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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. 2016. "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 = {Fri Jun 17 00:00:00 EDT 2016},
month = {Fri Jun 17 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
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Citation Metrics:
Cited by: 42 works
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Figures / Tables:

FIGURE 1 FIGURE 1: Sampling site at Mushroom Spring, Yellowstone National Park, and microbial mat core (adapted from Kim et al., 2015).

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Disentangling the drivers of functional complexity at the metagenomic level in Shark Bay microbial mat microbiomes
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