DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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. https://doi.org/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. https://doi.org/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 = {Wed May 27 00:00:00 EDT 2015},
month = {Wed May 27 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 25 works
Citation information provided by
Web of Science

Figures / Tables:

Fig. 1 Fig. 1: Olavius algarvensis and the Mediterranean seagrass sediments it inhabits. A. The O. algarvensis environment is characterized by medium- to coarse-grained silicate sediments and patches of the seagrass Posidonia oceanica. Subsurface roots and rhizomes (horizontal stems) stabilize the plants in the sediment. The roots and rhizomes form dense matsmore » that are very stable, even after the seagrass has died, and can remain in the sediment for millennia (Mateo et al., 1997; Alcoverro et al., 2001; Duarte, 2002; Boudouresque et al., 2009; Gutiérrez et al., 2011). At the collection site for this study (Sant’ Andrea in the north of the Island of Elba), reef-like mats of dead rhizomes are buried underneath the sediment in the entire bay. The sediment overlying the rhizome mats is very poor in nutrients and energy sources (Kleiner et al., 2012b). B. Image of the O. algarvensis collection site showing sandy sediments surrounded by seagrass beds in 5–6 m water depth. C. Dead seagrass rhizomes from the O. algarvensis collection site. D. Olavius algarvensis, scale bar = 0.4 mm.« less

Save / Share:

Works referenced in this record:

Resourceful heterotrophs make the most of light in the coastal ocean
journal, October 2007

  • Moran, Mary Ann; Miller, William L.
  • Nature Reviews Microbiology, Vol. 5, Issue 10
  • DOI: 10.1038/nrmicro1746

Look@NanoSIMS - a tool for the analysis of nanoSIMS data in environmental microbiology: Look@NanoSIMS
journal, January 2012


Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review
journal, January 2009

  • Boudouresque, Charles F.; Bernard, Guillaume; Pergent, Gérard
  • Botanica Marina, Vol. 52, Issue 5
  • DOI: 10.1515/BOT.2009.057

Soil Microbial Activity at High Levels of Carbon Monoxide
journal, July 1991


Revisiting N2 fixation in Guerrero Negro intertidal microbial mats with a functional single-cell approach
journal, October 2014

  • Woebken, Dagmar; Burow, Luke C.; Behnam, Faris
  • The ISME Journal, Vol. 9, Issue 2
  • DOI: 10.1038/ismej.2014.144

Chemosynthetic endosymbioses: adaptations to oxic–anoxic interfaces
journal, September 2005

  • Stewart, Frank J.; Newton, Irene L. G.; Cavanaugh, Colleen M.
  • Trends in Microbiology, Vol. 13, Issue 9
  • DOI: 10.1016/j.tim.2005.07.007

Carbon monoxide and chromophoric dissolved organic matter cycles in the shelf waters of the northern California upwelling system
journal, January 2009

  • Day, Douglas A.; Faloona, Ian
  • Journal of Geophysical Research, Vol. 114, Issue C1
  • DOI: 10.1029/2007JC004590

Annual metabolic carbon balance of the seagrass Posidonia oceanica: the importance of carbohydrate reserves
journal, January 2001

  • Alcoverro, T.; Manzanera, M.; Romero, J.
  • Marine Ecology Progress Series, Vol. 211
  • DOI: 10.3354/meps211105

Symbiosis insights through metagenomic analysis of a microbial consortium
journal, September 2006

  • Woyke, Tanja; Teeling, Hanno; Ivanova, Natalia N.
  • Nature, Vol. 443, Issue 7114
  • DOI: 10.1038/nature05192

Arid soils as a source of atmospheric carbon monoxide
journal, December 1982


Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm
journal, May 2001

  • Dubilier, Nicole; Mülders, Caroline; Ferdelman, Tim
  • Nature, Vol. 411, Issue 6835
  • DOI: 10.1038/35077067

Convergent and divergent evolution of metabolism in sulfur-oxidizing symbionts and the role of horizontal gene transfer
journal, October 2012

  • Kleiner, Manuel; Petersen, Jillian M.; Dubilier, Nicole
  • Current Opinion in Microbiology, Vol. 15, Issue 5
  • DOI: 10.1016/j.mib.2012.09.003

Animals in a bacterial world, a new imperative for the life sciences
journal, February 2013

  • McFall-Ngai, Margaret; Hadfield, Michael G.; Bosch, Thomas C. G.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 9
  • DOI: 10.1073/pnas.1218525110

Symbioses between Bacteria and Gutless Marine Oligochaetes
book, January 2006


Symbiotic diversity in marine animals: the art of harnessing chemosynthesis
journal, October 2008

  • Dubilier, Nicole; Bergin, Claudia; Lott, Christian
  • Nature Reviews Microbiology, Vol. 6, Issue 10
  • DOI: 10.1038/nrmicro1992

Why bacteria matter in animal development and evolution
journal, June 2010


Symbioses of Methanotrophs and Deep-Sea Mussels (Mytilidae: Bathymodiolinae)
book, January 2006


Distribution, diversity and ecology of aerobic CO-oxidizing bacteria
journal, February 2007

  • King, Gary M.; Weber, Carolyn F.
  • Nature Reviews Microbiology, Vol. 5, Issue 2
  • DOI: 10.1038/nrmicro1595

Dynamics of Millenary Organic Deposits Resulting from the Growth of the Mediterranean SeagrassPosidonia oceanica
journal, January 1997

  • Mateo, M. A.; Romero, J.; Pérez, M.
  • Estuarine, Coastal and Shelf Science, Vol. 44, Issue 1
  • DOI: 10.1006/ecss.1996.0116

An oxygen microsensor with a guard cathode
journal, March 1989


Hydrogen and acetate cycling in two sulfate-reducing sediments: Buzzards Bay and Town Cove, Mass.
journal, October 1988


Multiple bacterial symbionts in two species of co-occurring gutless oligochaete worms from Mediterranean sea grass sediments
journal, December 2008


Carbon monoxide-dependent growth of Rhodospirillum rubrum.
journal, April 1995


Microbial carbon monoxide consumption in salt marsh sediments: Benthic marine CO consumption
journal, January 2007


Biology of Aerobic Carbon Monoxide-Oxidizing Bacteria
journal, October 1983


Detecting metabolic activities in single cells, with emphasis on nanoSIMS
journal, March 2012


Carbon monoxide-dependent energy metabolism in anaerobic bacteria and archaea
journal, June 2008


This place is big enough for both of us
journal, February 2007

  • Walker, Alan; Crossman, Lisa C.
  • Nature Reviews Microbiology, Vol. 5, Issue 2
  • DOI: 10.1038/nrmicro1601

Symbiosis as an adaptive process and source of phenotypic complexity
journal, May 2007

  • Moran, N. A.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue Supplement 1
  • DOI: 10.1073/pnas.0611659104

Occurrence, Classification, and Biological Function of Hydrogenases:  An Overview
journal, October 2007

  • Vignais, Paulette M.; Billoud, Bernard
  • Chemical Reviews, Vol. 107, Issue 10, p. 4206-4272
  • DOI: 10.1021/cr050196r

Metaproteomics of a gutless marine worm and its symbiotic microbial community reveal unusual pathways for carbon and energy use
journal, April 2012

  • Kleiner, M.; Wentrup, C.; Lott, C.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 19
  • DOI: 10.1073/pnas.1121198109

Learning how to live together: genomic insights into prokaryote–animal symbioses
journal, March 2008

  • Moya, Andrés; Peretó, Juli; Gil, Rosario
  • Nature Reviews Genetics, Vol. 9, Issue 3
  • DOI: 10.1038/nrg2319

Kinetics of H 2 oxidation in respiring and denitrifying Paracoccus denitrificans
journal, March 1991


Inhibitory effect of ZnCl2 on glycolysis in human oral microbes
journal, February 2002


Enrichment of High-Affinity CO Oxidizers in Maine Forest Soil
journal, August 2001


Unseen Forces: The Influence of Bacteria on Animal Development
journal, February 2002


Characteristics of abiological carbon monoxide formation from soil organic matter, humic acids, and phenolic compounds
journal, December 1985

  • Conrad, Ralf.; Seiler, Wolfgang.
  • Environmental Science & Technology, Vol. 19, Issue 12
  • DOI: 10.1021/es00142a004

Hydrogen is an energy source for hydrothermal vent symbioses
journal, August 2011

  • Petersen, Jillian M.; Zielinski, Frank U.; Pape, Thomas
  • Nature, Vol. 476, Issue 7359
  • DOI: 10.1038/nature10325

Comparative metagenomics of bathypelagic plankton and bottom sediment from the Sea of Marmara
journal, July 2010

  • Quaiser, Achim; Zivanovic, Yvan; Moreira, David
  • The ISME Journal, Vol. 5, Issue 2
  • DOI: 10.1038/ismej.2010.113

The future of seagrass meadows
journal, June 2002


The effect of FISH and CARD-FISH on the isotopic composition of 13C- and 15N-labeled Pseudomonas putida cells measured by nanoSIMS
journal, June 2014

  • Musat, Niculina; Stryhanyuk, Hryhoriy; Bombach, Petra
  • Systematic and Applied Microbiology, Vol. 37, Issue 4
  • DOI: 10.1016/j.syapm.2014.02.002

Physiological characteristics of various species of strains of carboxydobacteria
journal, October 1980

  • Cypionka, H.; Meyer, O.; Schlegel, H. G.
  • Archives of Microbiology, Vol. 127, Issue 3
  • DOI: 10.1007/BF00427208

Potentiation of bacterial killing activity of zinc chloride by pyrrolidine dithiocarbamate
journal, February 2010

  • Choi, Eun-Kyoung; Lee, Hye-Hyang; Kang, Mi-Sun
  • The Journal of Microbiology, Vol. 48, Issue 1
  • DOI: 10.1007/s12275-009-0049-2

Role of Microorganisms in the Consumption and Production of Atmospheric Carbon Monoxide by Soil
journal, January 1980


The Specific Potency of Certain Cations with Reference to Their Effect on Bacterial Viability 1
journal, January 1931


Occurrence, Classification, and Biological Function of Hydrogenases: An Overview
journal, December 2007


Geochemical constraints on the diversity and activity of H2-oxidizing microorganisms in diffuse hydrothermal fluids from a basalt- and an ultramafic-hosted vent
journal, May 2013

  • Perner, Mirjam; Petersen, Jillian M.; Zielinski, Frank
  • FEMS Microbiology Ecology, Vol. 85, Issue 1
  • DOI: 10.1111/1574-6941.12147

Animals in a bacterial world, a new imperative for the life sciences
text, January 2013

  • Nicole, Dubilier,; G., Hadfield, Michael; Nicole, King,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/ecbw-3974

Why bacteria matter in animal development and evolution
journal, June 2010


Carbon monoxide-dependent energy metabolism in anaerobic bacteria and archaea
journal, June 2008


Potentiation of bacterial killing activity of zinc chloride by pyrrolidine dithiocarbamate
journal, February 2010

  • Choi, Eun-Kyoung; Lee, Hye-Hyang; Kang, Mi-Sun
  • The Journal of Microbiology, Vol. 48, Issue 1
  • DOI: 10.1007/s12275-009-0049-2

Convergent and divergent evolution of metabolism in sulfur-oxidizing symbionts and the role of horizontal gene transfer
journal, October 2012

  • Kleiner, Manuel; Petersen, Jillian M.; Dubilier, Nicole
  • Current Opinion in Microbiology, Vol. 15, Issue 5
  • DOI: 10.1016/j.mib.2012.09.003

The effect of FISH and CARD-FISH on the isotopic composition of 13C- and 15N-labeled Pseudomonas putida cells measured by nanoSIMS
journal, June 2014

  • Musat, Niculina; Stryhanyuk, Hryhoriy; Bombach, Petra
  • Systematic and Applied Microbiology, Vol. 37, Issue 4
  • DOI: 10.1016/j.syapm.2014.02.002

Chemosynthetic endosymbioses: adaptations to oxic–anoxic interfaces
journal, September 2005

  • Stewart, Frank J.; Newton, Irene L. G.; Cavanaugh, Colleen M.
  • Trends in Microbiology, Vol. 13, Issue 9
  • DOI: 10.1016/j.tim.2005.07.007

Characteristics of abiological carbon monoxide formation from soil organic matter, humic acids, and phenolic compounds
journal, December 1985

  • Conrad, Ralf.; Seiler, Wolfgang.
  • Environmental Science & Technology, Vol. 19, Issue 12
  • DOI: 10.1021/es00142a004

Endosymbiotic sulphate-reducing and sulphide-oxidizing bacteria in an oligochaete worm
journal, May 2001

  • Dubilier, Nicole; Mülders, Caroline; Ferdelman, Tim
  • Nature, Vol. 411, Issue 6835
  • DOI: 10.1038/35077067

Comparative metagenomics of bathypelagic plankton and bottom sediment from the Sea of Marmara
journal, July 2010

  • Quaiser, Achim; Zivanovic, Yvan; Moreira, David
  • The ISME Journal, Vol. 5, Issue 2
  • DOI: 10.1038/ismej.2010.113

Learning how to live together: genomic insights into prokaryote–animal symbioses
journal, March 2008

  • Moya, Andrés; Peretó, Juli; Gil, Rosario
  • Nature Reviews Genetics, Vol. 9, Issue 3
  • DOI: 10.1038/nrg2319

Distribution, diversity and ecology of aerobic CO-oxidizing bacteria
journal, February 2007

  • King, Gary M.; Weber, Carolyn F.
  • Nature Reviews Microbiology, Vol. 5, Issue 2
  • DOI: 10.1038/nrmicro1595

Resourceful heterotrophs make the most of light in the coastal ocean
journal, October 2007

  • Moran, Mary Ann; Miller, William L.
  • Nature Reviews Microbiology, Vol. 5, Issue 10
  • DOI: 10.1038/nrmicro1746

Symbiosis as an adaptive process and source of phenotypic complexity
journal, May 2007

  • Moran, N. A.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue Supplement 1
  • DOI: 10.1073/pnas.0611659104

Animals in a bacterial world, a new imperative for the life sciences
journal, February 2013

  • McFall-Ngai, Margaret; Hadfield, Michael G.; Bosch, Thomas C. G.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 9
  • DOI: 10.1073/pnas.1218525110

Geochemical constraints on the diversity and activity of H2-oxidizing microorganisms in diffuse hydrothermal fluids from a basalt- and an ultramafic-hosted vent
journal, May 2013

  • Perner, Mirjam; Petersen, Jillian M.; Zielinski, Frank
  • FEMS Microbiology Ecology, Vol. 85, Issue 1
  • DOI: 10.1111/1574-6941.12147

Multiple bacterial symbionts in two species of co-occurring gutless oligochaete worms from Mediterranean sea grass sediments
journal, December 2008


Detecting metabolic activities in single cells, with emphasis on nanoSIMS
journal, March 2012


CO Dehydrogenase Genes Found in Metagenomic Fosmid Clones from the Deep Mediterranean Sea
journal, October 2009

  • Martin-Cuadrado, A. -B.; Ghai, R.; Gonzaga, A.
  • Applied and Environmental Microbiology, Vol. 75, Issue 23
  • DOI: 10.1128/aem.01283-09

Influence of pH on microbial hydrogen metabolism in diverse sedimentary ecosystems.
journal, January 1988


Energy Generation from the CO Oxidation-Hydrogen Production Pathway in Rubrivivax gelatinosus
journal, June 2005


Carbon Monoxide Oxidation by Clostridium thermoaceticum and Clostridium formicoaceticum
journal, January 1978


Effects of Deletion of Genes Encoding Fe-Only Hydrogenase of Desulfovibrio vulgaris Hildenborough on Hydrogen and Lactate Metabolism
journal, February 2002


Biology of Aerobic Carbon Monoxide-Oxidizing Bacteria
journal, October 1983


Works referencing / citing this record:

Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation
journal, October 2016


Genomic, transcriptomic, and proteomic insights into the symbiosis of deep-sea tubeworm holobionts
journal, October 2019


Metaproteomics method to determine carbon sources and assimilation pathways of species in microbial communities
journal, May 2018

  • Kleiner, Manuel; Dong, Xiaoli; Hinzke, Tjorven
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 24
  • DOI: 10.1073/pnas.1722325115

Chemosynthetic symbiont with a drastically reduced genome serves as primary energy storage in the marine flatworm Paracatenula
journal, April 2019

  • Jäckle, Oliver; Seah, Brandon K. B.; Tietjen, Målin
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 17
  • DOI: 10.1073/pnas.1818995116

A metaproteomics method to determine carbon sources and assimilation pathways of species in microbial communities
posted_content, January 2018


Evidence for H 2 consumption by uncultured Desulfobacterales in coastal sediments: H 2 -consuming sulfate reducers in coastal sediments
journal, September 2017

  • Dyksma, Stefan; Pjevac, Petra; Ovanesov, Kin
  • Environmental Microbiology, Vol. 20, Issue 2
  • DOI: 10.1111/1462-2920.13880

Sulfur-Oxidizing Symbionts without Canonical Genes for Autotrophic CO 2 Fixation
journal, June 2019

  • Seah, Brandon K. B.; Antony, Chakkiath Paul; Huettel, Bruno
  • mBio, Vol. 10, Issue 3
  • DOI: 10.1128/mbio.01112-19

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


Chemosynthetic symbionts of marine invertebrate animals are capable of nitrogen fixation
journal, October 2016


Chemosynthetic symbiont with a drastically reduced genome serves as primary energy storage in the marine flatworm Paracatenula
journal, April 2019

  • Jäckle, Oliver; Seah, Brandon K. B.; Tietjen, Målin
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 17
  • DOI: 10.1073/pnas.1818995116

Acquisition of a Novel Sulfur-Oxidizing Symbiont in the Gutless Marine Worm Inanidrilus exumae
journal, April 2018

  • Bergin, C.; Wentrup, C.; Brewig, N.
  • Applied and Environmental Microbiology, Vol. 84, Issue 7
  • DOI: 10.1128/aem.02267-17

Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.