Review of nitrogen and phosphorus metabolism in seagrasses

Within the past few decades, major losses of seagrass habitats in coastal waters impacted by cultural eutrophication have been documented worldwide. In confronting a pressing need to improve the management and protection of seagrass meadows, surprisingly little is known about the basic nutritional physiology of these critical habitat species, or the physiological mechanisms that control their responses to N and P gradients. The limited available evidence to date already has revealed, for some seagrass species such as the north temperate dominant Zostera marina, unusual responses to nutrient enrichment in comparison to other vascular plants. Seagrasses derive N and P from sediment pore water (especially ammonium) and the water column (most nitrate). The importance of leaves versus roots in nutrient acquisition depends, in part, on the enrichment conditions. For example, a shift from reliance on sediment pore water to increased reliance on the overlying water for N and P supplies has been observed under progressive water-column nutrient enrichment. Seagrasses may be N-limited in nutrient-poor waters with sandy or (less so) organic sediments, and P-limited in carbonate sediments. On the basis of data from few species, seagrasses appear to have active uptake systems for NO(3)(-) and PO(4)(-3), but NH(4)(+) uptake may involve both low- and high-affinity systems. P(i) uptake affinities reported thus far are much lower than values for active ammonium uptake, but comparable to values for nitrate uptake by leaf tissues. Beyond such basic information, seagrass species have shown considerable variation in nutritional response. Dominance of acropetal versus basipetal nutrient translocation appears to vary among species as an innate trait. While some species follow classic Michaelis-Menten kinetics for N(i) uptake, others have exhibited sustained linear uptake with limited or negligible product feedback inhibition, perhaps in adaptation to oligotrophic environments. Zostera marina also is able to maintain nitrate reductase (NR) activity during dark periods if adequate carbohydrate reserves and substrate are available. Thus, this species can respond to nitrate pulses throughout a diel cycle, rather than being limited as most plants to nitrate uptake during the light period. Further adaptations may have occurred for seagrasses in extremely nitrate-depauperate conditions. For example, Halophila decipiens and H. stipulacea lack inducible NR and apparently have lost the ability to reduce nitrate; and a biphasic rather than hyperbolic P(i) uptake curve, with 'surge' uptake, has been described for Zostera noltii. Many seagrasses respond favorably to low or moderate N and/or P enrichment. However, excessive N(i) loading to the water column can inhibit seagrass growth and survival, not only as an indirect effect by stimulating algal overgrowth and associated light reduction, but-for some species-as a direct physiological effect. The latter direct impact has been most pronounced for plants growing in sandy (nutrient-poor) sediments, and is exacerbated by elevated temperatures and/or light reduction. Ammonia toxicity, known for many vascular plants, has been reported in seagrasses Ruppia drepanensis and Z. marina (125 µM water-column NH(4)(+), 5 weeks). Z. marina has shown to be inhibited, as well, by pulsed water-column nitrate enrichment (as low as 3.5-7 µM NO(3)(-), 3-5 weeks), which is actively taken up without apparent product feedback inhibition. Inhibition by elevated nitrate has also been reported, with description of the underlying physiological mechanisms, in certain macroalgae and microalgae. In Z. marina, this effect has been related to the high, sustained energy demands of nitrate uptake, and to inducement of internal carbon limitation by the concomitant 'carbon drain' into amino acid assimilation. In contrast, nitrate enrichment can stimulate growth of Z. marina when the sediment, rather than the water column, is the source. Because seagrass species have shown considerable variation in nutritional response, inferences about one well-studied species, from one geographic location, should not be applied a priori to that species in other regions or to seagrasses in general. Most of the available information has been obtained from study of a few species, and the basic nutritional physiology of many seagrasses remains to be examined and compared across geographic regions. Nonetheless, the relatively recent gains in general understanding about the physiological responses of some seagrass species to nutrient gradients already have proven valuable in both basic and applied research. For example, physiological variables such as tissue C:N:P content have begun to be developed as integrative indicators of nutrient conditions and anthropogenic nutrient enrichment. To strengthen insights for management strategies to optimize seagrass survival in coastal waters adjacent to exponential human population growth and associated nutrient inputs, additional emphasis is critically needed to assess the role of variable interactions-among inorganic as well as organic N, P and C, environmental factors such as temperature, light, and other community components-in controlling the physiology, growth and survival of these ecologically important marine angiosperms.