The role of natural radiation in the evolution of ancient microbes

Natural ionizing radiation, which potentially affects biota inhabiting the Earth, can be broadly divided into two types according to origin: cosmic radiation and subsurface radiation. Cosmic radiation contains galactic cosmic rays and solar energetic particles. Subsurface radiation is derived from radionuclides such as uranium, thorium, and radon. The levels of these forms of natural radiation were not constant temporally and spatially, and underwent a lot of changes in the early Earth environment. However, the ground level radiation dose rate of secondary muons derived from a supernova event that causes the most severe biological effects among forms of cosmic radiation is estimated to be 1 sievert (Sv) per year at most, which is too low to have lethal and mutagenic effects on terrestrial microbes. On the other hand, a nuclear fission chain reaction occurred in Oklo uranium ore deposit in Gabon about 2 billion years ago and continued intermittently 10⁵-10⁶ years. The average total radiation dose rate of a typical natural fission reactor in Oklo is estimated to be 47.4 Sv per hour. This value is high enough to serve as a physical mutagen for subsurface microbes inhabiting areas near the reactor, and a million years is long enough to generate a new species of microbes. The observed growth-inhibitory critical dose rate for Escherichia coli is estimated to be 36 to 67 Gy per hour. On the other hand, the radioresistant bacterium Deinococcus radiodurans is shown to be cultivated without any growth delay at up to 126 to 180 Gy per hour of gamma rays. Recent EXAFS and isotopic analyses indicate that biogenic processes are more important for uranium ore genesis than previously understood. D. radiodurans and its closely related species Thermus thermophilus are shown to have the ability to reduce U(VI) to U(IV) under anaerobic conditions. These lines of evidence suggest that a common ancestor of Deinococcus and Thermus might be involved in the formation process of Oklo uranium ore deposit. Therefore, the radiation dose rate at Oklo-type natural nuclear reactors would be suitable for affecting the growth of microbes and generating genome evolution through accumulated mutations. (author)