A general overview of the multifactorial adaptation to cold: biochemical mechanisms and strategies

Abstract

Cold environments are more frequent than people think. They include deep oceans, cold lakes, snow, permafrost, sea ice, glaciers, cold soils, cold deserts, caves, areas at elevations greater than 3000 m, and also artificial refrigeration systems. These environments are inhabited by a diversity of eukaryotic and prokaryotic organisms that must adapt to the hard conditions imposed by cold. This adaptation is multifactorial and includes (i) sensing the cold, mainly through the modification of the liquid-crystalline membrane state, leading to the activation of a two-component system that transduce the signal; (ii) adapting the composition of membranes for proper functions mainly due to the production of double bonds in lipids, changes in hopanoid composition, and the inclusion of pigments; (iii) producing cold-adapted proteins, some of which show modifications in the composition of amino acids involved in stabilizing interactions and structural adaptations, e.g., enzymes with high catalytic efficiency; and (iv) producing ice-binding proteins and anti-freeze proteins, extracellular polysaccharides and compatible solutes that protect cells from intracellular and extracellular ice. However, organisms also respond by reprogramming their metabolism and specifically inducing cold-shock and cold-adaptation genes through strategies such as DNA supercoiling, distinctive signatures in promoter regions and/or the action of CSPs on mRNAs, among others. In this review, we describe the main findings about how organisms adapt to cold, with a focus in prokaryotes and linking the information with findings in eukaryotes.

Keywords: Cold adaptation; Cold-shock proteins; Compatible solutes; Metabolism; Psychrophiles.

Fig. 1

Chemical structure of some molecules involved in avoiding freezing and restoring the liquid crystalline state of cellular membranes. a The structure of some acyl chains and; b the structure of carotenoids and hopanoids (a subgroup of triterpenoids)

Fig. 2

Production of unsaturated (UFA) and saturated fatty acids (SFA). a The pathways for UFA and SFA synthesis in E. coli and, some relevant enzymes. FabA introduces trans double bonds and also isomerized trans to cis; FabB elongates the cis-FA produced by FabA; FabF and FabH are also elongation enzymes; and ACP means Acyl carrier protein. b A simplified diagram of fabA and fabB transcriptional regulation by FabR

Fig. 3

Representation of the membrane-bound sensor with histidine kinase/phosphatase activity, DesK. The figure shows the two protamers with the five transmembrane segments (sensor domain) and the regions (2-HCC and DHp) that link the sensor domain and the catalytic and ATP-binding domain. Nt and Ct means N-terminal and C-terminal domain

Fig. 4

Sensing temperature; the DesKR two component system. At high temperature, a the desKR mRNA is expressed; the membrane is in liquid-crystalline phase and DesK shows phosphatase activity; thus, DesR is inactive (non-phosphorylated). At low temperature, (b1) des mARN and desKR mRNA are expressed; the membrane is in gel phase and DesK shows kinase activity; DesR is active (phosphorylated) and acts as transcriptional activator of des mARN; Des is active and introduce insaturations in membrane acyl chains. After the introduction of insaturations by Des (b2), the membrane goes back to the liquid-crystalline phase; DesK goes back to the phosphate activity and inactivates Des

Fig. 5

General features involved in cold adaptation of psychrophilic enzymes

Fig. 6

The diversity of antifreeze protein structures. The figure shows examples of structures of antifreeze proteins produced by a Marinomonas primoryensis (3p4g.pdb), b Hypogastrura harveyi (3boi.pdb); c Tenebrio molitor (1c3y.pdb); d Choristoneura fumiferana (1l0s.pdb); e Myoxocephalus scorpius (1y03.pdb); f) Zoarces americanus (2msi. pdb); g Leucosporidium sp. AY30 (3uyu.pdb); h Pseudopleuronectes americanus (4ke2.pdb). This figure was generated using Chimera 1.16 (Goddard et al., 2004)

Fig. 7

Mechanisms involved in the induction of cold-shock and cold adaptation genes. See main text for details

Fig. 8

Futile cycles in brown adipose tissue (BAT) cells. The cells can increase energy expenditure by activating futile cycles; these cycles need ATP derived from mitochondria that remain coupled. This figure shows a schematic vision of the cycles and how they work. a Lipid cycling, ATGL: adipose triglyceride lipase; FFA: free fatty acid; glycerol k: glycerol kinase; TGA: triacylglycerides. b Calcium cycling, RyR2: ryanodine Ca²⁺ channel; SERCA 2b: sarcoendoplasmic reticulum Ca²⁺ ATPase; PDH: pyruvate dehydrogenase; AcCoA: acetyl-CoA. c Creatine cycling, ACC, ATP/ADP carrier; MiCK, mitochondrial creatine kinase; PCr-ase, phosphocreatine phosphatase; IMS, mitochondrial intermembrane compartment