Prospects for Fungal Bioremediation of Acidic Radioactive Waste Sites: Characterization and Genome Sequence of Rhodotorula taiwanensis MD1149.

Rok Tkavc,Clifton L Dalgard,Theron Hamilton,Bonnee Rubinfeld,Lawrence Dugan,Jatinder Singh,Elena K Gaidamakova,Vera Y Matrosova,Michael J Daly,Polina Klimenkova,Mathew G Lyman,Cene Gostinčar,Robert P Volpe,Stephanie Malfatti ,Nina Gunde‐Cimerman ,K G Frey ,Mélanie Courtot ,Carol L Ecale Zhou ,Olga Grichenko ,Benjamin Stewart

doi:10.3389/fmicb.2017.02528

Abstract

Highly concentrated radionuclide waste produced during the Cold War era is stored at US Department of Energy (DOE) production sites. This radioactive waste was often highly acidic and mixed with heavy metals, and has been leaking into the environment since the 1950s. Because of the danger and expense of cleanup of such radioactive sites by physicochemical processes, in situ bioremediation methods are being developed for cleanup of contaminated ground and groundwater. To date, the most developed microbial treatment proposed for high-level radioactive sites employs the radiation-resistant bacterium Deinococcus radiodurans. However, the use of Deinococcus spp. and other bacteria is limited by their sensitivity to low pH. We report the characterization of 27 diverse environmental yeasts for their resistance to ionizing radiation (chronic and acute), heavy metals, pH minima, temperature maxima and optima, and their ability to form biofilms. Remarkably, many yeasts are extremely resistant to ionizing radiation and heavy metals. They also excrete carboxylic acids and are exceptionally tolerant to low pH. A special focus is placed on Rhodotorula taiwanensis MD1149, which was the most resistant to acid and gamma radiation. MD1149 is capable of growing under 66 Gy/h at pH 2.3 and in the presence of high concentrations of mercury and chromium compounds, and forming biofilms under high-level chronic radiation and low pH. We present the whole genome sequence and annotation of R. taiwanensis strain MD1149, with a comparison to other Rhodotorula species. This survey elevates yeasts to the frontier of biology's most radiation-resistant representatives, presenting a strong rationale for a role of fungi in bioremediation of acidic radioactive waste sites.

Highlights

Between 1945 and 1986, immense volumes of radioactive waste were generated from the production of 46,000 nuclear weapons in the United States
Over the last six decades, these radioactive wastes have been leaking into the environment, including mixtures of radionuclides, heavy metals and strong acids (e.g., HNO3) at levels that exceed those tolerated by most microorganisms (Brim et al, 2000; Daly, 2000)
We studied 16 ascomycetous and 11 basidiomycetous yeasts isolated from diverse environments including arctic ice, acid mine drainage, red wine, and apple juice, as well as dry environments with elevated temperatures (Table 1)

Summary

Introduction

Between 1945 and 1986, immense volumes of radioactive waste were generated from the production of 46,000 nuclear weapons in the United States. As a result of the chemical reprocessing of 1.1 × 108 kg of nuclear fuel at the Hanford Site (WA, USA) alone, 2.1 × 105 m3 of radioactive waste were produced at nine reactors and stored in 177 underground tanks. These storage tanks with a lifespan of 10–20 years have been used since 1943, and the first leaks were confirmed in 1959. The scale of these waste environments leaves few options for cleanup other than bioremediation (Brim et al, 2000)

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Results

Conclusion