Stable isotope labeling confirms mixotrophic nature of streamer biofilm communities at alkaline hot springs

Streamer biofilm communities (SBC) are often observed within chemosynthetic zones of Yellowstone hot spring outflow channels, where temperatures exceed those conducive to photosynthesis. Nearest the hydrothermal source (75–88°C) SBC comprise thermophilic Archaea and Bacteria, often mixed communities...

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Main Authors: Schubotz, Florence, Hays, Lindsay E., Meyer-Dombard, D'Arcy R., Gillespie, Aimee, Shock, Everett L., Summons, Roger E
Other Authors: Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
Format: Article
Language:en_US
Published: Frontiers Research Foundation 2015
Online Access:http://hdl.handle.net/1721.1/96420
https://orcid.org/0000-0002-7144-8537
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author Schubotz, Florence
Hays, Lindsay E.
Meyer-Dombard, D'Arcy R.
Gillespie, Aimee
Shock, Everett L.
Summons, Roger E
author2 Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
author_facet Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences
Schubotz, Florence
Hays, Lindsay E.
Meyer-Dombard, D'Arcy R.
Gillespie, Aimee
Shock, Everett L.
Summons, Roger E
author_sort Schubotz, Florence
collection MIT
description Streamer biofilm communities (SBC) are often observed within chemosynthetic zones of Yellowstone hot spring outflow channels, where temperatures exceed those conducive to photosynthesis. Nearest the hydrothermal source (75–88°C) SBC comprise thermophilic Archaea and Bacteria, often mixed communities including Desulfurococcales and uncultured Crenarchaeota, as well as Aquificae and Thermus, each carrying diagnostic membrane lipid biomarkers. We tested the hypothesis that SBC can alternate their metabolism between autotrophy and heterotrophy depending on substrate availability. Feeding experiments were performed at two alkaline hot springs in Yellowstone National Park: Octopus Spring and “Bison Pool,” using various [superscript 13]C-labeled substrates (bicarbonate, formate, acetate, and glucose) to determine the relative uptake of these different carbon sources. Highest [superscript 13]C uptake, at both sites, was from acetate into almost all bacterial fatty acids, particularly into methyl-branched C[subscript 15], C[subscript 17] and C[subscript 19] fatty acids that are diagnostic for Thermus/Meiothermus, and some Firmicutes as well as into universally common C[subscript 16:0] and C[subscript 18:0] fatty acids. [superscript 13]C-glucose showed a similar, but a 10–30 times lower uptake across most fatty acids. [superscript 13]C-bicarbonate uptake, signifying the presence of autotrophic communities was only significant at “Bison Pool” and was observed predominantly in non-specific saturated C[subscript 16], C[subscript 18], C[subscript 20], and C[subscript 22] fatty acids. Incorporation of [superscript 13]C-formate occurred only at very low rates at “Bison Pool” and was almost undetectable at Octopus Spring, suggesting that formate is not an important carbon source for SBC. [superscript 13]C-uptake into archaeal lipids occurred predominantly with [superscript 13]C-acetate, suggesting also that archaeal communities at both springs have primarily heterotrophic carbon assimilation pathways. We hypothesize that these communities are energy-limited and predominantly nurtured by input of exogenous organic material, with only a small fraction being sustained by autotrophic growth.
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spelling mit-1721.1/964202024-05-15T03:23:04Z Stable isotope labeling confirms mixotrophic nature of streamer biofilm communities at alkaline hot springs Schubotz, Florence Hays, Lindsay E. Meyer-Dombard, D'Arcy R. Gillespie, Aimee Shock, Everett L. Summons, Roger E Massachusetts Institute of Technology. Department of Earth, Atmospheric, and Planetary Sciences Summons, Roger Everett Schubotz, Florence Hays, Lindsay E. Meyer-Dombard, D'Arcy R. Gillespie, Aimee Streamer biofilm communities (SBC) are often observed within chemosynthetic zones of Yellowstone hot spring outflow channels, where temperatures exceed those conducive to photosynthesis. Nearest the hydrothermal source (75–88°C) SBC comprise thermophilic Archaea and Bacteria, often mixed communities including Desulfurococcales and uncultured Crenarchaeota, as well as Aquificae and Thermus, each carrying diagnostic membrane lipid biomarkers. We tested the hypothesis that SBC can alternate their metabolism between autotrophy and heterotrophy depending on substrate availability. Feeding experiments were performed at two alkaline hot springs in Yellowstone National Park: Octopus Spring and “Bison Pool,” using various [superscript 13]C-labeled substrates (bicarbonate, formate, acetate, and glucose) to determine the relative uptake of these different carbon sources. Highest [superscript 13]C uptake, at both sites, was from acetate into almost all bacterial fatty acids, particularly into methyl-branched C[subscript 15], C[subscript 17] and C[subscript 19] fatty acids that are diagnostic for Thermus/Meiothermus, and some Firmicutes as well as into universally common C[subscript 16:0] and C[subscript 18:0] fatty acids. [superscript 13]C-glucose showed a similar, but a 10–30 times lower uptake across most fatty acids. [superscript 13]C-bicarbonate uptake, signifying the presence of autotrophic communities was only significant at “Bison Pool” and was observed predominantly in non-specific saturated C[subscript 16], C[subscript 18], C[subscript 20], and C[subscript 22] fatty acids. Incorporation of [superscript 13]C-formate occurred only at very low rates at “Bison Pool” and was almost undetectable at Octopus Spring, suggesting that formate is not an important carbon source for SBC. [superscript 13]C-uptake into archaeal lipids occurred predominantly with [superscript 13]C-acetate, suggesting also that archaeal communities at both springs have primarily heterotrophic carbon assimilation pathways. We hypothesize that these communities are energy-limited and predominantly nurtured by input of exogenous organic material, with only a small fraction being sustained by autotrophic growth. Alexander von Humboldt-Stiftung (Feodor Lynen Fellowship) United States. National Aeronautics and Space Administration. Astrobiology Institute National Science Foundation (U.S.) (Biogeosciences Program Award 0525453) 2015-04-07T19:33:44Z 2015-04-07T19:33:44Z 2015-02 2014-08 Article http://purl.org/eprint/type/JournalArticle 1664-302X http://hdl.handle.net/1721.1/96420 Schubotz, Florence, Lindsay E. Hays, D’Arcy R. Meyer-Dombard, Aimee Gillespie, Everett L. Shock, and Roger E. Summons. “Stable Isotope Labeling Confirms Mixotrophic Nature of Streamer Biofilm Communities at Alkaline Hot Springs.” Frontiers in Microbiology 6 (February 5, 2015). https://orcid.org/0000-0002-7144-8537 en_US http://dx.doi.org/10.3389/fmicb.2015.00042 Frontiers in Microbiology Creative Commons Attribution http://creativecommons.org/licenses/by/4.0/ application/pdf Frontiers Research Foundation Frontiers Research Foundation
spellingShingle Schubotz, Florence
Hays, Lindsay E.
Meyer-Dombard, D'Arcy R.
Gillespie, Aimee
Shock, Everett L.
Summons, Roger E
Stable isotope labeling confirms mixotrophic nature of streamer biofilm communities at alkaline hot springs
title Stable isotope labeling confirms mixotrophic nature of streamer biofilm communities at alkaline hot springs
title_full Stable isotope labeling confirms mixotrophic nature of streamer biofilm communities at alkaline hot springs
title_fullStr Stable isotope labeling confirms mixotrophic nature of streamer biofilm communities at alkaline hot springs
title_full_unstemmed Stable isotope labeling confirms mixotrophic nature of streamer biofilm communities at alkaline hot springs
title_short Stable isotope labeling confirms mixotrophic nature of streamer biofilm communities at alkaline hot springs
title_sort stable isotope labeling confirms mixotrophic nature of streamer biofilm communities at alkaline hot springs
url http://hdl.handle.net/1721.1/96420
https://orcid.org/0000-0002-7144-8537
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