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

Title: Metagenomics-Guided Survey, Isolation, and Characterization of Uranium Resistant Microbiota from the Savannah River Site, USA

Abstract

Despite the recent advancements in culturomics, isolation of the majority of environmental microbiota performing critical ecosystem services, such as bioremediation of contaminants, remains elusive. Towards this end, we conducted a metagenomics-guided comparative assessment of soil microbial diversity and functions present in uraniferous soils relative to those that grew in diffusion chambers (DC) or microbial traps (MT), followed by isolation of uranium (U) resistant microbiota. Shotgun metagenomic analysis performed on the soils used to establish the DC/MT chambers revealed Proteobacterial phyla and Burkholderia genus to be the most abundant among bacteria. The chamber-associated growth conditions further increased their abundances relative to the soils. Ascomycota was the most abundant fungal phylum in the chambers relative to the soils, with Penicillium as the most dominant genus. Metagenomics-based taxonomic findings completely mirrored the taxonomic composition of the retrieved isolates such that the U-resistant bacteria and fungi mainly belonged to Burkholderia and Penicillium species, thus confirming that the chambers facilitated proliferation and subsequent isolation of specific microbiota with environmentally relevant functions. Furthermore, shotgun metagenomic analysis also revealed that the gene classes for carbohydrate metabolism, virulence, and respiration predominated with functions related to stress response, membrane transport, and metabolism of aromatic compounds were also identified, albeitmore » at lower levels. Of major note was the successful isolation of a potentially novel Penicillium species using the MT approach, as evidenced by whole genome sequence analysis and comparative genomic analysis, thus enhancing our overall understanding on the uranium cycling microbiota within the tested uraniferous soils.« less

Authors:
; ; ; ; ; ; ; ; ORCiD logo; ORCiD logo
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1509747
Grant/Contract Number:  
AC09-08SR22470
Resource Type:
Published Article
Journal Name:
Genes
Additional Journal Information:
Journal Name: Genes Journal Volume: 10 Journal Issue: 5; Journal ID: ISSN 2073-4425
Publisher:
MDPI AG
Country of Publication:
Switzerland
Language:
English

Citation Formats

Jaswal,, Pathak,, III,, III,, Seaman,, Stothard,, Krivushin,, Blom,, Rupp,, and Chauhan,. Metagenomics-Guided Survey, Isolation, and Characterization of Uranium Resistant Microbiota from the Savannah River Site, USA. Switzerland: N. p., 2019. Web. doi:10.3390/genes10050325.
Jaswal,, Pathak,, III,, III,, Seaman,, Stothard,, Krivushin,, Blom,, Rupp,, & Chauhan,. Metagenomics-Guided Survey, Isolation, and Characterization of Uranium Resistant Microbiota from the Savannah River Site, USA. Switzerland. doi:10.3390/genes10050325.
Jaswal,, Pathak,, III,, III,, Seaman,, Stothard,, Krivushin,, Blom,, Rupp,, and Chauhan,. Sun . "Metagenomics-Guided Survey, Isolation, and Characterization of Uranium Resistant Microbiota from the Savannah River Site, USA". Switzerland. doi:10.3390/genes10050325.
@article{osti_1509747,
title = {Metagenomics-Guided Survey, Isolation, and Characterization of Uranium Resistant Microbiota from the Savannah River Site, USA},
author = {Jaswal, and Pathak, and III, and III, and Seaman, and Stothard, and Krivushin, and Blom, and Rupp, and Chauhan,},
abstractNote = {Despite the recent advancements in culturomics, isolation of the majority of environmental microbiota performing critical ecosystem services, such as bioremediation of contaminants, remains elusive. Towards this end, we conducted a metagenomics-guided comparative assessment of soil microbial diversity and functions present in uraniferous soils relative to those that grew in diffusion chambers (DC) or microbial traps (MT), followed by isolation of uranium (U) resistant microbiota. Shotgun metagenomic analysis performed on the soils used to establish the DC/MT chambers revealed Proteobacterial phyla and Burkholderia genus to be the most abundant among bacteria. The chamber-associated growth conditions further increased their abundances relative to the soils. Ascomycota was the most abundant fungal phylum in the chambers relative to the soils, with Penicillium as the most dominant genus. Metagenomics-based taxonomic findings completely mirrored the taxonomic composition of the retrieved isolates such that the U-resistant bacteria and fungi mainly belonged to Burkholderia and Penicillium species, thus confirming that the chambers facilitated proliferation and subsequent isolation of specific microbiota with environmentally relevant functions. Furthermore, shotgun metagenomic analysis also revealed that the gene classes for carbohydrate metabolism, virulence, and respiration predominated with functions related to stress response, membrane transport, and metabolism of aromatic compounds were also identified, albeit at lower levels. Of major note was the successful isolation of a potentially novel Penicillium species using the MT approach, as evidenced by whole genome sequence analysis and comparative genomic analysis, thus enhancing our overall understanding on the uranium cycling microbiota within the tested uraniferous soils.},
doi = {10.3390/genes10050325},
journal = {Genes},
number = 5,
volume = 10,
place = {Switzerland},
year = {2019},
month = {4}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.3390/genes10050325

Citation Metrics:
Cited by: 2 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

SUPER-FOCUS: a tool for agile functional analysis of shotgun metagenomic data
journal, October 2015


Metabolically active microbial communities in uranium-contaminated subsurface sediments: Microbial communities in uranium-contaminated sediments
journal, January 2007


MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms
journal, May 2018

  • Kumar, Sudhir; Stecher, Glen; Li, Michael
  • Molecular Biology and Evolution, Vol. 35, Issue 6
  • DOI: 10.1093/molbev/msy096

Metal Toxicity Affects Fungal and Bacterial Activities in Soil Differently
journal, May 2004


Consistent responses of soil microbial taxonomic and functional attributes to mercury pollution across China
journal, October 2018


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


Structure, Function, and Formation of Biological Iron-Sulfur Clusters
journal, June 2005


Microbial Community Changes in Response to Ethanol or Methanol Amendments for U(VI) Reduction
journal, July 2010

  • Vishnivetskaya, T. A.; Brandt, C. C.; Madden, A. S.
  • Applied and Environmental Microbiology, Vol. 76, Issue 17
  • DOI: 10.1128/AEM.00308-10

Effects of Growth Medium, Inoculum Size, and Incubation Time on Culturability and Isolation of Soil Bacteria
journal, February 2005


The impact of human activities and lifestyles on the interlinked microbiota and health of humans and of ecosystems
journal, June 2018


Genome Sequences of Burkholderia sp. Strains CCGE1002 and H160, Isolated from Legume Nodules in Mexico and Brazil
journal, December 2012

  • Ormeno-Orrillo, E.; Rogel, M. A.; Chueire, L. M. O.
  • Journal of Bacteriology, Vol. 194, Issue 24
  • DOI: 10.1128/JB.01756-12

Effect of gelling agent on colony formation in solid cultivation of microbial community in lake sediment
journal, July 2009


Culture-dependent and -independent molecular analysis of the bacterial community within uranium ore
journal, March 2011


Short Peptide Induces an "Uncultivable" Microorganism To Grow In Vitro
journal, May 2008

  • Nichols, D.; Lewis, K.; Orjala, J.
  • Applied and Environmental Microbiology, Vol. 74, Issue 15
  • DOI: 10.1128/AEM.00393-08

A newly discovered role for iron-sulfur clusters
journal, August 2008

  • Dos Santos, P. C.; Dean, D. R.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 33
  • DOI: 10.1073/pnas.0805713105

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


Incubation of Environmental Samples in a Diffusion Chamber Increases the Diversity of Recovered Isolates
journal, August 2007

  • Bollmann, A.; Lewis, K.; Epstein, S. S.
  • Applied and Environmental Microbiology, Vol. 73, Issue 20
  • DOI: 10.1128/AEM.01309-07

Resistance, resilience, and redundancy in microbial communities
journal, August 2008

  • Allison, S. D.; Martiny, J. B. H.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1
  • DOI: 10.1073/pnas.0801925105

Biomineralization of Uranium by PhoY Phosphatase Activity Aids Cell Survival in Caulobacter crescentus
journal, May 2014

  • Yung, Mimi C.; Jiao, Yongqin
  • Applied and Environmental Microbiology, Vol. 80, Issue 16
  • DOI: 10.1128/AEM.01050-14

Diversity and significance of Burkholderia species occupying diverse ecological niches
journal, September 2003


Tapping into microbial diversity
journal, February 2004

  • Keller, Martin; Zengler, Karsten
  • Nature Reviews Microbiology, Vol. 2, Issue 2
  • DOI: 10.1038/nrmicro819

Penicillium arizonense, a new, genome sequenced fungal species, reveals a high chemical diversity in secreted metabolites
journal, October 2016

  • Grijseels, Sietske; Nielsen, Jens Christian; Randelovic, Milica
  • Scientific Reports, Vol. 6, Issue 1
  • DOI: 10.1038/srep35112

A trap for in situ cultivation of filamentous actinobacteria
journal, March 2008

  • Gavrish, Ekaterina; Bollmann, Annette; Epstein, Slava
  • Journal of Microbiological Methods, Vol. 72, Issue 3
  • DOI: 10.1016/j.mimet.2007.12.009

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

Metagenomic analysis of microbial community in uranium-contaminated soil
journal, October 2015


Fast and sensitive protein alignment using DIAMOND
journal, November 2014

  • Buchfink, Benjamin; Xie, Chao; Huson, Daniel H.
  • Nature Methods, Vol. 12, Issue 1
  • DOI: 10.1038/nmeth.3176

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


MEGAN analysis of metagenomic data
journal, February 2007

  • Huson, D. H.; Auch, A. F.; Qi, J.
  • Genome Research, Vol. 17, Issue 3
  • DOI: 10.1101/gr.5969107

Endogenous Stress Caused by Faulty Oxidation Reactions Fosters Evolution of 2,4-Dinitrotoluene-Degrading Bacteria
journal, August 2013


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


Direct analysis of wood-inhabiting fungi using denaturing gradient gel electrophoresis of amplified ribosomal DNA
journal, August 2000


Denitrifying Bacteria from the Genus Rhodanobacter Dominate Bacterial Communities in the Highly Contaminated Subsurface of a Nuclear Legacy Waste Site
journal, December 2011

  • Green, Stefan J.; Prakash, Om; Jasrotia, Puja
  • Applied and Environmental Microbiology, Vol. 78, Issue 4
  • DOI: 10.1128/AEM.06435-11

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


Molecular analysis of bacterial communities in uranium ores and surrounding soils from Banduhurang open cast uranium mine, India: A comparative study
journal, January 2011

  • Islam, Ekramul; Dhal, Paltu K.; Kazy, Sufia K.
  • Journal of Environmental Science and Health, Part A, Vol. 46, Issue 3
  • DOI: 10.1080/10934529.2011.535433

Isolation of Previously Uncultured Slow-Growing Bacteria by Using a Simple Modification in the Preparation of Agar Media
journal, July 2018

  • Kato, Souichiro; Yamagishi, Ayasa; Daimon, Serina
  • Applied and Environmental Microbiology, Vol. 84, Issue 19
  • DOI: 10.1128/AEM.00807-18

Microbial community dynamics in uranium contaminated subsurface sediments under biostimulated conditions with high nitrate and nickel pressure
journal, August 2008

  • Moreels, David; Crosson, Garry; Garafola, Craig
  • Environmental Science and Pollution Research, Vol. 15, Issue 6
  • DOI: 10.1007/s11356-008-0034-z

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

Evidence of Geobacter-associated phage in a uranium-contaminated aquifer
journal, August 2014

  • Holmes, Dawn E.; Giloteaux, Ludovic; Chaurasia, Akhilesh K.
  • The ISME Journal, Vol. 9, Issue 2
  • DOI: 10.1038/ismej.2014.128

Effective Soil Extraction Method for Cultivating Previously Uncultured Soil Bacteria
journal, October 2018

  • Nguyen, Tuan Manh; Seo, Chan; Ji, Moongi
  • Applied and Environmental Microbiology, Vol. 84, Issue 24
  • DOI: 10.1128/AEM.01145-18

Metagenomic analysis of microbial community and function involved in cd-contaminated soil
journal, February 2018


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

Short-Read Assembly of Full-Length 16S Amplicons Reveals Bacterial Diversity in Subsurface Sediments
journal, February 2013


Novel diesel-oil-degrading bacteria and fungi from the Ecuadorian Amazon rainforest
journal, May 2015

  • Maddela, N. R.; Masabanda, M.; Leiva-Mora, M.
  • Water Science and Technology, Vol. 71, Issue 10
  • DOI: 10.2166/wst.2015.142

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


Nonlinear partial differential equations and applications: Cultivating the uncultured
journal, November 2002

  • Zengler, K.; Toledo, G.; Rappe, M.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 24
  • DOI: 10.1073/pnas.252630999

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

Uranium and Fungi
journal, June 2011


Uranium phosphate biomineralization by fungi: Uranium biomineralization by fungi
journal, March 2015

  • Liang, Xinjin; Hillier, Stephen; Pendlowski, Helen
  • Environmental Microbiology, Vol. 17, Issue 6
  • DOI: 10.1111/1462-2920.12771

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


Biodegradation of petroleum hydrocarbons in the presence of nickel and cobalt: Petroleum hydrocarbon biodegradation in heavy metal-rich system
journal, March 2013

  • Oyetibo, Ganiyu Oladunjoye; Ilori, Matthew Olusoji; Obayori, Oluwafemi Sunday
  • Journal of Basic Microbiology, Vol. 53, Issue 11
  • DOI: 10.1002/jobm.201200151

Heavy metal tolerance traits of filamentous fungi isolated from gold and gemstone mining sites
journal, January 2018

  • Oladipo, Oluwatosin Gbemisola; Awotoye, Olusegun Olufemi; Olayinka, Akinyemi
  • Brazilian Journal of Microbiology, Vol. 49, Issue 1
  • DOI: 10.1016/j.bjm.2017.06.003

Printing soil: a single-step, high-throughput method to isolate micro-organisms and near-neighbour microbial consortia from a complex environmental sample
journal, November 2014

  • Ringeisen, Bradley R.; Rincon, Karina; Fitzgerald, Lisa A.
  • Methods in Ecology and Evolution, Vol. 6, Issue 2
  • DOI: 10.1111/2041-210X.12303

Cyclic AMP and Acyl Homoserine Lactones Increase the Cultivation Efficiency of Heterotrophic Bacteria from the Central Baltic Sea
journal, August 2002


Isolation and Physiology of Bacteria from Contaminated Subsurface Sediments
journal, September 2010

  • Bollmann, A.; Palumbo, A. V.; Lewis, K.
  • Applied and Environmental Microbiology, Vol. 76, Issue 22
  • DOI: 10.1128/AEM.00376-10

MicrobiomeAnalyst: a web-based tool for comprehensive statistical, visual and meta-analysis of microbiome data
journal, April 2017

  • Dhariwal, Achal; Chong, Jasmine; Habib, Salam
  • Nucleic Acids Research, Vol. 45, Issue W1
  • DOI: 10.1093/nar/gkx295

Application of Diffusion Growth Chambers for the Cultivation of Marine Sponge-Associated Bacteria
journal, May 2014

  • Steinert, Georg; Whitfield, Susanna; Taylor, Michael W.
  • Marine Biotechnology, Vol. 16, Issue 5
  • DOI: 10.1007/s10126-014-9575-y

Effects of uranium concentration on microbial community structure and functional potential
journal, August 2017

  • Sutcliffe, Brodie; Chariton, Anthony A.; Harford, Andrew J.
  • Environmental Microbiology, Vol. 19, Issue 8
  • DOI: 10.1111/1462-2920.13839

Common Features of Environmental and Potentially Beneficial Plant-Associated Burkholderia
journal, August 2011

  • Suárez-Moreno, Zulma Rocío; Caballero-Mellado, Jesús; Coutinho, Bruna G.
  • Microbial Ecology, Vol. 63, Issue 2
  • DOI: 10.1007/s00248-011-9929-1

Laboratory Cultivation of Widespread and Previously Uncultured Soil Bacteria
journal, December 2003


A large-scale evaluation of algorithms to calculate average nucleotide identity
journal, February 2017


Taxonomic Affiliation of New Genomes Should Be Verified Using Average Nucleotide Identity and Multilocus Phylogenetic Analysis
journal, November 2014


Bioleaching remediation of heavy metal-contaminated soils using Burkholderia sp. Z-90
journal, January 2016


Using native and syntenically mapped cDNA alignments to improve de novo gene finding
journal, January 2008


Assessment of the Resistance to Uranium (VI) Exposure by Arthrobacter sp. Isolated from Hanford Site Soil
journal, January 2013


Global analysis of biosynthetic gene clusters reveals vast potential of secondary metabolite production in Penicillium species
journal, April 2017

  • Nielsen, Jens Christian; Grijseels, Sietske; Prigent, Sylvain
  • Nature Microbiology, Vol. 2, Issue 6
  • DOI: 10.1038/nmicrobiol.2017.44

Microbial Functional Gene Diversity with a Shift of Subsurface Redox Conditions during In Situ Uranium Reduction
journal, February 2012

  • Liang, Yuting; Van Nostrand, Joy D.; N′Guessan, Lucie A.
  • Applied and Environmental Microbiology, Vol. 78, Issue 8
  • DOI: 10.1128/AEM.06528-11

Influence of Uranium on Bacterial Communities: A Comparison of Natural Uranium-Rich Soils with Controls
journal, October 2011


The Uncultured Microbial Majority
journal, October 2003


Comparative metagenomics reveals impact of contaminants on groundwater microbiomes
journal, October 2015