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Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies.
ISME J 2019IJ

Abstract

Trichodesmium is an important dinitrogen (N2)-fixing cyanobacterium in marine ecosystems. Recent nucleic acid analyses indicate that Trichodesmium colonies with their diverse epibionts support various nitrogen (N) transformations beyond N2 fixation. However, rates of these transformations and concentration gradients of N compounds in Trichodesmium colonies remain largely unresolved. We combined isotope-tracer incubations, micro-profiling and numeric modelling to explore carbon fixation, N cycling processes as well as oxygen, ammonium and nitrate concentration gradients in individual field-sampled Trichodesmium colonies. Colonies were net-autotrophic, with carbon and N2 fixation occurring mostly during the day. Ten percent of the fixed N was released as ammonium after 12-h incubations. Nitrification was not detectable but nitrate consumption was high when nitrate was added. The consumed nitrate was partly reduced to ammonium, while denitrification was insignificant. Thus, the potential N transformation network was characterised by fixed N gain and recycling processes rather than denitrification. Oxygen concentrations within colonies were ~60-200% air-saturation. Moreover, our modelling predicted steep concentration gradients, with up to 6-fold higher ammonium concentrations, and nitrate depletion in the colony centre compared to the ambient seawater. These gradients created a chemically heterogeneous microenvironment, presumably facilitating diverse microbial metabolisms in millimetre-sized Trichodesmium colonies.

Authors+Show Affiliations

Department of Ecology, Environment and Plant Sciences, Stockholm University, Stockholm, Sweden. klawonn@stanford.edu. Department of Experimental Limnology, IGB-Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Berlin, Germany. klawonn@stanford.edu. Department of Earth System Science, Stanford University, Stanford, CA, USA. klawonn@stanford.edu.Department of Marine Sciences, University of Gothenburg, Gothenburg, Sweden. Centre A lgatech, Institute of Microbiology, The Czech Academy of Sciences, Trebon, Czech Republic.Daniel K. Inouye Center for Microbial Oceanography, Research and Education, University of Hawai'i at Manoa, Honolulu, HI, USA.Department of Physics & Earth Sciences, Jacobs University Bremen, Bremen, Germany. Max Planck Institute for Marine Microbiology, Bremen, Germany.Department of Biology and Nordic Center for Earth Evolution, University of Southern Denmark, Odense M, Denmark.Department of Isotope Biogeochemistry, Helmholtz Centre for Environmental Research (UFZ), Leipzig, Germany.Department of Isotope Biogeochemistry, Helmholtz Centre for Environmental Research (UFZ), Leipzig, Germany.Department of Physics & Earth Sciences, Jacobs University Bremen, Bremen, Germany. Max Planck Institute for Marine Microbiology, Bremen, Germany.Department of Experimental Limnology, IGB-Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Berlin, Germany.Daniel K. Inouye Center for Microbial Oceanography, Research and Education, University of Hawai'i at Manoa, Honolulu, HI, USA.Department of Marine Sciences, University of Gothenburg, Gothenburg, Sweden.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31636364

Citation

Klawonn, Isabell, et al. "Distinct Nitrogen Cycling and Steep Chemical Gradients in Trichodesmium Colonies." The ISME Journal, 2019.
Klawonn I, Eichner MJ, Wilson ST, et al. Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies. ISME J. 2019.
Klawonn, I., Eichner, M. J., Wilson, S. T., Moradi, N., Thamdrup, B., Kümmel, S., ... Ploug, H. (2019). Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies. The ISME Journal, doi:10.1038/s41396-019-0514-9.
Klawonn I, et al. Distinct Nitrogen Cycling and Steep Chemical Gradients in Trichodesmium Colonies. ISME J. 2019 Oct 21; PubMed PMID: 31636364.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies. AU - Klawonn,Isabell, AU - Eichner,Meri J, AU - Wilson,Samuel T, AU - Moradi,Nasrollah, AU - Thamdrup,Bo, AU - Kümmel,Steffen, AU - Gehre,Matthias, AU - Khalili,Arzhang, AU - Grossart,Hans-Peter, AU - Karl,David M, AU - Ploug,Helle, Y1 - 2019/10/21/ PY - 2019/03/11/received PY - 2019/09/11/accepted PY - 2019/09/10/revised PY - 2019/10/23/pubmed PY - 2019/10/23/medline PY - 2019/10/23/entrez JF - The ISME journal JO - ISME J N2 - Trichodesmium is an important dinitrogen (N2)-fixing cyanobacterium in marine ecosystems. Recent nucleic acid analyses indicate that Trichodesmium colonies with their diverse epibionts support various nitrogen (N) transformations beyond N2 fixation. However, rates of these transformations and concentration gradients of N compounds in Trichodesmium colonies remain largely unresolved. We combined isotope-tracer incubations, micro-profiling and numeric modelling to explore carbon fixation, N cycling processes as well as oxygen, ammonium and nitrate concentration gradients in individual field-sampled Trichodesmium colonies. Colonies were net-autotrophic, with carbon and N2 fixation occurring mostly during the day. Ten percent of the fixed N was released as ammonium after 12-h incubations. Nitrification was not detectable but nitrate consumption was high when nitrate was added. The consumed nitrate was partly reduced to ammonium, while denitrification was insignificant. Thus, the potential N transformation network was characterised by fixed N gain and recycling processes rather than denitrification. Oxygen concentrations within colonies were ~60-200% air-saturation. Moreover, our modelling predicted steep concentration gradients, with up to 6-fold higher ammonium concentrations, and nitrate depletion in the colony centre compared to the ambient seawater. These gradients created a chemically heterogeneous microenvironment, presumably facilitating diverse microbial metabolisms in millimetre-sized Trichodesmium colonies. SN - 1751-7370 UR - https://www.unboundmedicine.com/medline/citation/31636364/Distinct_nitrogen_cycling_and_steep_chemical_gradients_in_Trichodesmium_colonies L2 - http://dx.doi.org/10.1038/s41396-019-0514-9 DB - PRIME DP - Unbound Medicine ER -