Observed metabolic asymmetry within soybean root nodules reflects unexpected complexity in rhizobacteria-legume metabolite exchange
Abstract
Utilization of high-resolution molecular tomography revealed that the soybean nodule is not metabolically uniform, with several distinctive patterns of metabolite distributions through the nodule’s anatomy. Specifically, using two- and three-dimensional matrix-assisted laser desorption/ionization Fourier transform ion cyclotron resonance mass spectrometry imaging (MALDI-FTICR MSI) metabolites showed i) cortex localization, ii) a gradual increase toward the central infection zone, iii) uniform localization through whole nodule, iv) uniform localization throughout the infection zone, or v) asymmetric distribution within the infection zone. Some molecules belonging to the same or correlated metabolic pathways were found localized with different patterns, indicating localized differences in their synthesis/turnover. Special attention was given to asymmetrical distributed metabolites (e.g., S-adenosylmethionine; SAMe), where some small-scale patterns were detected in individual sections, and 3D reconstruction enabled resolution of whole nodule molecular distributions. These results hint at a complex, spatially differentiated metabolism occurring in soybean root nodules.
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1454346
- Alternate Identifier(s):
- OSTI ID: 1458774; OSTI ID: 1513206
- Report Number(s):
- PNNL-SA-127419
Journal ID: ISSN 1751-7362
- Grant/Contract Number:
- DOE-FOA-0001192; 1734145; AC05-76RL01830
- Resource Type:
- Published Article
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Name: The ISME Journal Journal Volume: 12 Journal Issue: 9; Journal ID: ISSN 1751-7362
- Publisher:
- Oxford University Press
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Veličković, Dušan, Agtuca, Beverly J., Stopka, Sylwia A., Vertes, Akos, Koppenaal, David W., Paša-Tolić, Ljiljana, Stacey, Gary, and Anderton, Christopher R. Observed metabolic asymmetry within soybean root nodules reflects unexpected complexity in rhizobacteria-legume metabolite exchange. United Kingdom: N. p., 2018.
Web. doi:10.1038/s41396-018-0188-8.
Veličković, Dušan, Agtuca, Beverly J., Stopka, Sylwia A., Vertes, Akos, Koppenaal, David W., Paša-Tolić, Ljiljana, Stacey, Gary, & Anderton, Christopher R. Observed metabolic asymmetry within soybean root nodules reflects unexpected complexity in rhizobacteria-legume metabolite exchange. United Kingdom. https://doi.org/10.1038/s41396-018-0188-8
Veličković, Dušan, Agtuca, Beverly J., Stopka, Sylwia A., Vertes, Akos, Koppenaal, David W., Paša-Tolić, Ljiljana, Stacey, Gary, and Anderton, Christopher R. Wed .
"Observed metabolic asymmetry within soybean root nodules reflects unexpected complexity in rhizobacteria-legume metabolite exchange". United Kingdom. https://doi.org/10.1038/s41396-018-0188-8.
@article{osti_1454346,
title = {Observed metabolic asymmetry within soybean root nodules reflects unexpected complexity in rhizobacteria-legume metabolite exchange},
author = {Veličković, Dušan and Agtuca, Beverly J. and Stopka, Sylwia A. and Vertes, Akos and Koppenaal, David W. and Paša-Tolić, Ljiljana and Stacey, Gary and Anderton, Christopher R.},
abstractNote = {Utilization of high-resolution molecular tomography revealed that the soybean nodule is not metabolically uniform, with several distinctive patterns of metabolite distributions through the nodule’s anatomy. Specifically, using two- and three-dimensional matrix-assisted laser desorption/ionization Fourier transform ion cyclotron resonance mass spectrometry imaging (MALDI-FTICR MSI) metabolites showed i) cortex localization, ii) a gradual increase toward the central infection zone, iii) uniform localization through whole nodule, iv) uniform localization throughout the infection zone, or v) asymmetric distribution within the infection zone. Some molecules belonging to the same or correlated metabolic pathways were found localized with different patterns, indicating localized differences in their synthesis/turnover. Special attention was given to asymmetrical distributed metabolites (e.g., S-adenosylmethionine; SAMe), where some small-scale patterns were detected in individual sections, and 3D reconstruction enabled resolution of whole nodule molecular distributions. These results hint at a complex, spatially differentiated metabolism occurring in soybean root nodules.},
doi = {10.1038/s41396-018-0188-8},
journal = {The ISME Journal},
number = 9,
volume = 12,
place = {United Kingdom},
year = {Wed Jun 13 00:00:00 EDT 2018},
month = {Wed Jun 13 00:00:00 EDT 2018}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1038/s41396-018-0188-8
https://doi.org/10.1038/s41396-018-0188-8
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 37 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Experimental evolution of nodule intracellular infection in legume symbionts
journal, February 2013
- Guan, Su Hua; Gris, Carine; Cruveiller, Stéphane
- The ISME Journal, Vol. 7, Issue 7
Feasibility Assessment of a MALDI FTICR Imaging Approach for the 3D Reconstruction of a Mouse Lung
journal, April 2017
- Jones, E. Ellen; Quiason, Cristine; Dale, Stephanie
- Journal of The American Society for Mass Spectrometry, Vol. 28, Issue 8
Involvement of polyamines in the root nodule regulation of soybeans (Glycine max)
journal, January 2008
- Terakado-Tonooka, Junko; Fujihara, Shinsuke
- Plant Root, Vol. 2
MALDI mass spectrometry-assisted molecular imaging of metabolites during nitrogen fixation in the Medicago truncatula - Sinorhizobium meliloti symbiosis
journal, May 2013
- Ye, Hui; Gemperline, Erin; Venkateshwaran, Muthusubramanian
- The Plant Journal, Vol. 75, Issue 1
Microbial metabolic exchange in 3D
journal, January 2013
- Watrous, Jeramie D.; Phelan, Vanessa V.; Hsu, Cheng-Chih
- The ISME Journal, Vol. 7, Issue 4
Leghemoglobin and Rhizobium Respiration
journal, June 1984
- Appleby, C. A.
- Annual Review of Plant Physiology, Vol. 35, Issue 1
The Site of Oxygen Limitation in Soybean Nodules
journal, February 1999
- Kuzma, Monika M.; Winter, Heike; Storer, Paul
- Plant Physiology, Vol. 119, Issue 2
Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant: Phosphatidylcholine biosynthesis in Bradyrhizobium japonicum
journal, March 2001
- Minder, Alexander C.; De Rudder, Karel E. E.; Narberhaus, Franz
- Molecular Microbiology, Vol. 39, Issue 5
Mass spectrometry imaging: Towards mapping the elemental and molecular composition of the rhizosphere
journal, June 2017
- Veličković, Dušan; Anderton, Christopher R.
- Rhizosphere, Vol. 3
Structure and Function of S -Adenosylmethionine Synthetase: Crystal Structures of S -Adenosylmethionine Synthetase with ADP, BrADP, and PP i at 2.8 Å Resolution † , ‡
journal, January 1996
- Takusagawa, Fusao; Kamitori, Shigehiro; Markham, George D.
- Biochemistry, Vol. 35, Issue 8
Multifaceted Investigation of Metabolites During Nitrogen Fixation in Medicago via High Resolution MALDI-MS Imaging and ESI-MS
journal, October 2014
- Gemperline, Erin; Jayaraman, Dhileepkumar; Maeda, Junko
- Journal of The American Society for Mass Spectrometry, Vol. 26, Issue 1
Laser-ablation electrospray ionization mass spectrometry with ion mobility separation reveals metabolites in the symbiotic interactions of soybean roots and rhizobia
journal, May 2017
- Stopka, Sylwia A.; Agtuca, Beverly J.; Koppenaal, David W.
- The Plant Journal, Vol. 91, Issue 2
Three-Dimensional Vizualization of Mouse Brain by Lipid Analysis Using Ambient Ionization Mass Spectrometry
journal, December 2009
- Eberlin, Livia S.; Ifa, Demian R.; Wu, Chunping
- Angewandte Chemie International Edition, Vol. 49, Issue 5