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Title: Assembly and Succession of Iron Oxide Microbial Mat Communities in Acidic Geothermal Springs

Abstract

Biomineralized ferric oxide microbial mats are ubiquitous features on Earth, are common in hot springs of Yellowstone National Park (YNP, WY, USA), and form due to direct interaction between microbial and physicochemical processes. The overall goal of this study was to determine the contribution of different community members to the assembly and succession of acidic high-temperature Fe(III)-oxide mat ecosystems. Spatial and temporal changes in Fe(III)-oxide accretion and the abundance of relevant community members were monitored over 70 days using sterile glass microscope slides incubated in the outflow channels of two acidic geothermal springs (pH = 3-3.5; temperature = 68-75°C) in YNP. Hydrogenobaculum spp. were the most abundant taxon identified during early successional stages (4-40 days), and have been shown to oxidize arsenite, sulfide, and hydrogen coupled to oxygen reduction. Iron-oxidizing populations of Metallosphaera yellowstonensis were detected within 4 days, and reached steady-state levels within 14-30 days, corresponding to visible Fe(III)-oxide accretion. Heterotrophic archaea colonized near 30 days, and emerged as the dominant functional guild after 70 days and in mature Fe(III)-oxide mats (1-2 cm thick). First-order rate constants of Fe(III)-oxide accretion ranged from 0.046 to 0.05 day -1 , and in situ microelectrode measurements showed that the oxidation of Fe(II)more » is limited by the diffusion of O2 into the Fe(III)-oxide mat. The formation of microterracettes also implicated O2 as a major variable controlling microbial growth and subsequent mat morphology. The assembly and succession of Fe(III)-oxide mat communities follows a repeatable pattern of colonization by lithoautotrophic organisms, and the subsequent growth of diverse organoheterotrophs. The unique geochemical signatures and micromorphology of extant biomineralized Fe(III)-oxide mats are also useful for understanding other Fe(II)-oxidizing systems.« less

Authors:
 [1];  [2];  [3];  [1];  [1];  [4];  [1]
  1. Montana State Univ., Bozeman, MT (United States). Dept. of Land Resources and Environmental Sciences
  2. Montana State Univ., Bozeman, MT (United States). Dept. of Chemical and Biological Engineering; Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Biodetection Science and Biological Science Division
  3. Montana State Univ., Bozeman, MT (United States). Dept. of Land Resources and Environmental Sciences, Dept. of Chemical and Biological Engineering
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1379092
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 7; Journal Issue: FEB; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
58 GEOSCIENCES; hydrogenobaculum; metallosphaera; lithoautotroph; organoheterotroph; archaea; biomineralization; oxygen

Citation Formats

Beam, Jacob P., Bernstein, Hans C., Jay, Zackary J., Kozubal, Mark A., Jennings, Ryan deM., Tringe, Susannah G., and Inskeep, William P. Assembly and Succession of Iron Oxide Microbial Mat Communities in Acidic Geothermal Springs. United States: N. p., 2016. Web. doi:10.3389/fmicb.2016.00025.
Beam, Jacob P., Bernstein, Hans C., Jay, Zackary J., Kozubal, Mark A., Jennings, Ryan deM., Tringe, Susannah G., & Inskeep, William P. Assembly and Succession of Iron Oxide Microbial Mat Communities in Acidic Geothermal Springs. United States. https://doi.org/10.3389/fmicb.2016.00025
Beam, Jacob P., Bernstein, Hans C., Jay, Zackary J., Kozubal, Mark A., Jennings, Ryan deM., Tringe, Susannah G., and Inskeep, William P. 2016. "Assembly and Succession of Iron Oxide Microbial Mat Communities in Acidic Geothermal Springs". United States. https://doi.org/10.3389/fmicb.2016.00025. https://www.osti.gov/servlets/purl/1379092.
@article{osti_1379092,
title = {Assembly and Succession of Iron Oxide Microbial Mat Communities in Acidic Geothermal Springs},
author = {Beam, Jacob P. and Bernstein, Hans C. and Jay, Zackary J. and Kozubal, Mark A. and Jennings, Ryan deM. and Tringe, Susannah G. and Inskeep, William P.},
abstractNote = {Biomineralized ferric oxide microbial mats are ubiquitous features on Earth, are common in hot springs of Yellowstone National Park (YNP, WY, USA), and form due to direct interaction between microbial and physicochemical processes. The overall goal of this study was to determine the contribution of different community members to the assembly and succession of acidic high-temperature Fe(III)-oxide mat ecosystems. Spatial and temporal changes in Fe(III)-oxide accretion and the abundance of relevant community members were monitored over 70 days using sterile glass microscope slides incubated in the outflow channels of two acidic geothermal springs (pH = 3-3.5; temperature = 68-75°C) in YNP. Hydrogenobaculum spp. were the most abundant taxon identified during early successional stages (4-40 days), and have been shown to oxidize arsenite, sulfide, and hydrogen coupled to oxygen reduction. Iron-oxidizing populations of Metallosphaera yellowstonensis were detected within 4 days, and reached steady-state levels within 14-30 days, corresponding to visible Fe(III)-oxide accretion. Heterotrophic archaea colonized near 30 days, and emerged as the dominant functional guild after 70 days and in mature Fe(III)-oxide mats (1-2 cm thick). First-order rate constants of Fe(III)-oxide accretion ranged from 0.046 to 0.05 day -1 , and in situ microelectrode measurements showed that the oxidation of Fe(II) is limited by the diffusion of O2 into the Fe(III)-oxide mat. The formation of microterracettes also implicated O2 as a major variable controlling microbial growth and subsequent mat morphology. The assembly and succession of Fe(III)-oxide mat communities follows a repeatable pattern of colonization by lithoautotrophic organisms, and the subsequent growth of diverse organoheterotrophs. The unique geochemical signatures and micromorphology of extant biomineralized Fe(III)-oxide mats are also useful for understanding other Fe(II)-oxidizing systems.},
doi = {10.3389/fmicb.2016.00025},
url = {https://www.osti.gov/biblio/1379092}, journal = {Frontiers in Microbiology},
issn = {1664-302X},
number = FEB,
volume = 7,
place = {United States},
year = {Mon Feb 15 00:00:00 EST 2016},
month = {Mon Feb 15 00:00:00 EST 2016}
}

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Cited by: 23 works
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Works referenced in this record:

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journal, January 2005


AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature
journal, February 2010


Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park
journal, November 2012


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Niche specialization of novel Thaumarchaeota to oxic and hypoxic acidic geothermal springs of Yellowstone National Park
journal, November 2013


Biomineralization of As(V)-hydrous ferric oxyhydroxide in microbial mats of an acid-sulfate-chloride geothermal spring, Yellowstone National Park
journal, August 2004


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journal, October 1988


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Comparative Genomic Analysis of Phylogenetically Closely Related Hydrogenobaculum sp. Isolates from Yellowstone National Park
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Isolation and Distribution of a Novel Iron-Oxidizing Crenarchaeon from Acidic Geothermal Springs in Yellowstone National Park
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Biogeochemistry and microbiology of microaerobic Fe(II) oxidation
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Microbial biomass: A catalyst for CaCO3 precipitation in advection-dominated transport regimes
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Effects of biofilm structures on oxygen distribution and mass transport
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Accumulation of arsenic from acidic mine waters by ferruginous bacterial accretions (stromatolites)
journal, July 1996


Biomineralization of As(V)-hydrous ferric oxyhydroxide in microbial mats of an acid-sulfate-chloride geothermal spring, Yellowstone National Park
journal, August 2004


Redox-driven regulation of microbial community morphogenesis
journal, April 2014


Sulfur-metabolizing bacterial populations in microbial mats of the Nakabusa hot spring, Japan
journal, June 2011


Rapid Oxidation of Arsenite in a Hot Spring Ecosystem, Yellowstone National Park
journal, August 2001


Relation between Catalytic Activity and Size of Particle
journal, July 1939


Loihi Seamount, Hawaii: a mid-plate volcano with a distinctive hydrothermal system
journal, October 1988


The role of microbes in accretion, lamination and early lithification of modern marine stromatolites
journal, August 2000


AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature
journal, February 2010


Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park
journal, November 2012


Niche specialization of novel Thaumarchaeota to oxic and hypoxic acidic geothermal springs of Yellowstone National Park
journal, November 2013


Jarosite as an indicator of water-limited chemical weathering on Mars
journal, October 2004


Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring
journal, August 2001


Tungsten in biological systems
journal, March 1996


A 3-Hydroxypropionate/4-Hydroxybutyrate Autotrophic Carbon Dioxide Assimilation Pathway in Archaea
journal, December 2007


The Strategy of Ecosystem Development
journal, April 1969


Acidic Mine Drainage: The Rate-Determining Step
journal, February 1970


Relative Importance of H2 and H2S as Energy Sources for Primary Production in Geothermal Springs
journal, July 2008


Autecology of an Arsenite Chemolithotroph: Sulfide Constraints on Function and Distribution in a Geothermal Spring
journal, September 2007


CO2 Uptake and Fixation by a Thermoacidophilic Microbial Community Attached to Precipitated Sulfur in a Geothermal Spring
journal, May 2009


Carbon Dioxide Fixation by Metallosphaera yellowstonensis and Acidothermophilic Iron-Oxidizing Microbial Communities from Yellowstone National Park
journal, February 2014


Investigation of an Iron-Oxidizing Microbial Mat Community Located near Aarhus, Denmark: Field Studies
journal, January 1994


Arsenite-Oxidizing Hydrogenobaculum Strain Isolated from an Acid-Sulfate-Chloride Geothermal Spring in Yellowstone National Park
journal, March 2004


Geochemistry and Dynamics of the Yellowstone National Park Hydrothermal System
journal, May 1989


Geomicrobiological Cycling of Iron
journal, January 2005


Works referencing / citing this record:

Flat pebbles and their edge-wise fabric in relation to 2-D microbial mat
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A review of the mechanisms of mineral-based metabolism in early Earth analog rock-hosted hydrothermal ecosystems
journal, January 2019


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journal, March 2019


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