Abstract
Aquifex aeolicus is a hyperthermophilic, hydrogen-oxidizing and carbon-fixing bacterium that can grow at temperatures up to 95 °C. A. aeolicus has an almost complete set of flagellar genes that are conserved in bacteria. Here we observed that A. aeolicus has polar flagellum and can swim with a speed of 90 μm s−1 at 85 °C. We expressed the A. aeolicus mot genes (motA and motB), which encode the torque generating stator proteins of the flagellar motor, in a corresponding mot nonmotile mutant of Escherichia coli. Its motility was slightly recovered by expression of A. aeolicus MotA and chimeric MotB whose periplasmic region was replaced with that of E. coli. A point mutation in the A. aeolicus MotA cytoplasmic region remarkably enhanced the motility. Using this system in E. coli, we demonstrate that the A. aeolicus motor is driven by Na+. As motor proteins from hyperthermophilic bacteria represent the earliest motor proteins in evolution, this study strongly suggests that ancient bacteria used Na+ for energy coupling of the flagellar motor. The Na+-driven flagellar genes might have been laterally transferred from early-branched bacteria into late-branched bacteria and the interaction surfaces of the stator and rotor seem not to change in evolution.
Highlights
Aquifex aeolicus is a hyperthermophilic, hydrogen-oxidizing and carbon-fixing bacterium that can grow at temperatures up to 95 °C
We cultivated the wild-type A. aeolicus VF5 strain in inorganic medium under a H2/CO2/O2 gas atmosphere at its optimum growth temperature of 85 °C, and the cultivated cells were observed by transmission electron microscope (TEM) using negative staining
We focused on the flagella, which have one of the most important roles for survival strategy of bacteria, of the hyperthermophilic bacterium, A. aeolicus
Summary
Aquifex aeolicus is a hyperthermophilic, hydrogen-oxidizing and carbon-fixing bacterium that can grow at temperatures up to 95 °C. We expressed the A. aeolicus mot genes (motA and motB), which encode the torque generating stator proteins of the flagellar motor, in a corresponding mot nonmotile mutant of Escherichia coli. We focused on the formation and the function of flagella of the hyperthermophilic bacterium, A. aeolicus We cultured this hyperthermophilic bacterium and observed its flagellum and motile behavior. From this bacterium, we cloned the genes for the stator and found that the stator of A. aeolicus could be compatible with the native stator of E. coli, by replacement of the periplasmic region of the A. aeolicus stator with that of E. coli. We discuss the thermo-stabilized feature of the flagellar system of hyperthermophilic bacteria, the ion selectivity and universal function of the stator units as torque generators in the motor, and the phylogenetic relationship of stators among bacterial species
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