Section 1.5.2).
In the context of the present chapter, however, the focus of interest is the extensive deployment of silicon polymers in the scales of the Synurophyceae and, especially, in the skeletal reinforcement of the pectinaceous cell walls of the Bacillariophyceae (diatoms). As the diatoms are among the most conspicuous and abundant groups represented in the phytoplankton of the sea and of fresh waters, the biological intervention in the movements of silicon are of profound ecological and biogeochemical significance. Several useful reviews of this topic (e.g. Werner, 1977; Paasche, 1980; Sullivan and Volcani, 1981; Reynolds, 1986a) appeared 20 to 30 years ago but more modern treatments are scarce. However, many aspects of the pelagic availability, uptake, deployment and dynamics of silicon have been well established for some time. In lots of ways, it is an ideal nutrient to study. Later work has considerably amplified, rather than revolutionised, the earlier findings.
Despite its chemical similarities to carbon, the second most common element in the Earth's crust is somewhat less reactive. It occurs almost invariably in combination with oxygen (as in the minerals quartz and cristobalite) and often also with aluminium, potassium or hydrogen (kaolin-ite, feldspars and micas - the so-called clay minerals). These are only sparingly soluble, but hydrolysis of aluminium silicates, aided by mechanical weathering, allows silicon into aqueous solution. Below pH ~9, the dissolved reactive silicon available that is exploitable by diatoms and other algae is the weak monosilicic acid (H4SiO4). Its upper concentration (at neutrality and 20 °C: ~10-2-7 M, or ~56 mg Si L-1) is regulated by the precipitation of amorphous silica (Siever, 1962; Stumm and Morgan, 1996). The concentrations of soluble reactive silicon (SRSi) that can be encountered in most open fresh waters are 1 or 2 orders lower (0.7-7 mg Si L-1, 25-250 |M); the maximal levels found in oceanic upwellings (~3 mg Si L-1) also fall within this range. In both habitats, the concentration may be drawn down substantially, as a consequence of uptake and growth by diatoms, by other algae, by radiolarian rhi-zopods and sponges.
Uptake and intracellular transport of H4SiO4 proceed by way of a membrane-bound carrier system that conforms to Michaelis-Menten kinetics (Azam and Chisholm, 1976; Paasche, 1980 Raven, 1983). Reported species-specific halfsaturation constants (Ku) for the uptake of monosilicic acid by marine planktic diatoms are generally within the range 0.3-5 | mol L-1, while those for freshwater species are slightly higher (Paasche, 1980). The next steps, leading to the precipitation of the opal-like cryptocrystalline silica polymer used in the skeletal elements and the species-specific morphogenesis and organisation into the punctuate plates, ribs, bracing spars, spines and other diagnostic features that both characterise the group and facilitate their identification, are closely regulated and coordinated by the genome of the living cell (Li and Volcani, 1984; Crawford and Schmid, 1986). The resultant structures, that may survive long after death and which can be isolated and purified by chemical treatment, inspire the deep interest of diatomists and taxonomists alike. Their forms are celebrated in compendia of scanning elec-tromicrographs (for instance, Round et al., 1990), published essentially as aids to diatom identification, although they generally project a powerful artistic appeal too. It is worth emphasising that the active uptake of silicic acid is necessary not simply to sustain the amounts of silica used in the skeleton but also to generate the saturated intracellular environment essential to aid its deposition in the wall (Raven, 1983). The mechanism is known to be extremely effective: external concentrations of SRSi can be lowered to barely detectable levels (<0.1 | mol L-1 in some instances: Hughes and Lund, 1962).
On the other hand, the cellular silicon requirement for a cell of a given species and size is quite predictable (see Section 1.5.2 and Fig. 1.9). The skeletal structure in diatoms comprises two interlocking frustules, or valves. At cell division (see Section 5.2.1), each of the daughter cells takes away one of the separating maternal frustules and elaborates a new one to just fit inside it. The amount of silicon taken up does not much differ from the amount required to form the new frus-tules and it is absorbed at the time of demand. This carries some negative implications for the new cell (see Section 5.2.2) but, because no more silicon is withdrawn than is required, the rate of its removal from solution provides a useful indi rect measure of the rate of recruitment of new cells.
Nevertheless, interspecific differences in size, shape and vacuole size determine that the amount of silicon needed to complete the new cell varies in relation to the mass of cytoplasm (and, hence, its content of C, P and N). Among the selection of diatoms included in Tables 1.4 and 1.5, Si : C varies between 0.76 and 1.42 by mass (supposing the non-silica dry mass to equal ash-free dry mass and 50% of this to be carbon.). This fact is not to be confused with the differing concentrations at which various diatoms experience growth-rate limitation by silicon availability (see Section 5.4.4).
Diatoms make a major impact upon the abiotic geochemical silicon cycle. This is due partly to the global abundance of diatoms but it is compounded by their behaviour and propensity to redissolve. Owing to the high density of opaline silica (~2600 kg m-3), most diatoms are significantly heavier than the water they displace and, hence, they sink continuously. Populations are correspondingly dependent upon turbulent entrainment for continued residence in surface waters and the loss rates through sinking remain sensitive to fluctuations in mixed depth (see Sections 2.7.1, 6.3.2). Much of the production is eventually destined to sediment out or to be eaten by pelagic consumers. Either way, there is a flux of diatomaceous silicon towards the abyss. During its passage through the water column, silicic acid is leached from the particulate material, at variable rates that relate to the size of particles, their degree of aggregation, pH and water temperature, though probably not much exceeding 0.1 x 10-9 mol m-2 s-1 (~3 pg Si m-2 s-1) (Wollast, 1974; Werner, 1977; Raven, 1983). Matching these to the sinking rates of dead diatoms (many of which sink at <1 m d-1), the time taken to dissolve completely (200-800 d) will have elapsed before they have settled through 1000 m (calculations of Reynolds, 1986a). Larger, faster-sinking centric diatoms may reach rather greater depths but the point is that very little silica reaches the deep ocean floor. Most will have been returned to solution in the water above, and its availability to future diatom growth is restored. It is easy to concur with Wollast's (1974) view that
45% of the mass of siliceous debris in the sea is redissolved between the surface and a depth of 1000 m. This uptake, incorporation, transport and resolution of silicon from diatoms plainly shortcuts the abiotic movements of silicon; Wollast (1974) estimated the annual consumption of silicon by diatoms (~12 Pg Si) reduced the residence time of oceanic silicon from ~13 000 to just a couple of hundred years.
In contrast, however, in the relatively truncated water columns of most lakes (between, say, 5 and 40 m in depth), a significant proportion of the spring 'bloom' of settling pelagic diatoms does reach the sediments intact (Reynolds and Wiseman, 1982; Reynolds et al., 1982b). This does not prevent re-solution from continuing but, once part of the superficial lake sediment, the rate of solution quickly becomes subject to regulation by the (usually high) external concentration of silicic acid in the interstitial water and by re-precipitation on the frustule surfaces. Other substances, including organic remains, may interfere (Lewin, 1962; Berner, 1980). Thus, the pelagic diatoms become preserved in the accumulating sediment, providing a superb record of unfolding sedimentary events over a long period of time and environmental change. In this instance, the limnetic silicon flux enters a highly retarded phase of its potential biogeochemical cycle.
The chapter deals with the components required to build algal cells and the means by which they are obtained, given the background of sometimes exceedingly dilute supplies. The materials are needed in differing quantities, some of which are in relatively plentiful supply (H, O, S), some are abundant in relation to relatively modest requirements (Ca, Mg, Na, K, Cl), while some occur as traces and are used as such (Mn, Zn, Cu, Co, Mo, Ba, Va). Four elements for which failure of supply to satiate demand has important ecological consequences are treated in some detail (P, N, Fe, Si). However, even the more abundant of these nutrients are orders of magni tude more dilute in the medium than in the living cell. They have to be drawn from the water against very steep concentration gradients. Plank-ters have sophisticated, ligand-specific membrane transport systems, comprising receptors and excitation responses, for the capture and internal assimilation of target nutrient molecules from within the vicinity of the cell. These work like pumps and they consume power supplied by ATP phosphorylation. However, cells are still reliant on external diffusivities to renew the water in their vicinities; quantitative expressions are available to demonstrate the importance of relative motion. The work of Wolf-Gladrow and Riebe-sell (1997) suggests that small cells may experience an advantage over larger cells in rarefied, nutrient-poor water, as they are less reliant upon turbulent motion to replenish their immediate environments.
The uptake of nutrients supplied to starved planktic cells conforms to the well-tested models based on Michaelis-Menten enzyme kinetics. Performances are characterised by reference to the maximum capacity to take up nutrient (VUmax) and the external concentration (Ku) that will half-saturate this maximum rate of uptake (i.e. that that will sustain 0.5 VUmax). Clearly, a high biomass-specific uptake rate and/or an ability to half-saturate it at low concentrations represent advantageous adaptations. Actual performances are conditioned by what is already in the cell and its 'blocking' of the assimilation pathways (according to the Droop 'cell quota' concept). A new expression (Eq. 4.12) is ventured to show how the uptake rate is conditoned by the contemporaneous quota. These formulations are used to distinguish among uptake mechanisms that are variously 'velocity adapted', 'storage adapted' or 'affinity adapted'. The usage of the terms 'limitation' and 'competition' (in the context of satisfying resource requirements) is also rationalised (see Box 4.1).
Phosphorus generally accounts for 1-1.2% of the ash-free dry mass of healthy, active cells, in the approximate molecular ratio to carbon of 0.009. Minimum cell quota (q0) may vary inte-specifically, generally to 0.2-0.4% of ash-free dry mass but some species may survive on as little as 0.03%. Natural concentrations of bioavailable
P (usually less than the total concentration in the water but often rather more than the soluble, molybdate-reactive fraction (MRP, or SRP), are frequently around 0.2 to 0.3 | M. These are variously augmented by the weathering of phosphatic minerals, especially in desert catchments. Forested catchments may restrict even this supply but anthropogenic activities (quarrying, agriculture and tillage and, of course, the treatment of sewage) may significantly augment them. As phosphorus is often considered to be the biomass-limiting constraint in pelagic ecosystems, P enrichment can provide a significant stimulus to the sustainable biomass of phyto-plankton. Many species can take up freely available phosphorus at very rapid rates, sufficient to sustain a doubling of cell mass in a matter of a few (<7) minutes. The external concentrations required to saturate the rates of growth are generally under 0.13 |M P and the most affinity-adapted species can function at concentrations of between 10-8 and 10-7 M. In the presence of MRP concentrations >0.1 |M P, phytoplank-ton is scarcely 'phosphorus limited'. The conclusion is supported by each of four quite distinct approaches to determining whether cells are experiencing P regulation.
Persistent P deficiency can be countered in appropriately adapted species by the production of phosphatase (which cleaves P from certain organic binders) or by phagotrophy (consumption of P-containing organic particles or bacteria). Both rely on the sustained availability of these alternative sources of P.
Nitrogen accounts for 7-8.5% of the ash-free dry mass of healthy, active cells, in the approximate molecular ratio to carbon of 0.12-0.15. Minimum cell quota (q0) may not be less than 3% ash-free dry mass of living cells. Nitrogen is relatively unreactive, organisms having to rely on sources of the element in inorganic combination (nitrate, ammonium) but which are extremely soluble. Aggregate concentrations of dissolved inorganic nitrogen (DIN) in the open sea are generally in the range 20-40 |M but are often depleted towards the surface. The most N-deficient waters are those of the North Pacific, the Sargasso and the Indian Ocean. Shelf waters may be relatively more replete, especially in temperate waters in late winter (concentrations 50-70 |M). Temperate lakes and rivers may offer similar levels of resource but, again, anthropogenic activities (especially the agricultural application of nitrogenous fertiliser) may augment these, up to 1 mM. On the continental masses at lower latitudes and, especially, in arid regions, DIN losses from catchment topsoils are small and subject to further microbial denitrification, so that receiving waters are often DIN-deficient in consequence (1-10 | M).
Nitrate is redox-sensitive. Ammonification is mediated by facultatively anaerobic bacteria. Ammonium is less volatile than elemental nitrogen, so DIN levels are not necessarily depleted as a consequence of anoxia.
Phytoplankton generally takes up DIN from external concentrations as low as 0.2-0.3 | M. Although nitrate is usually the most abundant of the DIN sources in surface waters, ammonium is taken up preferentially while concentrations exceed 0.15-0.5 |M N. Half-saturation of DIN uptake by small oceanic phytoplankters occurs at concentrations of 0.1-0.7 |M N with nitrate as substrate and 0.1-0.5 |M N with ammonium. Nitrogen availability is unlikely to constrain phytoplankton activity and growth before the DIN concentration in the medium falls to below 7 |mol N L-1 (~100 mg N m-3), in the case of large, low-affinity species, or below ~0.7 |mol N L-1, in the case of oceanic picoplankton.
In the effective absence of DIN, phytoplank-ton exploits the pool of dissolved organic nitrogen, including urea. Certain groups of bacteria, including the Cyanobacteria, are additionally able to reduce ('fix') dissolved nitrogen gas. The relevant enzymes operate only under anaerobic conditions. In the Nostocales, usually the most effective dinitrogen fixers in the freshwater plankton, fixation is confined to specialised cells called heterocysts. They are produced facultatively under conditions of depleted DIN. Differentiation commences against a background of falling DIN, below 19-25 |M. It is likely that the reaction actually responds to depletion of ammonium nitrogen (to <0.5 |M NH4.N). Successful fixation also depends upon threshold levels of light, phosphorus, iron and molybdenum being satisfied.
In parts of the Atlantic and Indian Oceans characterised by low DIN levels (often <1 |M DIN), nitrogen is fixed by Trichodesmium spp. The plankters succeed over non-fixers but dinitro-gen fixers are not more widespread in DIN-deficient seas because the energy and micronu-trient requirements are not simultaneouly satisfied.
Iron is a micronutrient, the availability of which is rarely problematic except in the large oceans. However, the amounts that occur in true solution are extremely small (~10-15 M) and the availability to algae depends upon its chelation by fine organic colloids. Some, at least, of this fraction is accessible to phytoplankton. A totaliron (TFe) content of 10-8 M seems adequate to support the needs of most species of phyto-plankton, in which iron constitutes some 0.03% and 0.1% of ash-free dry mass (about 0.1-0.4 mmol Fe : mol C). On the other hand, media containing <10-11 M are too dilute to support sustained growth of algae. It seems most likely that minimal productivity of the relatively high-nitrogen, low-chlorophyll areas of the Southern Ocean are absolutely iron deficient. The minimum iron requirements of active nitrogen fixers are suggested to be relatively higher, at about 1-2 x 10-10 M TFe. Lack of nitrogen may preclude most other algae but lack of sufficient iron means that the nitrogen fixers are not free to exploit the situation.
Silicon plays a regulatory role in the plankton, not as a conventional nutrient but as a vital skeletal requirement of diatoms. The crypto-crystalline, opal-like silica polymer that makes up the structure of the diatom frustules is precipitated and organised within the cell from the dissolved reactive monosilicic acid that the cells take up from solution. The transformations between external solution, internal deposition and re-solution of the frustule after death are regulated, in part, by the solubilities of the silicic acid and of the silica polymer after death of the cell.
The amounts of silicon that are deposited in cell walls vary interspecifically and, intraspecifi-cally, with size. Cell-specific silicon requirements range between 0.5% (in marine Phaeodactylum) and 37% of dry mass (in freshwater Aulacoseira); among well-studied diatoms, Si : C varies between 0.76 and 1.42 by mass. Populations draw down the concentrations present in natural waters, from a typical range, 25-250 | M, until depleted to halfsaturation levels (KU) of about 0.3-5 |M. However, uptake of Si scarcely exceeds the amounts deposited; silicon consumption provides an accurate guide to the numbers of diatoms produced.
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