Chemical microenvironments and single-cell carbon and nitrogen uptake in field-collected colonies of Trichodesmium under different pCO2

Gradients of oxygen (O 2 ) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O 2 were investigated under different partial pressures of carbon dioxide ( p CO 2 ) in field-collected colonies of the marine dinitrogen (N 2 )-fixing cyanobacterium Trichodesmium . Microsensor measurem...

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Published inThe ISME Journal Vol. 11; no. 6; pp. 1305 - 1317
Main Authors Eichner, Meri J, Klawonn, Isabell, Wilson, Samuel T, Littmann, Sten, Whitehouse, Martin J, Church, Matthew J, Kuypers, Marcel MM, Karl, David M, Ploug, Helle
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Published London Nature Publishing Group UK 01.06.2017
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Abstract Gradients of oxygen (O 2 ) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O 2 were investigated under different partial pressures of carbon dioxide ( p CO 2 ) in field-collected colonies of the marine dinitrogen (N 2 )-fixing cyanobacterium Trichodesmium . Microsensor measurements indicated that cells within colonies experienced large fluctuations in O 2 , pH and CO 2 concentrations over a day–night cycle. O 2 concentrations varied with light intensity and time of day, yet colonies exposed to light were supersaturated with O 2 (up to ~200%) throughout the light period and anoxia was not detected. Alternating between light and dark conditions caused a variation in pH levels by on average 0.5 units (equivalent to 15 nmol l −1 proton concentration). Single-cell analyses of C and N assimilation using secondary ion mass spectrometry (SIMS; large geometry SIMS and nanoscale SIMS) revealed high variability in metabolic activity of single cells and trichomes of Trichodesmium, and indicated transfer of C and N to colony-associated non-photosynthetic bacteria. Neither O 2 fluxes nor C fixation by Trichodesmium were significantly influenced by short-term incubations under different p CO 2 levels, whereas N 2 fixation increased with increasing p CO 2 . The large range of metabolic rates observed at the single-cell level may reflect a response by colony-forming microbial populations to highly variable microenvironments.
AbstractList Gradients of oxygen (O2 ) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O2 were investigated under different partial pressures of carbon dioxide (pCO2 ) in field-collected colonies of the marine dinitrogen (N2 )-fixing cyanobacterium Trichodesmium. Microsensor measurements indicated that cells within colonies experienced large fluctuations in O2 , pH and CO2 concentrations over a day-night cycle. O2 concentrations varied with light intensity and time of day, yet colonies exposed to light were supersaturated with O2 (up to ~200%) throughout the light period and anoxia was not detected. Alternating between light and dark conditions caused a variation in pH levels by on average 0.5 units (equivalent to 15 nmol l-1 proton concentration). Single-cell analyses of C and N assimilation using secondary ion mass spectrometry (SIMS; large geometry SIMS and nanoscale SIMS) revealed high variability in metabolic activity of single cells and trichomes of Trichodesmium, and indicated transfer of C and N to colony-associated non-photosynthetic bacteria. Neither O2 fluxes nor C fixation by Trichodesmium were significantly influenced by short-term incubations under different pCO2 levels, whereas N2 fixation increased with increasing pCO2 . The large range of metabolic rates observed at the single-cell level may reflect a response by colony-forming microbial populations to highly variable microenvironments.
Gradients of oxygen (O2) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O2 were investigated under different partial pressures of carbon dioxide ( p CO2) in field-collected colonies of the marine dinitrogen (N2)-fixing cyanobacterium  Trichodesmium . Microsensor measurements indicated that cells within colonies experienced large fluctuations in O2, pH and CO2concentrations over a day–night cycle. O2 concentrations varied with light intensity and time of day, yet colonies exposed to light were supersaturated with O2 (up to ~200%) throughout the light period and anoxia was not detected. Alternating between light and dark conditions caused a variation in pH levels by on average 0.5 units (equivalent to 15 nmol l−1 proton concentration). Single-cell analyses of C and N assimilation using secondary ion mass spectrometry (SIMS; large geometry SIMS and nanoscale SIMS) revealed high variability in metabolic activity of single cells and trichomes of  Trichodesmium,  and indicated transfer of C and N to colony-associated non-photosynthetic bacteria. Neither O2 fluxes nor C fixation by  Trichodesmium  were significantly influenced by short-term incubations under different  p CO2 levels, whereas N2fixation increased with increasing  p CO2. The large range of metabolic rates observed at the single-cell level may reflect a response by colony-forming microbial populations to highly variable microenvironments.
© 2017 The Author(s)Gradients of oxygen (O2) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O2 were investigated under different partial pressures of carbon dioxide (pCO2) in field-collected colonies of the marine dinitrogen (N2)-fixing cyanobacterium Trichodesmium. Microsensor measurements indicated that cells within colonies experienced large fluctuations in O2, pH and CO2 concentrations over a day–night cycle. O2 concentrations varied with light intensity and time of day, yet colonies exposed to light were supersaturated with O2 (up to ~200%) throughout the light period and anoxia was not detected. Alternating between light and dark conditions caused a variation in pH levels by on average 0.5 units (equivalent to 15nmoll-1 proton concentration). Single-cell analyses of C and N assimilation using secondary ion mass spectrometry (SIMS; large geometry SIMS and nanoscale SIMS) revealed high variability in metabolic activity of single cells and trichomes of Trichodesmium, and indicated transfer of C and N to colony-associated non-photosynthetic bacteria. Neither O2 fluxes nor C fixation by Trichodesmium were significantly influenced by short-term incubations under different pCO2 levels, whereas N2 fixation increased with increasing pCO2. The large range of metabolic rates observed at the single-cell level may reflect a response by colony-forming microbial populations to highly variable microenvironments.The ISME Journal advance online publication, 11 April 2017; doi:10.1038/ismej.2017.15.
Gradients of oxygen (O 2 ) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O 2 were investigated under different partial pressures of carbon dioxide ( p CO 2 ) in field-collected colonies of the marine dinitrogen (N 2 )-fixing cyanobacterium Trichodesmium . Microsensor measurements indicated that cells within colonies experienced large fluctuations in O 2 , pH and CO 2 concentrations over a day–night cycle. O 2 concentrations varied with light intensity and time of day, yet colonies exposed to light were supersaturated with O 2 (up to ~200%) throughout the light period and anoxia was not detected. Alternating between light and dark conditions caused a variation in pH levels by on average 0.5 units (equivalent to 15 nmol l −1 proton concentration). Single-cell analyses of C and N assimilation using secondary ion mass spectrometry (SIMS; large geometry SIMS and nanoscale SIMS) revealed high variability in metabolic activity of single cells and trichomes of Trichodesmium, and indicated transfer of C and N to colony-associated non-photosynthetic bacteria. Neither O 2 fluxes nor C fixation by Trichodesmium were significantly influenced by short-term incubations under different p CO 2 levels, whereas N 2 fixation increased with increasing p CO 2 . The large range of metabolic rates observed at the single-cell level may reflect a response by colony-forming microbial populations to highly variable microenvironments.
Author Eichner, Meri J
Karl, David M
Klawonn, Isabell
Ploug, Helle
Wilson, Samuel T
Littmann, Sten
Kuypers, Marcel MM
Whitehouse, Martin J
Church, Matthew J
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  givenname: Meri J
  surname: Eichner
  fullname: Eichner, Meri J
  email: meichner@mpi-bremen.de
  organization: Department of Marine Sciences, University of Gothenburg, 6Current address: Max Planck Institute for Marine Microbiology, Bremen, Germany
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  givenname: Isabell
  surname: Klawonn
  fullname: Klawonn, Isabell
  organization: Department of Ecology, Environment and Plant Sciences, University of Stockholm, 7Current address: Leibnitz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany
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  givenname: Samuel T
  surname: Wilson
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  organization: Daniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaii
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  givenname: Sten
  surname: Littmann
  fullname: Littmann, Sten
  organization: Department of Biogeochemistry, Max Planck Institute for Marine Microbiology
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  givenname: Martin J
  surname: Whitehouse
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  organization: Department of Geosciences, Swedish Museum of Natural History
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  surname: Church
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  organization: Daniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaii
– sequence: 7
  givenname: Marcel MM
  surname: Kuypers
  fullname: Kuypers, Marcel MM
  organization: Department of Biogeochemistry, Max Planck Institute for Marine Microbiology
– sequence: 8
  givenname: David M
  surname: Karl
  fullname: Karl, David M
  organization: Daniel K. Inouye Center for Microbial Oceanography: Research and Education, University of Hawaii
– sequence: 9
  givenname: Helle
  surname: Ploug
  fullname: Ploug, Helle
  organization: Department of Marine Sciences, University of Gothenburg
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Current address: Max Planck Institute for Marine Microbiology, Bremen, Germany.
Current address: Leibnitz Institute of Freshwater Ecology and Inland Fisheries (IGB), Berlin, Germany.
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    fullname: Waterbury
– volume: 96
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  article-title: Mechanism of molybdenum nitrogenase
  publication-title: Chem Rev
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SSID ssj0057667
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Snippet Gradients of oxygen (O 2 ) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O 2 were investigated under different partial pressures of...
Gradients of oxygen (O2 ) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O2 were investigated under different partial pressures of...
Gradients of oxygen (O2) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O2 were investigated under different partial pressures of carbon...
Gradients of oxygen (O2) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O2 were investigated under different partial pressures of carbon...
© 2017 The Author(s)Gradients of oxygen (O2) and pH, as well as small-scale fluxes of carbon (C), nitrogen (N) and O2 were investigated under different partial...
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SubjectTerms 101/58
14/63
631/326/171/1878
704/158/2165
704/158/2466
704/158/855
Anoxia
Assimilation
Bacteria
Biomedical and Life Sciences
Carbon
Carbon dioxide
Climate Research
Colonies
Ecology
Ecosystems and species history
Ekologi
Ekosystem och arthistoria
Evolutionary Biology
Fixation
Fluxes
Geosciences, Multidisciplinary
Klimatforskning
Life Sciences
Light intensity
Light levels
Luminous intensity
Mass spectrometry
Mass spectroscopy
Metabolism
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Microenvironments
Microorganisms
Multidisciplinär geovetenskap
Night
Nitrogen
Nitrogen fixation
Original
original-article
Photosynthesis
Populations
Secondary ion mass spectrometry
Time of use
Trichomes
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Title Chemical microenvironments and single-cell carbon and nitrogen uptake in field-collected colonies of Trichodesmium under different pCO2
URI https://link.springer.com/article/10.1038/ismej.2017.15
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https://urn.kb.se/resolve?urn=urn:nbn:se:nrm:diva-2537
https://gup.ub.gu.se/publication/252946
Volume 11
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