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

Jaswal,; Pathak,; III,; III,; Seaman,; Stothard,; Krivushin,; Blom,; Rupp,; Chauhan,

doi:10.3390/genes10050325

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 »« less

Authors:

Jaswal,; Pathak,; III,; III,; Seaman,; Stothard,; Krivushin,; Blom,;

;

Publication Date:: Sun Apr 28 00:00:00 EDT 2019

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.

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                    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.  https://doi.org/10.3390/genes10050325

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                    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.  https://doi.org/10.3390/genes10050325.

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@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         = {Sun Apr 28 00:00:00 EDT 2019},

  month        = {Sun Apr 28 00:00:00 EDT 2019}

}

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Background: Currently, much is unknown about the taxonomic diversity and the mechanisms of methane metabolism in the Florida Everglades ecosystem. The Loxahatchee National Wildlife Refuge is a section of the Florida Everglades that is almost entirely unstudied in regard to taxonomic profiling. This short report analyzes the metagenome of soil samples from this Refuge to investigate the predominant taxa, as well as the abundance of genes involved in environmentally significant metabolic pathways related to methane production (nitrogen fixation and dissimilatory sulfite reduction). Methods: Shotgun metagenomic sequencing using the Illumina platform was performed on 17 soil samples from four different sitesmore »« less
Cited by 12
https://doi.org/10.1186/s40793-019-0352-4
Avocado_Bark_Diversity

Dataset Aguirre von Wobeser, Eneas ; Alfonso-Sánchez, Alexandro ; Méndez-Bravo, Alfonso ; ...

Bark is a permanent surface for microbial colonization at the interface of trees and the surrounding air. However, little is known about the microbial communities harbored on these tissues. Studies on bark microbial ecology show a dominance of bacteria from a few phyla. Bark microbial communities of avocado (Persea americana) could have implications for tree health, as a first barrier for defense against certain pests and diseases in this economically important species. We used shotgun metagenomic sequencing to analyze the bark microbial communities of avocado trees from two orchards, and compared one of them to rhizospheric soil. Our results showmore »« less
https://doi.org/10.25982/69195.32/1647032

View Dataset
Microbial Tracking-2, a metagenomics analysis of bacteria and fungi onboard the International Space Station

Journal Article Urbaniak, Camilla ; Morrison, Michael D. ; Thissen, James B. ; ... - Microbiome

The International Space Station (ISS) is a unique and complex built environment with the ISS surface microbiome originating from crew and cargo or from life support recirculation in an almost entirely closed system. The Microbial Tracking 1 (MT-1) project was the first ISS environmental surface study to report on the metagenome profiles without using whole-genome amplification. The study surveyed the microbial communities from eight surfaces over a 14-month period. The Microbial Tracking 2 (MT-2) project aimed to continue the work of MT-1, sampling an additional four flights from the same locations, over another 14 months. Eight surfaces across the ISSmore »« less
https://doi.org/10.1186/s40168-022-01293-0

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

Abstract

Citation Formats

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

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

Proteogenomic Analysis of Burkholderia Species Strains 25 and 46 Isolated from Uraniferous Soils Reveals Multiple Mechanisms to Cope with Uranium Stress journal, December 2018

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

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

Isolating "Uncultivable" Microorganisms in Pure Culture in a Simulated Natural Environment journal, May 2002

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

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

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

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

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

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

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

Tapping into microbial diversity journal, February 2004

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

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

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

Physiological and Comparative Genomic Analysis of Arthrobacter sp. SRS-W-1-2016 Provides Insights on Niche Adaptation for Survival in Uraniferous Soils journal, January 2018

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

Fast and sensitive protein alignment using DIAMOND journal, November 2014

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

MEGAN analysis of metagenomic data journal, February 2007

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

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

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

Genome-centric evaluation of Burkholderia sp. strain SRS-W-2-2016 resistant to high concentrations of uranium and nickel isolated from the Savannah River Site (SRS), USA journal, June 2017

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

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

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

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

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

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

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

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

Uranium and Fungi journal, June 2011

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

Isolation, Characterization, and Metal Response of Novel, Acid-Tolerant Penicillium spp. from Extremely Metal-Rich Waters at a Mining Site in Transbaikal (Siberia, Russia) journal, April 2018

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

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

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

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

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

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

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

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

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

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

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

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

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

Proteogenomic Analysis of Burkholderia Species Strains 25 and 46 Isolated from Uraniferous Soils Reveals Multiple Mechanisms to Cope with Uranium Stress
journal, December 2018

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

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

Isolating "Uncultivable" Microorganisms in Pure Culture in a Simulated Natural Environment
journal, May 2002

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

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

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

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

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

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

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

Tapping into microbial diversity
journal, February 2004

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

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

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

Physiological and Comparative Genomic Analysis of Arthrobacter sp. SRS-W-1-2016 Provides Insights on Niche Adaptation for Survival in Uraniferous Soils
journal, January 2018

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

Fast and sensitive protein alignment using DIAMOND
journal, November 2014

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

MEGAN analysis of metagenomic data
journal, February 2007

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

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

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

Genome-centric evaluation of Burkholderia sp. strain SRS-W-2-2016 resistant to high concentrations of uranium and nickel isolated from the Savannah River Site (SRS), USA
journal, June 2017

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

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

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

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

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

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

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

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

Uranium and Fungi
journal, June 2011

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

Isolation, Characterization, and Metal Response of Novel, Acid-Tolerant Penicillium spp. from Extremely Metal-Rich Waters at a Mining Site in Transbaikal (Siberia, Russia)
journal, April 2018

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

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

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

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

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

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

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

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

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

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

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