skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Proteogenomic Analysis of Burkholderia Species Strains 25 and 46 Isolated from Uraniferous Soils Reveals Multiple Mechanisms to Cope with Uranium Stress

Abstract

Two Burkholderia spp. (strains SRS-25 and SRS-46) were isolated from high concentrations of uranium (U) from the U.S. Department of Energy (DOE)-managed Savannah River Site (SRS). SRS contains soil gradients that remain co-contaminated by heavy metals from previous nuclear weapons production activities. Uranium (U) is one of the dominant contaminants within the SRS impacted soils, which can be microbially transformed into less toxic forms. We established microcosms containing strains SRS-25 and SRS-46 spiked with U and evaluated the microbially-mediated depletion with concomitant genomic and proteomic analysis. Both strains showed a rapid depletion of U; draft genome sequences revealed SRS-25 genome to be of approximately 8,152,324 bp, a G + C content of 66.5, containing a total 7604 coding sequences with 77 total RNA genes. Similarly, strain SRS-46 contained a genome size of 8,587,429 bp with a G + C content of 67.1, 7895 coding sequences, with 73 total RNA genes, respectively. An in-depth, genome-wide comparisons between strains 25, 46 and a previously isolated strain from our research (Burkholderia sp. strain SRS-W-2-2016), revealed a common pool of 3128 genes; many were found to be homologues to previously characterized metal resistance genes (e.g., for cadmium, cobalt, and zinc), as well as formore » transporter, stress/detoxification, cytochromes, and drug resistance functions. Furthermore, proteomic analysis of strains with or without U stress, revealed the increased expression of 34 proteins from strain SRS-25 and 52 proteins from strain SRS-46; similar to the genomic analyses, many of these proteins have previously been shown to function in stress response, DNA repair, protein biosynthesis and metabolism. Overall, this comparative proteogenomics study confirms the repertoire of metabolic and stress response functions likely rendering the ecological competitiveness to the isolated strains for colonization and survival in the heavy metals contaminated SRS soil habitat.« less

Authors:
; ; ; ; ; ; ; ORCiD logo
Publication Date:
Research Org.:
Univ. of Georgia, Athens, GA (United States); Savannah River Nuclear Solutions, Aiken, SC (United States)
Sponsoring Org.:
USDOE Office of Environmental Management (EM)
OSTI Identifier:
1485520
Alternate Identifier(s):
OSTI ID: 1614656
Grant/Contract Number:  
AC09-08SR22470; EM0004391
Resource Type:
Published Article
Journal Name:
Cells
Additional Journal Information:
Journal Name: Cells Journal Volume: 7 Journal Issue: 12; Journal ID: ISSN 2073-4409
Publisher:
MDPI
Country of Publication:
Switzerland
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Cell Biology

Citation Formats

Agarwal, Meenakshi, Pathak, Ashish, Rathore, Rajesh, Prakash, Om, Singh, Rakesh, Jaswal, Rajneesh, Seaman, John, and Chauhan, Ashvini. Proteogenomic Analysis of Burkholderia Species Strains 25 and 46 Isolated from Uraniferous Soils Reveals Multiple Mechanisms to Cope with Uranium Stress. Switzerland: N. p., 2018. Web. doi:10.3390/cells7120269.
Agarwal, Meenakshi, Pathak, Ashish, Rathore, Rajesh, Prakash, Om, Singh, Rakesh, Jaswal, Rajneesh, Seaman, John, & Chauhan, Ashvini. Proteogenomic Analysis of Burkholderia Species Strains 25 and 46 Isolated from Uraniferous Soils Reveals Multiple Mechanisms to Cope with Uranium Stress. Switzerland. doi:10.3390/cells7120269.
Agarwal, Meenakshi, Pathak, Ashish, Rathore, Rajesh, Prakash, Om, Singh, Rakesh, Jaswal, Rajneesh, Seaman, John, and Chauhan, Ashvini. Wed . "Proteogenomic Analysis of Burkholderia Species Strains 25 and 46 Isolated from Uraniferous Soils Reveals Multiple Mechanisms to Cope with Uranium Stress". Switzerland. doi:10.3390/cells7120269.
@article{osti_1485520,
title = {Proteogenomic Analysis of Burkholderia Species Strains 25 and 46 Isolated from Uraniferous Soils Reveals Multiple Mechanisms to Cope with Uranium Stress},
author = {Agarwal, Meenakshi and Pathak, Ashish and Rathore, Rajesh and Prakash, Om and Singh, Rakesh and Jaswal, Rajneesh and Seaman, John and Chauhan, Ashvini},
abstractNote = {Two Burkholderia spp. (strains SRS-25 and SRS-46) were isolated from high concentrations of uranium (U) from the U.S. Department of Energy (DOE)-managed Savannah River Site (SRS). SRS contains soil gradients that remain co-contaminated by heavy metals from previous nuclear weapons production activities. Uranium (U) is one of the dominant contaminants within the SRS impacted soils, which can be microbially transformed into less toxic forms. We established microcosms containing strains SRS-25 and SRS-46 spiked with U and evaluated the microbially-mediated depletion with concomitant genomic and proteomic analysis. Both strains showed a rapid depletion of U; draft genome sequences revealed SRS-25 genome to be of approximately 8,152,324 bp, a G + C content of 66.5, containing a total 7604 coding sequences with 77 total RNA genes. Similarly, strain SRS-46 contained a genome size of 8,587,429 bp with a G + C content of 67.1, 7895 coding sequences, with 73 total RNA genes, respectively. An in-depth, genome-wide comparisons between strains 25, 46 and a previously isolated strain from our research (Burkholderia sp. strain SRS-W-2-2016), revealed a common pool of 3128 genes; many were found to be homologues to previously characterized metal resistance genes (e.g., for cadmium, cobalt, and zinc), as well as for transporter, stress/detoxification, cytochromes, and drug resistance functions. Furthermore, proteomic analysis of strains with or without U stress, revealed the increased expression of 34 proteins from strain SRS-25 and 52 proteins from strain SRS-46; similar to the genomic analyses, many of these proteins have previously been shown to function in stress response, DNA repair, protein biosynthesis and metabolism. Overall, this comparative proteogenomics study confirms the repertoire of metabolic and stress response functions likely rendering the ecological competitiveness to the isolated strains for colonization and survival in the heavy metals contaminated SRS soil habitat.},
doi = {10.3390/cells7120269},
journal = {Cells},
number = 12,
volume = 7,
place = {Switzerland},
year = {2018},
month = {12}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.3390/cells7120269

Citation Metrics:
Cited by: 3 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

ELECTRON STAINS: I. Chemical Studies on the Interaction of DNA with Uranyl Salts
journal, July 1961


Spatial Distribution of an Uranium-Respiring Betaproteobacterium at the Rifle, CO Field Research Site
journal, April 2015


Shotgun Proteomic Analysis Unveils Survival and Detoxification Strategies by Caulobacter crescentus during Exposure to Uranium, Chromium, and Cadmium
journal, March 2014

  • Yung, Mimi C.; Ma, Jincai; Salemi, Michelle R.
  • Journal of Proteome Research, Vol. 13, Issue 4
  • DOI: 10.1021/pr400880s

Genomic complexity and plasticity of Burkholderia cepacia
journal, November 1996


Comparative proteomics of Acidithiobacillus ferrooxidans grown in the presence and absence of uranium
journal, April 2016

  • Dekker, Linda; Arsène-Ploetze, Florence; Santini, Joanne M.
  • Research in Microbiology, Vol. 167, Issue 3
  • DOI: 10.1016/j.resmic.2016.01.007

The biogeochemistry and bioremediation of uranium and other priority radionuclides
journal, January 2014


SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012

  • Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 19, Issue 5
  • DOI: 10.1089/cmb.2012.0021

Bacterial interactions with uranium: An environmental perspective
journal, December 2008


Effect of catechins and tannins on depleted uranium-induced DNA strand breaks
journal, March 2012

  • Matsuda, Emiko; Nakajima, Akira
  • Journal of Radioanalytical and Nuclear Chemistry, Vol. 293, Issue 2
  • DOI: 10.1007/s10967-012-1725-y

Uranium (U)-Tolerant Bacterial Diversity from U Ore Deposit of Domiasiat in North-East India and Its Prospective Utilisation in Bioremediation
journal, January 2013

  • Kumar, Rakshak; Nongkhlaw, Macmillan; Acharya, Celin
  • Microbes and Environments, Vol. 28, Issue 1
  • DOI: 10.1264/jsme2.ME12074

The multifarious, multireplicon Burkholderia cepacia complex
journal, January 2005

  • Mahenthiralingam, Eshwar; Urban, Teresa A.; Goldberg, Joanna B.
  • Nature Reviews Microbiology, Vol. 3, Issue 2
  • DOI: 10.1038/nrmicro1085

Bioremediation of heavy metals by growing hyperaccumulaor endophytic bacterium Bacillus sp. L14
journal, November 2010


Change in Bacterial Community Structure during In Situ Biostimulation of Subsurface Sediment Cocontaminated with Uranium and Nitrate
journal, August 2004


2016 update of the PRIDE database and its related tools
journal, November 2015

  • Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1145

Comparing thousands of circular genomes using the CGView Comparison Tool
journal, January 2012


Whole-Genome Transcriptional Analysis of Heavy Metal Stresses in Caulobacter crescentus
journal, November 2005


Uranium Biomineralization as a Result of Bacterial Phosphatase Activity:  Insights from Bacterial Isolates from a Contaminated Subsurface
journal, August 2007

  • Beazley, Melanie J.; Martinez, Robert J.; Sobecky, Patricia A.
  • Environmental Science & Technology, Vol. 41, Issue 16
  • DOI: 10.1021/es070567g

Fast gapped-read alignment with Bowtie 2
journal, March 2012

  • Langmead, Ben; Salzberg, Steven L.
  • Nature Methods, Vol. 9, Issue 4
  • DOI: 10.1038/nmeth.1923

Resistance to, and Accumulation of, Uranium by Bacteria from a Uranium-Contaminated Site
journal, March 2004


Fungi outcompete bacteria under increased uranium concentration in culture media
journal, June 2013


Reduction of Nickel and Uranium Toxicity and Enhanced Trichloroethylene Degradation to Burkholderia vietnamiensis PR1 301 with Hydroxyapatite Amendment
journal, March 2007

  • Van Nostrand, Joy D.; Khijniak, Tatiana J.; Neely, Benjamin
  • Environmental Science & Technology, Vol. 41, Issue 6
  • DOI: 10.1021/es0616581

Evidence of horizontal gene transfer between obligate leaf nodule symbionts
journal, March 2016

  • Pinto-Carbó, Marta; Sieber, Simon; Dessein, Steven
  • The ISME Journal, Vol. 10, Issue 9
  • DOI: 10.1038/ismej.2016.27

Genetic basis and importance of metal resistant genes in bacteria for bioremediation of contaminated environments with toxic metal pollutants
journal, February 2016

  • Das, Surajit; Dash, Hirak R.; Chakraborty, Jaya
  • Applied Microbiology and Biotechnology, Vol. 100, Issue 7
  • DOI: 10.1007/s00253-016-7364-4

IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011

  • Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1044

Microbial Community Responses to Organophosphate Substrate Additions in Contaminated Subsurface Sediments
journal, June 2014


Proteome of Geobacter sulfurreducens in the presence of U(VI)
journal, October 2014


Biosorption and Biomineralization of U(VI) by the Marine Bacterium Idiomarina loihiensis MAH1: Effect of Background Electrolyte and pH
journal, March 2014


Interaction of Uranium with Bacterial Cell Surfaces: Inferences from Phosphatase-Mediated Uranium Precipitation
journal, June 2016

  • Kulkarni, Sayali; Misra, Chitra Seetharam; Gupta, Alka
  • Applied and Environmental Microbiology, Vol. 82, Issue 16
  • DOI: 10.1128/AEM.00728-16

Members of the genus Burkholderia: good and bad guys
journal, January 2016


EDGAR: A software framework for the comparative analysis of prokaryotic genomes
journal, May 2009


Aerobic uranium (VI) bioprecipitation by metal-resistant bacteria isolated from radionuclide- and metal-contaminated subsurface soils
journal, December 2007


The RAST Server: Rapid Annotations using Subsystems Technology
journal, January 2008

  • Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A.
  • BMC Genomics, Vol. 9, Issue 1, Article No. 75
  • DOI: 10.1186/1471-2164-9-75

Genomic islands: tools of bacterial horizontal gene transfer and evolution
journal, March 2009


Proteogenomic insights into uranium tolerance of a Chernobyl's Microbacterium bacterial isolate
journal, April 2018