Community Ecology of Deinococcus in Irradiated Soil

Deinococcus is a genus of soil bacteria known for radiation resistance. However, the effects of radiation exposure on its community structure are unknown. We exposed soil to three levels of gamma radiation, 0.1 kGy/h (low), 1 kGy/h (medium), and 3 kGy/h (high), once a week for 6 weeks and then extracted soil DNA for 16S rRNA amplicon sequencing. We found the following: (1) Increasing radiation dose produced a major increase in relative abundance of Deinococcus, reaching ~ 80% of reads at the highest doses. Differing abundances of the various Deinococcus species in relation to exposure levels indicate distinct "radiation niches." At 3 kGy/h, a single OTU identified as D. ficus overwhelmingly dominated the mesocosms. (2) Corresponding published genome data show that the dominant species at 3 kGy/h, D. ficus, has a larger and more complex genome than other Deinococcus species with a greater proportion of genes related to DNA and nucleotide metabolism, cell wall, membrane, and envelope biogenesis as well as more cell cycle control, cell division, and chromosome partitioning-related genes. Deinococcus ficus also has a higher guanine-cytosine ratio than most other Deinococcus. These features may be linked to genome stability and may explain its greater abundance in this apparently competitive system, under high-radiation exposures. (3) Genomic analysis suggests that Deinococcus, including D. ficus, are capable of utilizing diverse carbon sources derived from both microbial cells killed by the radiation (including C5-C12-containing compounds, like arabinose, lactose, N-acetyl-D-glucosamine) and plant-derived organic matter in the soil (e.g., cellulose and hemicellulose). (4) Overall, based on its metagenome, even the most highly irradiated (3 kGy/h) soil possesses a wide range of the activities necessary for a functional soil system. Future studies may consider the resilience and sustainability of such soils in a high-radiation environment.