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.

Keywords: Adaptation; Crowding; Extremophiles; Hydrostatic pressure; Osmolytes; Temperature.

Fig. 1

The effects of TMAO and urea on the rate of labeling of sulfhydryl groups of glutamate dehydrogenase by the reagent 4-chloro-7-nitrobenzofurazan (Nbf-Cl). Control mixtures had neither TMAO nor urea. The structures of TMAO and urea are shown to the right of the graph. (Figure redrawn after Yancey and Somero 1979)

Fig. 2

Efficacies of differently methylated forms of glycine in offsetting salt-induced inhibition (300 mol/L NaCl) of an enzyme (malate dehydrogenase from barley). Activation rises as additional methyl groups are added. (Figure redrawn after Pollard and Wynn-Jones 1979)

Fig. 3

The efficacies of different organic osmolytes in stabilizing the structures of malate dehydrogenase (MDH) and staphylococcal nuclease (SNase). Osmolyte concentrations were 0.5 mol/L except for GGG, which was 0.4 mol/L. Chemical structures of the extremolytes, MG (mannosylglycerate), GG (glucosylglycerate), DIP (di-myo-inositol 1-3’phosphate) and GGG (α(1,6)glucosyl-α(1,2) glucosylglycerate) are shown to right of the graph. (Figure modified after Lamosa et al. 2013)

Fig. 4

The effects of TMAO, urea, and KCl concentration on the stability of an RNA thermometer. The filled black circle indicates no added solutes to the buffer mixture. TMAO and urea were separately added to solutions that contained either 25 mmol/L or 150 mmol/L KCl. (Figure redrawn after Gao et al. 2017a)

Fig. 5

A Depth-related concentrations of TMAO in skeletal muscle of marine bony fishes belonging to 9 families. Each point represents a single specimen captured at the depth shown on the X-axis. Data for three species captured at multiple depths are indicated by open symbols: the rattail fish Coryphaenoides armatus (open circles); the rattail fish Coryphaenoides yaquinae (open squares), and the Marianas Trench snailfish, Pseudoliparis swirei (open triangles). (Figure redrawn after Yancey 2020). B Depth-related patterns of urea and TMAO concentrations in skeletal muscle of 15 species of marine chondrichthyan fishes (sharks, skates, chimeras, and rays). Each point represents either the urea or TMAO concentration from a single specimen. (Figure redrawn after Laxon et al. 2011)

Fig. 6

The effects of bovine serum albumin (BSA) concentration on the thermal stability (upper panel) and catalytic activity (lower panel) of the mitochondrial paralog of malate dehydrogenase (mMDH). (Figure redrawn after Lin et al. 2002)