There was more to osmolyte selection than just osmotic balance.

Jason Treberg discusses the impact of Paul Yancey et al.'s classic paper 'Living with water stress: evolution of osmolyte systems', published in Science in 1982. Occasionally a hypothesis comes along that is so broadly applicable to biological systems that it borders on being universal. Even less frequent is when the hypothesis involves linking knowledge from almost a century before with recent experimental observations on physiological and biochemical responses to environmental challenges. However, the seminal paper by Paul Yancey and colleagues (1982) was one such feat. The paper, entitled 'Living with water stress: evolution of osmolyte systems', synthesized ideas into the now well-accepted notion that the small solutes that are accumulated within cells for osmotic balance were likely selected because they do not disrupt macromolecular structure or function. The paper is well suited to those who are unfamiliar with osmoregulatory biology and physicochemical interactions because it summarizes the literature on the intracellular solutes common across taxa while also proposing a profoundly wide-reaching hypothesis linking the convergence of intracellular osmoregulatory strategies across diverse organisms. The authors noted how, out of all the possible low molecular weight molecules 'available' for intracellular accumulation, only a small number have been selected by most taxa. Moreover, most of the selected solutes were small organic compounds. Perhaps more remarkable was the narrow range of chemical classes that the accumulated 'organic osmolytes' fell into: they were virtually all polyhydric alcohols (polyols such as glycerol or mannitol), free amino acids and their derivatives or methylamines [a group of molecules with one or more methyl moiety attached to an amine group, such as trimethylamine-N-oxide (TMAO) and glycine-betaine]. In addition, urea – a solute also found across diverse animal taxa – was viewed as an unusual evolutionary option, because at concentrations of hundreds of millimoles per litre, which can be found in vivo, it is known to denature proteins and disturb function. Most of the intracellular organic osmolytes found across organisms could be further described as 'compatible osmolytes' [reviewed in Yancey et al. (1982) but also see Brown (1976)], which are solutes that can accumulate in the cell without significantly disturbing macromolecular function and cellular processes. Yancey and co-workers then went on to demonstrate the concept of osmolyte compatibility using examples from barley, algae, a decapod crab and a teleost fish, where increasing amounts of compatible solutes do not alter enzyme kinetics or substrate binding, whereas increasing ion concentrations (NaCl or …