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Title: Use of carbon monoxide and hydrogen by a bacteria-animal symbiosis from seagrass sediments

Abstract

The gutless marine worm Olavius algarvensis lives in symbiosis with chemosynthetic bacteria that provide nutrition by fixing carbon dioxide (CO2) into biomass using reduced sulfur compounds as energy sources. A recent metaproteomic analysis of the O. algarvensis symbiosis indicated that carbon monoxide (CO) and hydrogen (H2) might also be used as energy sources. We provide direct evidence that the O. algarvensis symbiosis consumes CO and H2. Single cell imaging using nanoscale secondary ion mass spectrometry revealed that one of the symbionts, the γ3-symbiont, uses the energy from CO oxidation to fix CO2. Pore water analysis revealed considerable in-situ concentrations of CO and H2 in the O. algarvensis environment, Mediterranean seagrass sediments. Pore water H2 concentrations (89-2147 nM) were up to two orders of magnitude higher than in seawater, and up to 36-fold higher than previously known from shallow-water marine sediments. Pore water CO concentrations (17-51 nM) were twice as high as in the overlying seawater (no literature data from other shallow-water sediments are available for comparison). Ex-situ incubation experiments showed that dead seagrass rhizomes produced large amounts of CO. Lastly, CO production from decaying plant material could thus be a significant energy source for microbial primary production in seagrass sediments.

Authors:
 [1];  [2];  [3];  [3];  [3];  [4];  [3];  [3];  [3]
  1. Max Planck Institute for Marine Microbiology, Bremen (Germany); Univ. of Calgary, Calgary, AB (Canada)
  2. Max Planck Institute for Marine Microbiology, Bremen (Germany); Univ. of Vienna, Vienna (Austria)
  3. Max Planck Institute for Marine Microbiology, Bremen (Germany)
  4. Max Planck Institute for Marine Microbiology, Bremen (Germany); HYDRA Institute for Marine Sciences, Campo nell'Elba (Italy)
Publication Date:
Research Org.:
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Gordon and Betty Moore Foundation; Studienstiftung des deutschen Volkes
OSTI Identifier:
1344909
Grant/Contract Number:  
AC02-05CH11231; GBMF3811
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 17; Journal Issue: 12; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES

Citation Formats

Kleiner, Manuel, Wentrup, Cecilia, Holler, Thomas, Lavik, Gaute, Harder, Jens, Lott, Christian, Littmann, Sten, Kuypers, Marcel M. M., and Dubilier, Nicole. Use of carbon monoxide and hydrogen by a bacteria-animal symbiosis from seagrass sediments. United States: N. p., 2015. Web. doi:10.1111/1462-2920.12912.
Kleiner, Manuel, Wentrup, Cecilia, Holler, Thomas, Lavik, Gaute, Harder, Jens, Lott, Christian, Littmann, Sten, Kuypers, Marcel M. M., & Dubilier, Nicole. Use of carbon monoxide and hydrogen by a bacteria-animal symbiosis from seagrass sediments. United States. doi:10.1111/1462-2920.12912.
Kleiner, Manuel, Wentrup, Cecilia, Holler, Thomas, Lavik, Gaute, Harder, Jens, Lott, Christian, Littmann, Sten, Kuypers, Marcel M. M., and Dubilier, Nicole. Wed . "Use of carbon monoxide and hydrogen by a bacteria-animal symbiosis from seagrass sediments". United States. doi:10.1111/1462-2920.12912. https://www.osti.gov/servlets/purl/1344909.
@article{osti_1344909,
title = {Use of carbon monoxide and hydrogen by a bacteria-animal symbiosis from seagrass sediments},
author = {Kleiner, Manuel and Wentrup, Cecilia and Holler, Thomas and Lavik, Gaute and Harder, Jens and Lott, Christian and Littmann, Sten and Kuypers, Marcel M. M. and Dubilier, Nicole},
abstractNote = {The gutless marine worm Olavius algarvensis lives in symbiosis with chemosynthetic bacteria that provide nutrition by fixing carbon dioxide (CO2) into biomass using reduced sulfur compounds as energy sources. A recent metaproteomic analysis of the O. algarvensis symbiosis indicated that carbon monoxide (CO) and hydrogen (H2) might also be used as energy sources. We provide direct evidence that the O. algarvensis symbiosis consumes CO and H2. Single cell imaging using nanoscale secondary ion mass spectrometry revealed that one of the symbionts, the γ3-symbiont, uses the energy from CO oxidation to fix CO2. Pore water analysis revealed considerable in-situ concentrations of CO and H2 in the O. algarvensis environment, Mediterranean seagrass sediments. Pore water H2 concentrations (89-2147 nM) were up to two orders of magnitude higher than in seawater, and up to 36-fold higher than previously known from shallow-water marine sediments. Pore water CO concentrations (17-51 nM) were twice as high as in the overlying seawater (no literature data from other shallow-water sediments are available for comparison). Ex-situ incubation experiments showed that dead seagrass rhizomes produced large amounts of CO. Lastly, CO production from decaying plant material could thus be a significant energy source for microbial primary production in seagrass sediments.},
doi = {10.1111/1462-2920.12912},
journal = {Environmental Microbiology},
number = 12,
volume = 17,
place = {United States},
year = {2015},
month = {5}
}

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    Works referencing / citing this record:

    Transcriptomic and proteomic insights into innate immunity and adaptations to a symbiotic lifestyle in the gutless marine worm Olavius algarvensis
    journal, November 2016