Protein adaptation to low temperatures: a comparative study of ?-tubulin sequences in mesophilic and psychrophilic algae

Willem, Sabine; Srahna, Mohammed; Devos, Nathalie; Gerday, Charles; Loppes, Roland; Matagne, René-Fernand

doi:10.1007/s007920050119

Cited by 29 publications

(22 citation statements)

References 15 publications

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“…Nucleic-acid-binding proteins relieve the adverse effects of low temperatures and could play a central role in the cold adaptation of psychrophiles (17,18). Other adaptive strategies developed by psychrophilic organisms involve the regulation of ion channel permeability, seasonal dormancy and microtubule polymerization (19)(20)(21). In addition to these cellular adaptations, a key adaptive strategy of psychrophiles is the modification of enzyme kinetics, allowing the emergence of metabolic rates compatible to life at low temperatures.…”

Section: Psychrophilic Organismsmentioning

confidence: 99%

Extreme catalysts from low-temperature environments

Hoyoux

Blaise

Collins

et al. 2004

Journal of Bioscience and Bioengineering

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Cold-loving or psychrophilic organisms are widely distributed in nature as a large part of the earth's surface is at temperatures around 0°C. To maintain metabolic rates and to prosper in cold environments, these extremophilic organisms have developed a vast array of adaptations. One main adaptive strategy developed in order to cope with the reduction of chemical reaction rates induced by low temperatures is the synthesis of cold-adapted or psychrophilic enzymes. These enzymes are characterized by a high catalytic activity at low temperatures associated with a low thermal stability. A study of protein adaptation strategies suggests that the high activity of psychrophilic enzymes could be achieved by the destabilization of the active site, allowing the catalytic center to be more flexible at low temperatures, whereas other protein regions may be destabilized or as rigid as their mesophilic counterparts. Due to these particular properties, psychrophilic enzymes offer a high potential not only for fundamental research but also for biotechnological applications.[Key words: psychrophile, extremophiles, cold adaptation, enzyme kinetics, flexibility strategy]Life under low-temperature conditions was identified as early as 1840 by Hooker, who observed that algae were associated with sea ice. In 1887, Forster was the first who reported that microorganisms isolated from fish could grow well at 0°C (1). The term "psychrophilic" was first used in 1902 by Schmidt-Nielsen to describe such cold-adapted organisms (2). Psychrophile is defined as an organism, prokaryotic or eukaryotic, living permanently at temperatures close to the freezing point of water in thermal equilibrium with the medium. Thus psychrophiles are numerous, including a large range of species of gram-positive and gram-negative bacteria, yeast, algae, marine invertebrates, insects and polar fish, and are widely distributed (3). Psychrophiles have developed mechanisms of adaptation to temperature including a huge range of structural and physiological adjustments in order to cope with the deleterious effect of low temperatures. Indeed, they display metabolic fluxes at low temperatures that are more or less comparable to those exhibited by closely related mesophiles living at moderate temperatures (4-6). This is explained by the capability of these psychrophilic organisms to produce "cold-adapted" enzymes which are able to cope with the reduction of chemical reaction rates induced by low temperatures. However, most cellular adaptations to low temperatures and the underlying molecular mechanisms are not fully understood and are still being investigated. Moreover, a study of proteins and enzymes from cold-adapted organisms is not only useful in the understanding of some general processes related to the protein structure and function but also in protein folding investigations. In addition, cold-active and heat-labile psychrophilic enzymes possess an interesting biotechnological potential.

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Section: Psychrophilic Organismsmentioning

confidence: 99%

Extreme catalysts from low-temperature environments

Hoyoux

Blaise

Collins

et al. 2004

Journal of Bioscience and Bioengineering

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“…The near universal substitution of Leu or Phe for Met at position 302 of the Antarctic fish ␣-chains may create a pocket of greater hydrophobicity that constrains additional water molecules whose release on subunit association would increase the entropy of polymerization. Similarly, ␣-tubulins from two psychrophilic algae of the genus Chloromonas contain lateral hydrophobic substitutions (M268V and A295V relative to the ␣-tubulins of the temperate alga Chlamydomonas reinhardtii) that are likely to increase the hydrophobicity of their lateral contact surfaces (45). Third, the ␤:Y202F substitution may stabilize the assembly-competent conformation of tubulin.…”

Section: Cold Adaptation Of Microtubule Assembly Via Small Numbers Ofmentioning

confidence: 99%

Cold Adaptation of Microtubule Assembly and Dynamics

Detrich¹,

Parker²,

Williams³

et al. 2000

Journal of Biological Chemistry

143

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The microtubules of Antarctic fishes, unlike those of homeotherms, assemble at very low temperatures (؊1.8°C). The adaptations that enhance assembly of these microtubules are intrinsic to the tubulin dimer and reduce its critical concentration for polymerization at 0°C to ϳ0.9 mg/ml (Williams, R. C., Jr., Correia, J. J., and DeVries, A. L. (1985) Biochemistry 24, 2790 -2798). Here we demonstrate that microtubules formed by pure brain tubulins of Antarctic fishes exhibit slow dynamics at both low (5°C) and high (25°C) temperatures; the rates of polymer growth and shortening and the frequencies of interconversion between these states are small relative to those observed for mammalian microtubules (37°C). To investigate the contribution of tubulin primary sequence variation to the functional properties of the microtubules of Antarctic fishes, we have sequenced brain cDNAs that encode 9 ␣-tubulins and 4 ␤-tubulins from the yellowbelly rockcod Notothenia coriiceps and 4 ␣-tubulins and 2 ␤-tubulins from the ocellated icefish Chionodraco rastrospinosus. The tubulins of these fishes were found to contain small sets of unique or rare residue substitutions that mapped to the lateral, interprotofilament surfaces or to the interiors of the ␣-and ␤-polypeptides; longitudinal interaction surfaces are not altered in the fish tubulins. Four changes (A278T and S287T in ␣; S280G and A285S in ␤) were present in the S7-H9 interprotofilament "M" loops of some monomers and would be expected to increase the flexibility of these regions. A fifth lateral substitution specific to the ␣-chain (M302L or M302F) may increase the hydrophobicity of the interprotofilament interaction. Two hydrophobic substitutions (␣:S187A in helix H5 and ␤:Y202F in sheet S6) may act to stabilize the monomers in conformations favorable to polymerization. We propose that cold adaptation of microtubule assembly in Antarctic fishes has occurred in part by evolutionary restructuring of the lateral surfaces and the cores of the tubulin monomers.The capacity of the cytoplasmic tubulins of Antarctic fishes to form microtubules at temperatures as low as Ϫ1.8°C, the freezing point of the seawater habitat of these fish, is remarkable. The critical concentration for polymerization at 0°C of purified, MAP 1 -free brain tubulin is ϳ0.9 mg/ml (1-3), which approximates the values observed for mammalian brain tubulins at 37°C (1, 4). Unlike mammalian microtubules, however, the cytoplasmic microtubules of Antarctic fishes are very stable and exhibit slow dynamics at cold temperatures (5, 6). Evidently, both the capacity to polymerize at low critical concentration and the slow exchange of tubulin dimers into and out of microtubule polymers are properties intrinsic to the tubulin subunits of these fishes. These unusual functional characteristics must be explicable by structural alterations to the primary sequences and/or by changes in the posttranslational modifications of the tubulin chains that, alone or in concert, modify the quaternary interactions between dimers in a microtu...

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“…For example, psychophilic fish (e.g., Notothenia coriiceps; Detrich et al, 2000), ciliates (e.g., Euplotes focardii; Pucciarelli and Miceli, 2002) and algae (e.g., Chloromonas sp. ; Willem et al, 1999) have all substituted amino acids at lateral contact points between protofilaments that increase hydrophobicity and/or flexibility, thereby increasing the predicted entropy (ΔS) of the system and facilitating polymerization (Fygenson et al, 1994;Niranjan et al, 2003). Note that gains in ion pairing between subunits could also contribute to polymerization (e.g., by reducing ΔH), but no such interactions have been confirmed in available models.…”

Section: Ice Worm Amino Acid Substitution Comparisonsmentioning

confidence: 92%