DNA supercoiling and temperature adaptation: A clue to early diversification of life?

Cellular systems to control an appropriate DNA geometry for function probab ly evolved simultaneously with DNA genomes. Such systems are basically DNA topoisomerases and DNA-binding proteins. Therefore, their distribution in e xtant organisms may be a source of information on early evolution and the n ature of the last common ancestor (cenancestor). Most living beings need th e strand-opening potential of negative DNA supercoiling to allow transcript ion and other DNA-dependent processes. Mesophiles have global negatively su percoiled DNA, essentially due to gyrase (introducing negative supercoils) in bacteria and to DNA wrapping around histone cores in eukaryotes. Mesophi lic archaea, halophilic methanogens, and halophiles might use a gyrase, whe reas some methanogens might use histone wrapping. The existence of these tw o distinct mechanisms suggests that mesophily appeared at least twice in ev olution. On the other hand, only one system which is based on reverse gyras e (introducing positive supercoils) appears to be required for hyperthermop hilic life. Archaeal hyperthermophiles lacking gyrase have relaxed to posit ively supercoiled DNA, but hyperthermophilic bacteria of the genus Thermoto ga, which have both gyrase and reverse gyrase, have negative supercoiling. This suggests that reverse gyrase is necessary at least locally, but wherea s these hyperthermophilic bacteria favor general melting potential and stab ility at critical active regions, hyperthermophilic archaea favor general l inking excess and local melting. In this context, the existence of a thermo philic (60-80 degrees C) ancestor endowed with only relaxing topoisomerases is hypothesized. Such temperatures allow a compromise between melting pote ntial and stability, i.e., an appropriate DNA geometry for function. Subseq uent duplication and functional specialization of existing DNA topoisomeras es would then have facilitated adaptation to hyperthermophily and mesophily in archaea and bacteria, respectively. If reverse gyrase is an ancient cha racter in hyperthermophilic bacteria, the cenancestor would have already be en a hyperthermophile. Histone sequence homology and similarities of nucleo some structural dynamics suggest that eukaryotes inherited this system for DNA structural homeostasis from methanogenic euryarchaea. Some mesophilic a rchaea would have improved their adaptability to mesophily by importing gyr ase from bacteria.