Limiting Nutrients

Among the elements required for algal growth, there are some that can become limiting. The original notion of limitation was introduced by von Liebig more than a century ago to establish a correlation between the yield of a crop and the elemental composition of the substrate required for the synthesis of that crop. Von Liebig stated that if one crop nutrient is missing or deficient, plant growth will be poor, even if the other elements are abundant. That nutrient will be defined “limiting nutrient.” This concept is known as Liebig’s “Law of the Minimum.” Simply stated, Liebig’s law means that growth is not controlled by the total of nutrients available but by the nutrient available in the smallest quantity with respect to the requirements of the plant. Liebig likens the potential of a crop to a barrel with staves of unequal length. The capacity of this barrel is limited by the length of the shortest stave and can only be increased by lengthening that stave. When that stave is lengthened, another one becomes the limiting factor.

The concentration of a nutrient will give some indication whether the nutrient is limiting, but the nutrient’s supply rate or turnover time is more important in determining the magnitude or degree of limitation. For example, if the concentration of a nutrient is limiting, but the supply rate is slightly less than the uptake rate by the algae, then the algae will only be slightly nutrientlimited. Not all the algae are limited by the same nutrient, but it occurs at the species level, for example, all the diatoms are limited by silicate. Moreover, there is a considerable variation in the degree, kind, and seasonality of nutrient limitation, which is related to variations in riverine input, but also to conditions and weather in the outflow area.

In general, growth rate of a population of organisms would be proportional to the uptake rate of that one limiting factor. Nutrient-limited growth is usually modeled with a Monod (or Michaelis- Menten) equation:



where µ is the specific growth rate of the population as a function of [LN]; [LN] is the concentration of limiting nutrient; µ_max is the maximum population growth rate (at “optimal” conditions) and K_m is the Monod coefficient, also called the half-saturation coefficient because it corresponds to the concentration at which m is one-half of its maximum. When the concentration of limiting nutrient [LN] equals K_m, the population growth rate is µ_max/2.

As [LN] increases, µ increases and so the algal population (number of cells) increases. Beyond a certain [LN], µ tends asymptotically to its maximum (µ_max), and the population tends to its maximum yield. If this concentration is not maintained, rapidly primary productivity returns to a level comparable to that prior to the nutrient enrichment. This productivity variation is the seasonal blooming. Normal becomes abnormal when there is a continuous over-stimulation of the system by excess supply of one or more limiting nutrients, which leads to intense and prolonged algal blooms throughout the year. The continuous nutrient supply sustains a constant maximum algal growth rate (µ_max). Therefore, instead of peaks of normal blooms, followed by periods when phytoplankton is less noticeable, we have a continuous primary production. When this occurs, we refer to it as eutrophication. In this process, the enhanced primary productivity triggers various physical, chemical, and biological changes in autotroph and heterotroph communities, as well as changes in processes in and on the bottom sediments and changes in the level of oxygen supply to surface water and oxygen consumption in deep waters. Eutrophication is considered to be a natural aging process for lakes and some estuaries, and it is one of the ways in which a water body (lake, rivers, and seas) transforms from a state where nutrients are scarce (oligotrophic), through a slightly richer phase (mesotrophic) to an enriched state (eutrophic).

Eutrophication can result in a series of undesirable effects. Excessive growth of planktonic algae increases the amount of organic matter settling to the bottom. This may be enhanced by changes in the species composition and functioning of the pelagic food web by stimulating the growth of small flagellates rather than larger diatoms, which leads to lower grazing by copepods and increased sedimentation. The increase in oxygen consumption in areas with stratified water masses can lead to oxygen depletion and changes in community structure or death of the benthic fauna. Bottom dwelling fish may either die or escape. Eutrophication can also promote the risk of harmful algal blooms that may cause discoloration of the water, foam formation, death of benthic fauna and wild or caged fish, or shellfish poisoning of humans. Increased growth and dominance of fast growing filamentous macroalgae in shallow sheltered areas are yet another effect of nutrient overload, which will change the coastal ecosystem, increase the risk of local oxygen depletion, and reduce biodiversity and nurseries for fish.

Human activities can greatly accelerate eutrophication by increasing the rate at which nutrients and organic substances enter aquatic ecosystems from their surrounding watersheds, for example introducing in the water bodies detergents and fertilizers very rich in phosphorus. The resultant aging, which occurs through anthropogenic activity, is termed cultural eutrophication.

Globally, nitrogen and phosphorus are the two elements that immediately limit, in a Liebig sense, the growth of photosynthetic organisms. Silicon could also become a more generally limiting nutrient, particularly for diatom growth. These nutrients are present in algal cells in a speciesspecific structural ratio, the so-called Redfield ratio, which determines the nutrient requirement of the species, and whose value depends on the conditions under which species grow and compete. Consequently, the species composition of an environment will be determined not only by nutrient availability but also by their proper relation, because changes in nutrient ratio cause shifts in phytoplankton communities and subsequent trophic linkages. Nitrogen generally limits overall productivity in the marine system. Nitrogen limitation occurs most often at higher salinities and during low flow periods. However, because marine system is in stoichiometric balance, any nutrient can become limiting. Phosphorus limitation occurs most often in freshwater system, in environments of intermediate salinities, and along the coasts during periods of high fresh water input. The occurrence of silicon limitation appears to be more spatially and temporally variable than phosphorus or nitrogen limitation, and is more prevalent in spring than summer.

In the case of phosphorus, the limitation of algal growth can be at least twofold. First, there is a limitation of nucleic acid synthesis. This limitation can be at the level of genome replication or at the level of RNA synthesis (a form of transcriptional control). The limitation can affect photosynthetic energy conversion by reducing the rate of synthesis of proteins in the photosynthetic apparatus, which is effectively a negative feedback on photosynthesis. This inhibition of protein synthesis may thus have effects on cell metabolism and oxidative stress similar to those for inhibition of protein synthesis under N limitation, except that the effect is indirect and less immediate. Secondly, a more immediate response to phosphorus limitation is on the rate of synthesis and regeneration of substrates in the Calvin-Benson cycle, thereby reducing the rate of light utilization for carbon fixation. Cells can undergo also a decrease in membrane phospholipids; moreover, the inability to produce nucleic acids under P limitation limits cell division, leading to an increased cell volume.

On a biochemical level, nitrogen limitation directly influences the supply of amino acids, which in turn limits the translation of mRNA and hence reduces the rate of protein synthesis. Under nitrogen-limited conditions also the efficiency of PSII decreases, primarily as a consequence of thermal dissipation of absorbed excitation energy in the pigment bed. This appears to be due mainly to a decrease in the number of PSII reaction centers relative to the antennae. The functional absorption cross-section of PSII increases under nitrogen-limiting conditions, while the probability of energy transfer between PSII reaction centers decreases. From a structural point of view, the reaction centers behave as if they were energetically isolated with a significant portion of the light-harvesting antenna disconnected from the photochemical processes. As nitrogen limitation leads to a reduction of growth and photosynthetic rates, it also leads to a reduction in respiratory rates. The relationship between the specific growth rate and specific respiration rate is linear with a positive intercept at zero growth, which is termed maintenance respiration. The molecular basis of the alterations is unclear; however, the demands for carbon skeletons and ATP, two of the major products of the respiratory pathways, are markedly reduced if protein synthesis is depressed.

The requirement for silicon for the construction of diatom frustule makes this group uniquely subject to silicate limitation. As silicic acid uptake, silica frustule formation, and the cell division cycle are all tightly linked, under silica limitation, the diatom cell cycle predominantly stops at the G2 phase, before the completion of cell division. Thus, an inhibition of cell division linked to an inability to synthesize new cell wall material under silicon limitation can lead to an increase in the volume per cell. This increase could also be partly explained by the formation of auxospores with a larger cell diameter.