CASE STUDY 17.2  Aquatic organisms and compatible solutes

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M.A. Borowitzka

Algae and seagrasses are predominantly aquatic species. Overall, they range from freshwater organisms to the most salt tolerant eukaryotic organism on earth, the single-celled alga Dunaliella salina that grows in saturated salt solutions (about 5.5 M NaCl).

Intertidal, marine and estuarine species are commonly exposed to large diurnal and seasonal variation in salinity. To prevent dehydration or excessive hydration they need mechanisms such as osmoregulation to cope with changes in environmental salinity.

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Figure 1 A generalised response of glycerol content in Dunaliella sp. To a change in external NaCl concentration (1.5 M up to 4.0 M NaCl with an accompanying increase in glycerol content (cf. 4.0 M down to 2.0 M NaCl and an associated decrease in glycerol content). An initial fast phase occurs in response to a sudden shift in osmolarity of the cell's external medium that lasts 5 to 10 s, followed by a second slower phase that can take about 40 min and is shown here in detail. (Based on Kessley, courtesy M.A. Borowitzka)

In walled cells, cell water potential (ψcell) can be expressed as the difference between two components, turgor (Pcell) and osmotic pressure (Πcell) where ψcell = Pcell – Πcell. In such walled cells, osmoregulation results largely in regulation of turgor. However, in wall-less cells such as the halophytic unicellular alga D. salina, Pcell is very small and Πcell is the major component of ψcell, so that any change in Ymedium will initially cause a corresponding change in cell volume to restore osmotic equilibrium. When subjected to a rapid change in salinity, cells shrink or swell in direct proportion to the reciprocal of the external osmolarity, as expected from a perfect osmometer. Following such volume change, cells slowly revert to their original size in 1–3 h depending on the magnitude of the salinity shock. During this adjustment phase, cells alter their internal glycerol content to reach an osmotic equilib-rium with the external medium (Figure 1).

At high salinity (saturated salt solution, approximately 5.5 M NaCl), cells contain 50% glycerol or thereabouts on a volume basis, and this is sufficient to balance extracellular osmolarity. Accumulated glycerol comes mainly from degradation of starch and occurs in both light and darkness.

Glycerol is an ideal compatible solute, protecting enzymes against both inactivation and inhibition as well as fulfilling a crucial osmotic role in maintenance of cell volume. Glycerol meets important physico-chemical criteria by being infinitely soluble, uncharged and non-permeating (the plasma membrane of Dunaliella is impermeable to glycerol at usual temperatures). In D. tertiolecta and D. viridis, glycerol accumulation to 4 M does not inhibit crucial enzymes such as glucose-6-phosphate dehydrogenase, and even at 10 M glycerol this enzyme retains about 15% activity.

Prokaryotic algae (blue-green algae or Cyanobacteria) in less extreme environments have a range of other organic solutes which accumulate in response to increased salinity. Different species of Cyanobacteria accumulate glycinebetaine, glutamate betaine, glycosylglycerol, trehalose and sucrose. Across this range of compatible solutes, a direct relationship exists between solute solubility and salinity tolerance. Highly tolerant Cyanobacteria that grow in salt lakes accumulate glycinebetaine or glutamate betaine (both highly soluble); those with intermediate salt tolerance accumulate glucosylglycerol; least tolerant Cyanobacteria, those that grow in seawater, accumulate trehalose and sucrose (least soluble of this series). By analogy with the enzymology of single-celled eukaryotes (e.g. Dunaliella spp. mentioned above), the solubility of osmolytes in Cyanobacteria again correlates with their effect on enzyme activities. Less soluble compounds are more inhibitory to enzyme activity and vice versa.

Adaptations to salinity in seagrasses resemble those in terrestrial halophytes and marine algae. Turgor is maintained by an adjustment in internal osmotic potential based on accumulation of Na+ and Cl ions in vacuolar compartments (K+ remaining constant), while organic solutes such as proline, sucrose and alanine accumulate in cytoplasmic compartments.

In summary, a great natural diversity in plant form and habitat is reflected in accumulation of an equally wide variety of compatible solutes that constitute an adaptative response to salinity. In all cases, the osmotic impact of inorganic solutes, in either an external environment and/or a vacuolar compart-ment, is alleviated by an accumulation of low molecular weight organic solutes in adjacent metabolic compartments. Such osmolytes are commonly confined to cytoplasmic com-part-ments in eukaryotic organisms and counter the osmotic effects of inorganic solutes in vacuolar compartments. Prokaryotic organisms accumulate cellular osmolytes in response to external solutes.

In either circumstance, these compatible solutes exert direct osmotic effects for regulation of either turgor or cell volume, plus indirect physico-chemical effects on enzyme proteins that protect their metabolic function during salt stress. 

Further reading

Avron, M. (1992). ‘Osmoregulation’, in Dunaliella: Physiology, Biochemistry, and Biotechnology, eds. M. Avron and A.
Ben-Amotz, 135–164, CRC Press: Boca Raton, Florida.

Borowitzka, L.J. (1986). ‘Osmoregulation in blue-green algae’, Progress in Phycological Research, 4, 243–256.

Tyerman, S.D. (1990). ‘Solute and water relations of seagrasses’, in Biology of Seagrasses, eds A.W.D. Larkum, A.J. McComb and S.A. Shepherd, 723–759, Elsevier: Amsterdam.

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