Bioenergetic aspects of halophilism

Abstract

Examination of microbial diversity in environments of increasing salt concentrations indicates that certain types of dissimilatory metabolism do not occur at the highest salinities. Examples are methanogenesis for H2 + CO2 or from acetate, dissimilatory sulfate reduction with oxidation of acetate, and autotrophic nitrification. Occurrence of the different metabolic types is correlated with the free-energy change associated with the dissimilatory reactions. Life at high salt concentrations is energetically expensive. Most bacteria and also the methanogenic Archaea produce high intracellular concentrations of organic osmotic solutes at a high energetic cost. All halophilic microorganisms expend large amounts of energy to maintain steep gradients of NA+ and K+ concentrations across their cytoplasmic membrane. The energetic cost of salt adaptation probably dictates what types of metabolism can support life at the highest salt concentrations. Use of KCl as an intracellular solute, while requiring far-reaching adaptations of the intracellular machinery, is energetically more favorable than production of organic-compatible solutes. This may explain why the anaerobic halophilic fermentative bacteria (order Haloanaerobiales) use this strategy and also why halophilic homoacetogenic bacteria that produce acetate from H2 + CO2 exist whereas methanogens that use the same substrates in a reaction with a similar free-energy yield do not.

FIG. 1

Some organic compatible solutes found in halophilic and halotolerant microorganisms.

FIG. 2

Energy requirement (in ATP equivalents) for the synthesis of selected organic compatible solutes from CO₂ (open bars) and the cost of the production of these solutes for an aerobic heterotrophic microorganism growing on glucose (solid bars). For autotrophic microorganisms, the cost of synthesis of compatible solutes from CO₂ was calculated based on the reactions of the Calvin cycle and the specific reactions leading to the formation of the product. Calculations of the energetic cost for heterotrophs were based on the assumption that each glucose molecule spent in the synthesis of osmotic solutes would have yielded 38 ATP equivalents upon complete oxidation to CO₂ via the Embden-Meyerhof pathway and the tricarboxylic acid cycle. In all cases, the consumption and formation of one NADH or NADPH molecule was taken to be equivalent to the requirement for and generation of three ATP molecules, respectively. Calculations of the energetic cost of the biosynthesis of glycine betaine were based in part on Fig. 5 in reference , and separate calculations were made for synthesis of glycine betaine by the oxidation of choline and by stepwise methylation of glycine. For nitrogen-containing solutes, ammonia was assumed to be assimilated via the glutamine synthetase/glutamate synthase system, adding the need for one ATP molecule and one NADH molecule (three potential ATP equivalents) per atom of nitrogen (104).

FIG. 3

Ion movements in the aerobic halophilic archaea (family Halobacteriaceae). 1, proton extrusion via respiratory electron transport; 2, light-driven proton extrusion mediated by bacteriorhodopsin; 3, ATP formation by ATP synthase, driven by the proton gradient (alternatively, this system can serve to generate a proton gradient at the expense of ATP during fermentative growth on l-arginine); 4, electrogenic sodium/proton antiporter; 5, sodium gradient-driven inward amino acid transport; 6, potassium uniport, driven by the membrane potential; 7, light-independent chloride transport system, probably coupled with inward transport of sodium; 8, halorhodopsin, a light-driven inward chloride pump. For details, see the text.

FIG. 4

Approximate upper salt concentration limits for the occurrence of selected microbial processes. Values presented are based in part on laboratory studies of pure cultures (solid bars) and in part on activity measurements of microbial communities in hypersaline environments in nature (open bars). Data are based on references , , , , , , and many other sources. For additional information, see the text.