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

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 expens...

Full description

Bibliographic Details
Main Authors: Rok Tkavc, Vera Y. Matrosova, Olga E. Grichenko, Cene Gostinčar, Robert P. Volpe, Polina Klimenkova, Elena K. Gaidamakova, Carol E. Zhou, Benjamin J. Stewart, Mathew G. Lyman, Stephanie A. Malfatti, Bonnee Rubinfeld, Melanie Courtot, Jatinder Singh, Clifton L. Dalgard, Theron Hamilton, Kenneth G. Frey, Nina Gunde-Cimerman, Lawrence Dugan, Michael J. Daly
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.02528/full
_version_ 1811195284530659328
author Rok Tkavc
Rok Tkavc
Vera Y. Matrosova
Vera Y. Matrosova
Olga E. Grichenko
Olga E. Grichenko
Cene Gostinčar
Robert P. Volpe
Robert P. Volpe
Polina Klimenkova
Polina Klimenkova
Elena K. Gaidamakova
Elena K. Gaidamakova
Carol E. Zhou
Benjamin J. Stewart
Mathew G. Lyman
Stephanie A. Malfatti
Bonnee Rubinfeld
Melanie Courtot
Jatinder Singh
Clifton L. Dalgard
Clifton L. Dalgard
Theron Hamilton
Kenneth G. Frey
Nina Gunde-Cimerman
Lawrence Dugan
Michael J. Daly
author_facet Rok Tkavc
Rok Tkavc
Vera Y. Matrosova
Vera Y. Matrosova
Olga E. Grichenko
Olga E. Grichenko
Cene Gostinčar
Robert P. Volpe
Robert P. Volpe
Polina Klimenkova
Polina Klimenkova
Elena K. Gaidamakova
Elena K. Gaidamakova
Carol E. Zhou
Benjamin J. Stewart
Mathew G. Lyman
Stephanie A. Malfatti
Bonnee Rubinfeld
Melanie Courtot
Jatinder Singh
Clifton L. Dalgard
Clifton L. Dalgard
Theron Hamilton
Kenneth G. Frey
Nina Gunde-Cimerman
Lawrence Dugan
Michael J. Daly
author_sort Rok Tkavc
collection DOAJ
description 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.
first_indexed 2024-04-12T00:40:58Z
format Article
id doaj.art-b919e934934f4f2cb0d915ffeb94ff35
institution Directory Open Access Journal
issn 1664-302X
language English
last_indexed 2024-04-12T00:40:58Z
publishDate 2018-01-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Microbiology
spelling doaj.art-b919e934934f4f2cb0d915ffeb94ff352022-12-22T03:55:02ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-01-01810.3389/fmicb.2017.02528305317Prospects for Fungal Bioremediation of Acidic Radioactive Waste Sites: Characterization and Genome Sequence of Rhodotorula taiwanensis MD1149Rok Tkavc0Rok Tkavc1Vera Y. Matrosova2Vera Y. Matrosova3Olga E. Grichenko4Olga E. Grichenko5Cene Gostinčar6Robert P. Volpe7Robert P. Volpe8Polina Klimenkova9Polina Klimenkova10Elena K. Gaidamakova11Elena K. Gaidamakova12Carol E. Zhou13Benjamin J. Stewart14Mathew G. Lyman15Stephanie A. Malfatti16Bonnee Rubinfeld17Melanie Courtot18Jatinder Singh19Clifton L. Dalgard20Clifton L. Dalgard21Theron Hamilton22Kenneth G. Frey23Nina Gunde-Cimerman24Lawrence Dugan25Michael J. Daly26Department of Pathology, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, United StatesDepartment of Pathology, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, United StatesDepartment of Pathology, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, United StatesDepartment of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, SloveniaDepartment of Pathology, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, United StatesDepartment of Pathology, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, United StatesDepartment of Pathology, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, United StatesLawrence Livermore National Laboratory, Computing Applications and Research Department, Livermore, CA, United StatesBiosciences and Biotechnology Division, Physics and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, United StatesBiosciences and Biotechnology Division, Physics and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, United StatesBiosciences and Biotechnology Division, Physics and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, United StatesBiosciences and Biotechnology Division, Physics and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, United StatesEuropean Molecular Biology Laboratory, European Bioinformatics Institute, Cambridge, United KingdomCollaborative Health Initiative Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesDepartment of Anatomy, Physiology and Genetics, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesThe American Genome Center, Bethesda, MD, United States0Biological Defense Research Directorate, Naval Medical Research Center, Fredrick, MD, United States0Biological Defense Research Directorate, Naval Medical Research Center, Fredrick, MD, United StatesDepartment of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, SloveniaBiosciences and Biotechnology Division, Physics and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, CA, United StatesDepartment of Pathology, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesHighly 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.http://journal.frontiersin.org/article/10.3389/fmicb.2017.02528/fullbioremediationyeastsradiation resistanceheavy metal resistancepH minimumtemperature maximum
spellingShingle Rok Tkavc
Rok Tkavc
Vera Y. Matrosova
Vera Y. Matrosova
Olga E. Grichenko
Olga E. Grichenko
Cene Gostinčar
Robert P. Volpe
Robert P. Volpe
Polina Klimenkova
Polina Klimenkova
Elena K. Gaidamakova
Elena K. Gaidamakova
Carol E. Zhou
Benjamin J. Stewart
Mathew G. Lyman
Stephanie A. Malfatti
Bonnee Rubinfeld
Melanie Courtot
Jatinder Singh
Clifton L. Dalgard
Clifton L. Dalgard
Theron Hamilton
Kenneth G. Frey
Nina Gunde-Cimerman
Lawrence Dugan
Michael J. Daly
Prospects for Fungal Bioremediation of Acidic Radioactive Waste Sites: Characterization and Genome Sequence of Rhodotorula taiwanensis MD1149
Frontiers in Microbiology
bioremediation
yeasts
radiation resistance
heavy metal resistance
pH minimum
temperature maximum
title Prospects for Fungal Bioremediation of Acidic Radioactive Waste Sites: Characterization and Genome Sequence of Rhodotorula taiwanensis MD1149
title_full Prospects for Fungal Bioremediation of Acidic Radioactive Waste Sites: Characterization and Genome Sequence of Rhodotorula taiwanensis MD1149
title_fullStr Prospects for Fungal Bioremediation of Acidic Radioactive Waste Sites: Characterization and Genome Sequence of Rhodotorula taiwanensis MD1149
title_full_unstemmed Prospects for Fungal Bioremediation of Acidic Radioactive Waste Sites: Characterization and Genome Sequence of Rhodotorula taiwanensis MD1149
title_short Prospects for Fungal Bioremediation of Acidic Radioactive Waste Sites: Characterization and Genome Sequence of Rhodotorula taiwanensis MD1149
title_sort prospects for fungal bioremediation of acidic radioactive waste sites characterization and genome sequence of rhodotorula taiwanensis md1149
topic bioremediation
yeasts
radiation resistance
heavy metal resistance
pH minimum
temperature maximum
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.02528/full
work_keys_str_mv AT roktkavc prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT roktkavc prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT veraymatrosova prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT veraymatrosova prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT olgaegrichenko prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT olgaegrichenko prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT cenegostincar prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT robertpvolpe prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT robertpvolpe prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT polinaklimenkova prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT polinaklimenkova prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT elenakgaidamakova prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT elenakgaidamakova prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT carolezhou prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT benjaminjstewart prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT mathewglyman prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT stephanieamalfatti prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT bonneerubinfeld prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT melaniecourtot prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT jatindersingh prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT cliftonldalgard prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT cliftonldalgard prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT theronhamilton prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT kennethgfrey prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT ninagundecimerman prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT lawrencedugan prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149
AT michaeljdaly prospectsforfungalbioremediationofacidicradioactivewastesitescharacterizationandgenomesequenceofrhodotorulataiwanensismd1149