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Title: The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. II. Metabolic Functions of Abundant Community Members Predicted from Metagenomic Analyses

Microbial mat communities in the effluent channels of Octopus and Mushroom Springs within the Lower Geyser Basin of Yellowstone National Park have been extensively characterized. Previous studies have focused on the chlorophototrophic organisms of the phyla Cyanobacteria and Chloroflexi. However, the diversity and metabolic functions of the other portion of the community in the microoxic/anoxic region of the mat are poorly understood. We recently described the diverse but extremely uneven microbial assemblage in the undermat of Mushroom Spring based on 16S rRNA amplicon sequences, which was dominated by Roseiflexus members, filamentous anoxygenic chlorophototrophs. In this study, we analyzed the orange-colored undermat portion of the community of Mushroom Spring mats in a genome-centric approach and discuss the metabolic potentials of the major members. Metagenome binning recovered partial genomes of all abundant community members, ranging in completeness from ~28 to 96%, and allowed affiliation of function with taxonomic identity even for representatives of novel and Candidate phyla. Less complete metagenomic bins correlated with high microdiversity. The undermat portion of the community was found to be a mixture of phototrophic and chemotrophic organisms, which use bicarbonate as well as organic carbon sources derived from different cell components and fermentation products. The presence ofmore » rhodopsin genes in many taxa strengthens the hypothesis that light energy is of major importance. Evidence for the usage of all four bacterial carbon fixation pathways was found in the metagenome. Nitrogen fixation appears to be limited to Synechococcus spp. in the upper mat layer and Thermodesulfovibrio sp. in the undermat, and nitrate/nitrite metabolism was limited. A closed sulfur cycle is indicated by biological sulfate reduction combined with the presence of genes for sulfide oxidation mainly in phototrophs. Finally, a variety of undermat microorganisms have genes for hydrogen production and consumption, which leads to the observed diel hydrogen concentration patterns.« less
Authors:
 [1] ;  [2] ;  [3] ;  [4]
  1. Pennsylvania State Univ., University Park, PA (United States). Dept of Biochemistry and Molecular Biology
  2. DVGW-Technologiezentrum Wasser, Karlsruhe (Germany). Dept. of Microbiology and Molecular Biology
  3. Montana State Univ., Bozeman, MT (United States). Dept. of Land Resources and Environmental Sciences
  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:
Grant/Contract Number:
FG02-94ER20137; AC02-05CH11231
Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Research Org:
Pennsylvania State Univ., University Park, PA (United States); THE REGENTS OF THE UNIVERSITY OF CALIFORNIA
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; hot spring; microbial community; microbial diversity; extreme environments; chlorophototrophic bacteria; metagenomics
OSTI Identifier:
1424228

Thiel, Vera, Hügler, Michael, Ward, David M., and Bryant, Donald A.. The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. II. Metabolic Functions of Abundant Community Members Predicted from Metagenomic Analyses. United States: N. p., Web. doi:10.3389/fmicb.2017.00943.
Thiel, Vera, Hügler, Michael, Ward, David M., & Bryant, Donald A.. The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. II. Metabolic Functions of Abundant Community Members Predicted from Metagenomic Analyses. United States. doi:10.3389/fmicb.2017.00943.
Thiel, Vera, Hügler, Michael, Ward, David M., and Bryant, Donald A.. 2017. "The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. II. Metabolic Functions of Abundant Community Members Predicted from Metagenomic Analyses". United States. doi:10.3389/fmicb.2017.00943. https://www.osti.gov/servlets/purl/1424228.
@article{osti_1424228,
title = {The Dark Side of the Mushroom Spring Microbial Mat: Life in the Shadow of Chlorophototrophs. II. Metabolic Functions of Abundant Community Members Predicted from Metagenomic Analyses},
author = {Thiel, Vera and Hügler, Michael 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 of Yellowstone National Park have been extensively characterized. Previous studies have focused on the chlorophototrophic organisms of the phyla Cyanobacteria and Chloroflexi. However, the diversity and metabolic functions of the other portion of the community in the microoxic/anoxic region of the mat are poorly understood. We recently described the diverse but extremely uneven microbial assemblage in the undermat of Mushroom Spring based on 16S rRNA amplicon sequences, which was dominated by Roseiflexus members, filamentous anoxygenic chlorophototrophs. In this study, we analyzed the orange-colored undermat portion of the community of Mushroom Spring mats in a genome-centric approach and discuss the metabolic potentials of the major members. Metagenome binning recovered partial genomes of all abundant community members, ranging in completeness from ~28 to 96%, and allowed affiliation of function with taxonomic identity even for representatives of novel and Candidate phyla. Less complete metagenomic bins correlated with high microdiversity. The undermat portion of the community was found to be a mixture of phototrophic and chemotrophic organisms, which use bicarbonate as well as organic carbon sources derived from different cell components and fermentation products. The presence of rhodopsin genes in many taxa strengthens the hypothesis that light energy is of major importance. Evidence for the usage of all four bacterial carbon fixation pathways was found in the metagenome. Nitrogen fixation appears to be limited to Synechococcus spp. in the upper mat layer and Thermodesulfovibrio sp. in the undermat, and nitrate/nitrite metabolism was limited. A closed sulfur cycle is indicated by biological sulfate reduction combined with the presence of genes for sulfide oxidation mainly in phototrophs. Finally, a variety of undermat microorganisms have genes for hydrogen production and consumption, which leads to the observed diel hydrogen concentration patterns.},
doi = {10.3389/fmicb.2017.00943},
journal = {Frontiers in Microbiology},
number = ,
volume = 8,
place = {United States},
year = {2017},
month = {6}
}

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