Physiological and genetic responses of bacteria to osmotic stress.

Examinination 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.

Bioenergetic Aspects of Halophilism

Two general strategies exist for the growth and survival of prokaryotes in environments of elevated osmolarity. The ‘salt in cytoplasm’ approach, which requires extensive structural modifications, is restricted mainly to members of the Halobacteriaceae. All other species have convergently evolved to cope with environments of elevated osmolarity by the accumulation of a restricted range of low molecular mass molecules, termed compatible solutes owing to their compatibility with cellular processes at high internal concentrations. Herein we review the molecular mechanisms governing the accumulation of these compounds, both in Gram-positive and Gram-negative bacteria, focusing specifically on the regulation of their transport/synthesis systems and the ability of these systems to sense and respond to changes in the osmolarity of the extracellular environment. Finally, we examine the current knowledge on the role of these osmostress responsive systems in contributing to the virulence potential of a number of pathogenic bacteria.

Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence

The osmoadaptation of most micro-organisms involves the accumulation of K+ ions and one or more of a restricted range of low molecular mass organic solutes, collectively termed ‘compatible solutes’. These solutes are accumulated to high intracellular concentrations, in order to balance the osmotic pressure of the growth medium and maintain cell turgor pressure, which provides the driving force for cell extension growth. In this review, I discuss the alternative roles which compatible solutes may also play as intracellular reserves of carbon, energy and nitrogen, and as more general stress metabolites involved in protection of cells against other environmental stresses including heat, desiccation and freezing. Thus, the evolutionary selection for the accumulation of a specific compatible solute may not depend solely upon its function during osmoadaptation, but also upon the secondary benefits its accumulation provides, such as increased tolerance of other environmental stresses prevalent in the organism’s niche or even anti-herbivory or dispersal functions in the case of dimethylsulfoniopropionate (DMSP). In the second part of the review, I discuss the ecological consequences of the release of compatible solutes to the environment, where they can provide sources of compatible solutes, carbon, nitrogen and energy for other members of the micro-flora. Finally, at the global scale the metabolism of specific compatible solutes (betaines and DMSP) in brackish water, marine and hypersaline environments may influence global climate, due to the production of the trace gases, methane and dimethylsulfide (DMS) and in the case of DMS, also couple the marine and terrestrial sulfur cycles.

Ecological significance of compatible solute accumulation by micro‐organisms: from single cells to global climate

Publisher Summary This chapter focuses on the osmoadaptation in bacteria. Bacterial ability to osmoadapt seems to be the norm rather than the exception. Under the right environmental circumstances (external osmolytes or precursors thereof), many bacteria, so far believed to be salt-sensitive, show considerable osmotolerance. Mechanisms for survival and growth in a high-osmolarity environment aim at maintaining osmotic equilibrium across the membrane. Compatible solutes used and produced by halo/osmophilic bacteria are useful tools to study and understand water solvent interactions, and to resolve principles of enzyme stabilization. They are bound to offer a range of technological applications as universal stress protectants. Among anaerobic halophilic eubacteria, attempts to find organic osmolytes have been unsuccessful; instead,high cytoplasmic amounts of potassium and sodium chloride were detected and proteins displayed an excess of acidic amino acids. As all enzymes investigated also showed maximal activity at high salt concentrations, there seems to be sufficient evidence that this eubacterial physiological group is adapted to an ionic cytoplasm. The salt-in-cytoplasm type of osmoadaptation is therefore apparently not confined to archaebacterial representatives, although NaCl rather than KCl seems to be the dominant cytoplasmic solute in these eubacteria. The best-studied model systems of osmotic adaptation are E. coli and S. typhimurium, which are discussed.

Osmoadaptation in Bacteria

The major organic osmoregulatory solutes of 36 cyanobacteria from a wide range of environmental sources have been examined using 13C nuclear magnetic resonance spectroscopy. These strains were also examined for their salt-tolerance, and could be arranged in three salt-tolerance groups, designated freshwater, marine and hypersaline. The most salt-tolerant cyanobacteria in the hypersaline group are properly classified as moderately halophilic. Cyanobacteria from all habitats and taxonomic groups accumulated organic osmoregulatory solutes, and the chemical class of the solute correlated with the salt-tolerance and habitat of the strain. Freshwater strains accumulated simple saccharides, predominantly sucrose and trehalose; marine strains accumulated the heteroside O-α-D-glucopyranosyl-(1→2)-glycerol, and hypersaline strains accumulated sucrose and/or trehalose together with glycine betaine or the novel solute L-glutamate betaine (N-trimethyl-L-glutamate) or they accumulated glycine betaine alone. The results suggest that the presence of certain major organic osmoregulatory solutes may be useful in the numerical taxonomy of cyanobacteria, and in the identification of some ionic characteristics of the environment of origin of each isolate.

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Mark A. Mackay

Papers

Organic Osmoregulatory Solutes in Cyanobacteria