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

Title: The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. I. Microbial Diversity Based on 16S rRNA Gene Amplicons and Metagenomic Sequencing

Abstract

Microbial-mat communities in the effluent channels of Octopus and Mushroom Springs within the Lower Geyser Basin at Yellowstone National Park have been studied for nearly 50 years. The emphasis has mostly focused on the chlorophototrophic bacterial organisms of the phyla Cyanobacteria and Chloroflexi. In contrast, the diversity and metabolic functions of the heterotrophic community in the microoxic/anoxic region of the mat are not well understood. In this study we analyzed the orange-colored undermat of the microbial community of Mushroom Spring using metagenomic and rRNA-amplicon (iTag) analyses. Our analyses disclosed a highly diverse community exhibiting a high degree of unevenness, strongly dominated by a single taxon, the filamentous anoxygenic phototroph, Roseiflexus spp. The second most abundant organisms belonged to the Thermotogae, which have been hypothesized to be a major source of H-2 from fermentation that could enable photomixotrophic metabolism by Chloroflexus and Roseiflexus spp. Other abundant organisms include two members of the Armatimonadetes (OP10); Thermocrinis sp.; and phototrophic and heterotrophic members of the Chloroflexi. Further, an Atribacteria (OP9/JS1) member; a sulfate-reducing Therrnodesulfovibrio sp.; a Planctomycetes member; a member of the EM3 group tentatively affiliated with the Thermotogae, as well as a putative member of the Arrninicenantes (OP8) represented ≥ 1% ofmore » the reads. Archaea were not abundant in the iTag analysis, and no metagenomic bin representing an archaeon was identified. A high microdiversity of 16S rRNA gene sequences was identified for the dominant taxon, Roseiflexus spp. Previous studies demonstrated that highly similar Synechococcus variants in the upper layer of the mats represent ecological species populations with specific ecological adaptations. In conclusion, this study suggests that similar putative ecotypes specifically adapted to different niches occur within the undermat community, particularly for Roseiflexus spp.« less

Authors:
 [1];  [2];  [2];  [1];  [3];  [2];  [4]
  1. Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology
  2. Montana State Univ., Bozeman, MT (United States). Dept. of Land Resources and Environmental Sciences
  3. Montana State Univ., Bozeman, MT (United States). Dept. of Land Resources and Environmental Sciences; Univ. of Minnesota, Saint Paul, MN (United States). Agricultural Research Service, United States Dept. of Agriculture
  4. Pennsylvania State Univ., University Park, PA (United States). Dept. of Biochemistry and Molecular Biology; Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry
Publication Date:
Research Org.:
Pennsylvania State Univ., University Park, PA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1286006
Grant/Contract Number:  
FG02-94ER20137; AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; hot spring; microbial community; microbial diversity; extreme environments; phototrophic bacteria; yellowstone-national-park; candidatus chloracidobacterium thermophilum; gradient gel-electrophoresis; operational taxonomic units; algal-bacterial mats; alkaline hot-springs; cyanobacterial mat; sp-nov.; synechococcus populations; molecular signatures

Citation Formats

Thiel, Vera, Wood, Jason M., Olsen, Millie T., Tank, Marcus, Klatt, Christian G., Ward, David M., and Bryant, Donald A. The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. I. Microbial Diversity Based on 16S rRNA Gene Amplicons and Metagenomic Sequencing. United States: N. p., 2016. Web. doi:10.3389/fmicb.2016.00919.
Thiel, Vera, Wood, Jason M., Olsen, Millie T., Tank, Marcus, Klatt, Christian G., Ward, David M., & Bryant, Donald A. The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. I. Microbial Diversity Based on 16S rRNA Gene Amplicons and Metagenomic Sequencing. United States. https://doi.org/10.3389/fmicb.2016.00919
Thiel, Vera, Wood, Jason M., Olsen, Millie T., Tank, Marcus, Klatt, Christian G., Ward, David M., and Bryant, Donald A. Fri . "The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. I. Microbial Diversity Based on 16S rRNA Gene Amplicons and Metagenomic Sequencing". United States. https://doi.org/10.3389/fmicb.2016.00919. https://www.osti.gov/servlets/purl/1286006.
@article{osti_1286006,
title = {The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. I. Microbial Diversity Based on 16S rRNA Gene Amplicons and Metagenomic Sequencing},
author = {Thiel, Vera and Wood, Jason M. and Olsen, Millie T. and Tank, Marcus and Klatt, Christian G. and Ward, David M. and Bryant, Donald A.},
abstractNote = {Microbial-mat communities in the effluent channels of Octopus and Mushroom Springs within the Lower Geyser Basin at Yellowstone National Park have been studied for nearly 50 years. The emphasis has mostly focused on the chlorophototrophic bacterial organisms of the phyla Cyanobacteria and Chloroflexi. In contrast, the diversity and metabolic functions of the heterotrophic community in the microoxic/anoxic region of the mat are not well understood. In this study we analyzed the orange-colored undermat of the microbial community of Mushroom Spring using metagenomic and rRNA-amplicon (iTag) analyses. Our analyses disclosed a highly diverse community exhibiting a high degree of unevenness, strongly dominated by a single taxon, the filamentous anoxygenic phototroph, Roseiflexus spp. The second most abundant organisms belonged to the Thermotogae, which have been hypothesized to be a major source of H-2 from fermentation that could enable photomixotrophic metabolism by Chloroflexus and Roseiflexus spp. Other abundant organisms include two members of the Armatimonadetes (OP10); Thermocrinis sp.; and phototrophic and heterotrophic members of the Chloroflexi. Further, an Atribacteria (OP9/JS1) member; a sulfate-reducing Therrnodesulfovibrio sp.; a Planctomycetes member; a member of the EM3 group tentatively affiliated with the Thermotogae, as well as a putative member of the Arrninicenantes (OP8) represented ≥ 1% of the reads. Archaea were not abundant in the iTag analysis, and no metagenomic bin representing an archaeon was identified. A high microdiversity of 16S rRNA gene sequences was identified for the dominant taxon, Roseiflexus spp. Previous studies demonstrated that highly similar Synechococcus variants in the upper layer of the mats represent ecological species populations with specific ecological adaptations. In conclusion, this study suggests that similar putative ecotypes specifically adapted to different niches occur within the undermat community, particularly for Roseiflexus spp.},
doi = {10.3389/fmicb.2016.00919},
url = {https://www.osti.gov/biblio/1286006}, journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = ,
volume = 7,
place = {United States},
year = {2016},
month = {6}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 8 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Community Structure and Function of High-Temperature Chlorophototrophic Microbial Mats Inhabiting Diverse Geothermal Environments
journal, January 2013


IMG/M 4 version of the integrated metagenome comparative analysis system
journal, October 2013


Chloracidobacterium thermophilum gen. nov., sp. nov.: an anoxygenic microaerophilic chlorophotoheterotrophic acidobacterium
journal, February 2015


Genome Sequence of the Sulfate-Reducing Thermophilic Bacterium Thermodesulfovibrio yellowstonii Strain DSM 11347 T (Phylum Nitrospirae )
journal, January 2015


Molecular Characterization of Novel Red Green Nonsulfur Bacteria from Five Distinct Hot Spring Communities in Yellowstone National Park
journal, January 2002


Thermomicrobium, a New Genus of Extremely Thermophilic Bacteria
journal, January 1973


Phylogenetic Delineation of the Novel Phylum Armatimonadetes (Former Candidate Division OP10) and Definition of Two Novel Candidate Divisions
journal, February 2013


Community-wide analysis of microbial genome sequence signatures
journal, January 2009


Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007


Candidatus Chloracidobacterium thermophilum: An Aerobic Phototrophic Acidobacterium
journal, July 2007


AmphoraNet: The webserver implementation of the AMPHORA2 metagenomic workflow suite
journal, January 2014


Regulation of nif gene expression and the energetics of N2 fixation over the diel cycle in a hot spring microbial mat
journal, March 2008


Thermotoga hypogea sp. nov., a Xylanolytic, Thermophilic Bacterium from an Oil-Producing Well
journal, October 1997


In situ dynamics of O2, pH and cyanobacterial transcripts associated with CCM, photosynthesis and detoxification of ROS
journal, August 2010


Armatimonas rosea gen. nov., sp. nov., of a novel bacterial phylum, Armatimonadetes phyl. nov., formally called the candidate phylum OP10
journal, July 2010


Surprisingly extensive mixed phylogenetic and ecological signals among bacterial Operational Taxonomic Units
journal, April 2013


A natural species concept for prokaryotes
journal, June 1998


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


Elioraea tepidiphila gen. nov., sp. nov., a slightly thermophilic member of the Alphaproteobacteria
journal, April 2008


ARB: a software environment for sequence data
journal, February 2004


Population level functional diversity in a microbial community revealed by comparative genomic and metagenomic analyses
journal, October 2007


Micro-organisms adapted to High Temperatures
journal, May 1967


Characterization of novel bacteriochlorophyll- a -containing red filaments from alkaline hot springs in Yellowstone National Park
journal, August 2000


Draft Genome Sequence of the Deinococcus-Thermus Bacterium Meiothermus ruber Strain A
journal, March 2015


Community ecology of hot spring cyanobacterial mats: predominant populations and their functional potential
journal, June 2011


Basic local alignment search tool
journal, October 1990


High Rates of Sulfate Reduction in a Low-Sulfate Hot Spring Microbial Mat Are Driven by a Low Level of Diversity of Sulfate-Respiring Microorganisms
journal, June 2007


Identification of the Bacteriochlorophylls, Carotenoids, Quinones, Lipids, and Hopanoids of "Candidatus Chloracidobacterium thermophilum"
journal, December 2011


Bacterial community composition in thermophilic microbial mats from five hot springs in central Tibet
journal, November 2008


The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST)
journal, November 2013


Ecological studies of Chloroflexis, a gliding photosynthetic bacterium
journal, January 1973


Microbial methane production in deep aquifer associated with the accretionary prism in Southwest Japan
journal, December 2009


Compound-Specific Isotopic Fractionation Patterns Suggest Different Carbon Metabolisms among Chloroflexus-Like Bacteria in Hot-Spring Microbial Mats
journal, October 2003


Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group
journal, December 2010


Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol
journal, March 2008


Taxonomic Note: A Place for DNA-DNA Reassociation and 16S rRNA Sequence Analysis in the Present Species Definition in Bacteriology
journal, October 1994


PyNAST: a flexible tool for aligning sequences to a template alignment
journal, November 2009


A Systematics for Discovering the Fundamental Units of Bacterial Diversity
journal, May 2007


Novel Bacterial and Archaeal Lineages from an In Situ Growth Chamber Deployed at a Mid-Atlantic Ridge Hydrothermal Vent
journal, September 2000


Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics
journal, June 2015


Prokaryotic photosynthesis and phototrophy illuminated
journal, November 2006


Mapping the Tree of Life: Progress and Prospects
journal, November 2009


Global Patterns of Abundance, Diversity and Community Structure of the Aminicenantes (Candidate Phylum OP8)
journal, March 2014


Microbial Ecology and Evolution: A Ribosomal RNA Approach
journal, October 1986


Fine-Scale Distribution Patterns of Synechococcus Ecological Diversity in Microbial Mats of Mushroom Spring, Yellowstone National Park
journal, September 2011


The Ribosomal Database Project: improved alignments and new tools for rRNA analysis
journal, January 2009


Roseomonas aestuarii sp. nov., a bacteriochlorophyll-a containing alphaproteobacterium isolated from an estuarine habitat of India
journal, June 2010


Single-cell and metagenomic analyses indicate a fermentative and saccharolytic lifestyle for members of the OP9 lineage
journal, May 2013


Complete Genome Sequence of the Aerobic CO-Oxidizing Thermophile Thermomicrobium roseum
journal, January 2009


T-cell recognition of an immuno-dominant myelin basic protein epitope in multiple sclerosis
journal, July 1990


Temporal metatranscriptomic patterning in phototrophic Chloroflexi inhabiting a microbial mat in a geothermal spring
journal, April 2013


Metatranscriptomic analyses of chlorophototrophs of a hot-spring microbial mat
journal, June 2011


Diel Variations in Carbon Metabolism by Green Nonsulfur-Like Bacteria in Alkaline Siliceous Hot Spring Microbial Mats from Yellowstone National Park
journal, July 2005


Influence of Molecular Resolution on Sequence-Based Discovery of Ecological Diversity among Synechococcus Populations in an Alkaline Siliceous Hot Spring Microbial Mat
journal, December 2010


Thermogutta terrifontis gen. nov., sp. nov. and Thermogutta hypogea sp. nov., thermophilic anaerobic representatives of the phylum Planctomycetes
journal, December 2014

  • Slobodkina, G. B.; Kovaleva, O. L.; Miroshnichenko, M. L.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 65, Issue Pt 3
  • https://doi.org/10.1099/ijs.0.000009

Fractal dimension of vegetation and the distribution of arthropod body lengths
journal, April 1985


Phylogenetic identification and in situ detection of individual microbial cells without cultivation.
journal, January 1995


Formation and Fate of Fermentation Products in Hot Spring Cyanobacterial Mats
journal, January 1987


Photoexcretion and Fate of Glycolate in a Hot Spring Cyanobacterial Mat
journal, January 1988


Thermus aquaticus gen. n. and sp. n., a Nonsporulating Extreme Thermophile
journal, January 1969


Thermocrinis ruber gen. nov., sp. nov., a Pink-Filament-Forming Hyperthermophilic Bacterium Isolated from Yellowstone National Park
journal, October 1998


Impact of Culture-Independent Studies on the Emerging Phylogenetic View of Bacterial Diversity
journal, September 1998


Novel Division Level Bacterial Diversity in a Yellowstone Hot Spring
journal, January 1998


Photosynthate partitioning and fermentation in hot spring microbial mat communities.
journal, January 1996


Phylogenetic analysis of the hyperthermophilic pink filament community in Octopus Spring, Yellowstone National Park.
journal, January 1994


A Natural View of Microbial Biodiversity within Hot Spring Cyanobacterial Mat Communities
journal, December 1998


    Works referencing / citing this record:

    Disentangling the drivers of functional complexity at the metagenomic level in Shark Bay microbial mat microbiomes
    journal, July 2018


    Life in Hot Spring Microbial Mats Located in the Trans-Mexican Volcanic Belt: A 16S/18S rRNA Gene and Metagenomic Analysis
    journal, April 2018


    Disentangling the drivers of functional complexity at the metagenomic level in Shark Bay microbial mat microbiomes
    journal, July 2018


    How nature designs light-harvesting antenna systems: design principles and functional realization in chlorophototrophic prokaryotes
    journal, January 2018


    Effects of Physiochemical Factors on Prokaryotic Biodiversity in Malaysian Circumneutral Hot Springs
    journal, July 2017


    A metagenomic window into the 2-km-deep terrestrial subsurface aquifer revealed multiple pathways of organic matter decomposition
    journal, August 2018