Solutions: how adaptive changes in cellular fluids enable marine life to cope with abiotic stressors

Abstract

The seas confront organisms with a suite of abiotic stressors that pose challenges for physiological activity. Variations in temperature, hydrostatic pressure, and salinity have potential to disrupt structures, and functions of all molecular systems on which life depends. During evolution, sequences of nucleic acids and proteins are adaptively modified to “fit” these macromolecules for function under the particular abiotic conditions of the habitat. Complementing these macromolecular adaptations are alterations in compositions of solutions that bathe macromolecules and affect stabilities of their higher order structures. A primary result of these “micromolecular” adaptations is preservation of optimal balances between conformational rigidity and flexibility of macromolecules. Micromolecular adaptations involve several families of organic osmolytes, with varying effects on macromolecular stability. A given type of osmolyte generally has similar effects on DNA, RNA, proteins and membranes; thus, adaptive regulation of cellular osmolyte pools has a global effect on macromolecules. These effects are mediated largely through influences of osmolytes and macromolecules on water structure and activity. Acclimatory micromolecular responses are often critical in enabling organisms to cope with environmental changes during their lifetimes, for example, during vertical migration in the water column. A species’ breadth of environmental tolerance may depend on how effectively it can vary the osmolyte composition of its cellular fluids in the face of stress. Micromolecular adaptations remain an under-appreciated aspect of evolution and acclimatization. Further study can lead to a better understanding of determinants of environmental tolerance ranges and to biotechnological advances in designing improved stabilizers for biological materials.

Life in Multi-Extreme Environments: Brines, Osmotic and Hydrostatic Pressure─A Physicochemical View

“…However, not only mutations of the amino acid sequence of proteins but also the composition of the cytoplasm of the extremophile in the context of its geological environment has a significant impact on protein stability and function. The cellular milieu is fairly crowded and contains a rather complex aqueous solution with a variety of different cosolutes (organic osmolytes). − Organisms living under extreme conditions are able to accumulate certain cosolvents such as sorbitol or TMAO in their cells to protect their proteins from unfolding and denaturation. Interestingly, TMAO, one of the most potent cosolvents discovered to date, was found to be upregulated in deep sea organisms up to high levels and acts as a chemical chaperone to counteract the deteriorating effect of pressure (hence also denoted “piezolyte”) not only on proteins but also on noncanonical DNA and RNA structures. ,,,,− Genome sequencing of a snailfish from the Yap Trench (at ∼7000 m depth) revealed the presence of five copies of a gene encoding a flavin-containing monooxygenase that catalyzes the reaction of trimethylamine (TMA) to TMAO, with TMA supplied by gut bacteria .…”

“…Also, macromolecular crowding can help stabilize biomolecular systems such as proteins against unfolding. 12,40,121,125 Temperature-and pressure-induced unfolding of SNase is shifted to higher temperatures and drastically to higher pressures in 30 wt % polysaccharide solution, mimicking intracellular crowding conditions. 125 An ∼1.5 kbar increase of pressure stability at ambient temperature has also been observed for the protein RNase A upon addition of 30 wt % dextran crowder.…”

Harnessing Pressure-Axis Experiments to Explore Volume Fluctuations, Conformational Substates, and Solvation of Biomolecular Systems

“…Organisms living under extreme conditions accumulate protein-stabilizing organic cosolvents (also referred to as compatible cosolutes or osmolytes) in their cells, such as glycerol, sorbitol, glycine betaine, or the deep-sea osmolyte trimethylamine-N-oxide (TMAO). [19][20][21]43,53,54 In addition to genetically based adaptations of the structural stability of proteins via mutations of amino-acids (denoted as intrinsic adaptations), extrinsic adaptations using such particular cosolvents are required to achieve the required adaptive changes in the stability and hence function of the proteins. [19][20][21]43,53,54 Remarkably, a given organic osmolyte often shows similar effects on proteins, nucleic acids, and membranes, suggesting common stabilization effects.…”

“…In addition to this physicochemical interest in the pressure variable, pressure is also a well-known parameter in the biological and biotechnological context. ,− Although high hydrostatic pressure (HHP) of several hundred to thousand bar (1 bar = 0.1 MPa ≈ 1 atm) significantly affects the structural and dynamical properties and thus the function of cellular components, this has not banned life from occupying high-pressure habitats in the ocean depths and subseafloor crust. Life itself may even have been created under pressure, such as in black smoker environments in the deep sea.…”

“…The incorporation of one or more cis -double bonds leads to very low transition temperatures (even below 0 °C) and smaller Clapeyron-slopes, as they impose kinks in the linear conformations of the lipid acyl-chains, resulting in substantial free volume fluctuations in the bilayer and thus significantly reducing the ordering effect caused by HPP. Thus, to maintain the physiological relevant fluid-like (L α ) state at high pressures, more of such cis -unsaturated (or polyunsaturated) lipids are incorporated into cellular membranes of deep-sea organisms, providing a nice example of efficient homeoviscous adaptation through modulation of fatty acid synthesis patterns. ,− In addition to changes in lipid chain structure, nature is able to control the fluidity and robustness of its cellular membranes by other means, such as the incorporation of sterols, polyisoprenoids, and other small apolar molecules. ,, …”