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Community Ecology of Deinococcus in Irradiated Soil

  • Matthew Chidozie Ogwu
  • Sathiyaraj Srinivasan
  • Ke Dong
  • Dhamodharan Ramasamy
  • Bruce WaldmanEmail author
  • Jonathan M. AdamsEmail author
Environmental Microbiology

Abstract

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.

Keywords

Bacterial community Deinococcus–Thermus Gamma irradiation 16S rRNA sequencing Legacy effects Radiation-resistant 

Notes

Authors’ Contributions

JA and SS conceived the research questions and prepared the project strategy. KD did the field sampling and supervised the irradiation treatments, laboratory work, and 16S sequencing. MCO carried out the bioinformatics analysis of the 16s amplicon datasets, devised the data analysis methods, and carried out the analysis with contributions from SS and DR. MCO and JA interpreted the results, prepared all the draft versions, and co-wrote the main manuscript text. BW advised on the project at all stages. All the authors improved, reviewed, and approved the revisions and accepted the final manuscript.

Funding Information

This work was supported by the Basic Science Research Program of the National Research Foundation of Korea funded by the Ministry of Education (2016E1D1A1B03930385 and 2017R1D1A1B03035583). Matthew Chidozie Ogwu received the research support of BK-21 and the National Institute for International Education, Republic of Korea. Dhamodharan Ramasamy is a recipient of BK-21 Plus Postdoctoral Fellowship, Republic of Korea.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no competing interests.

Supplementary material

248_2019_1343_MOESM1_ESM.docx (1.6 mb)
ESM 1 (DOCX 1666 kb)

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Matthew Chidozie Ogwu
    • 1
    • 2
  • Sathiyaraj Srinivasan
    • 3
  • Ke Dong
    • 4
  • Dhamodharan Ramasamy
    • 1
  • Bruce Waldman
    • 1
    • 5
    Email author
  • Jonathan M. Adams
    • 6
    Email author
  1. 1.School of Biological SciencesSeoul National UniversityGwanak-guRepublic of Korea
  2. 2.Department of Plant Biology and BiotechnologyUniversity of BeninBenin CityNigeria
  3. 3.Department of Bio and Environmental Technology, Division of Environmental and Life Science, College of Natural ScienceSeoul Women’s UniversityNowon-guRepublic of Korea
  4. 4.Department of Life SciencesKyonggi UniversitySuwonRepublic of Korea
  5. 5.Department of Integrative BiologyOklahoma State UniversityStillwaterUSA
  6. 6.School of Geographic and Oceanographic SciencesNanjing UniversityNanjingPeople’s Republic of China

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