Microtubule assembly in cold-adapted organisms: functional properties and structural adaptations of tubulins from antarctic fishes.
Fishes native to the coastal waters of the Antarctic have adapted to habitat and body temperatures in the range -1.8 to +2 degrees C. Their cytoplasmic microtubules, unlike those of mammals and temperate poikilotherms, have evolved to assemble efficiently at these low temperatures. To learn about the underlying molecular adaptations, my laboratory is studying microtubule proteins [tubulin alpha beta dimers and microtubule-associated proteins (MAPs)] and tubulin genes from several Antarctic fishes, including the rockcods Notothenia coriiceps and Gobionotothen gibberifrons. We find that the assembly-enhancing adaptations of the fish microtubule proteins are intrinsic to the tubulin subunits themselves. Furthermore, microtubule formation by Antarctic fish tubulins is strongly entropy driven, due in part to an increased reliance, relative to tubulins from other species, on hydrophobic interactions. Based on analyses of tubulin polypeptides and cDNAs, we suggest that the structural adaptations of Antarctic fish tubulins most likely involve alterations in the primary sequences of tubulin isotypes. With respect to neural beta tubulins from other vertebrates, for example, the class II beta-tubulin isotype of N. coriiceps brain contains seven unique amino acid substitutions and one novel insertion in its 446-residue primary sequence. Most of these changes are located in a structural domain that forms contacts between tubulin dimers during microtubule assembly and would be expected to enhance polypeptide flexibility, thereby facilitating addition of tubulin to microtubule ends. The acidic carboxy-terminal tails of the alpha and beta tubulins, by contrast, appear not to be sites of cold adaptation of polymerization. We have also found that brain and egg tubulins from Antarctic fishes differ strikingly in their polymerization efficiencies, which demonstrates, in agreement with the multitubulin hypothesis, that tissue-specific tubulin isoforms can possess distinct functional properties. Thus, study of microtubule proteins from organisms, such as the Antarctic fishes, that have adapted to extreme thermal regimes should contribute significantly to an understanding of the quaternary interactions that control microtubule assembly in all eukaryotes.
Detrich
H W
HW
Department of Biology, Northeastern University, Boston, MA 02115, USA.
D000222:Adaptation, Physiological; D000595:Amino Acid Sequence; D000818:Animals; D000864:Antarctic Regions; D001483:Base Sequence; D001704:Biopolymers / Q000737:chemistry / Q000378:metabolism; D001921:Brain / Q000378:metabolism; D003081:Cold Climate; D018076:DNA, Complementary / Q000235:genetics; D005260:Female; D005399:Fishes / Q000235:genetics / Q000378:metabolism*; D008870:Microtubules / Q000378:metabolism*; D008969:Molecular Sequence Data; D010063:Ovum / Q000378:metabolism; D017386:Sequence Homology, Amino Acid; D013696:Temperature; D013816:Thermodynamics; D014404:Tubulin / Q000737:chemistry* / Q000235:genetics / Q000378:metabolism*
D001704:Biopolymers; D018076:DNA, Complementary; D014404:Tubulin