Observed metabolic asymmetry within soybean root nodules reflects unexpected complexity in rhizobacteria-legume metabolite exchange

Veličković, Dušan; Agtuca, Beverly J.; Stopka, Sylwia A.; Vertes, Akos; Koppenaal, David W.; Paša-Tolić, Ljiljana; Stacey, Gary; Anderton, Christopher R.

doi:10.1038/s41396-018-0188-8

Observed metabolic asymmetry within soybean root nodules reflects unexpected complexity in rhizobacteria-legume metabolite exchange

Journal Article · Wed Jun 13 00:00:00 EDT 2018 · The ISME Journal

DOI:https://doi.org/10.1038/s41396-018-0188-8· OSTI ID:1454346

Veličković, Dušan; Agtuca, Beverly J.; Stopka, Sylwia A.; Vertes, Akos; Koppenaal, David W.; Paša-Tolić, Ljiljana; Stacey, Gary;

Abstract

In this study, the three-dimensional spatial distributions of a number of metabolites involved in regulating symbiosis and biological nitrogen fixation (BNF) within soybean root nodules were revealed using matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI). While many metabolites exhibited distinct spatial compartmentalization, some metabolites were asymmetrically distributed throughout the nodule (e.g., S-adenosylmethionine). These results establish a more complex metabolic view of plant–bacteria symbiosis (and BNF) within soybean nodules than previously hypothesized. Collectively these findings suggest that spatial perspectives in metabolic regulation should be considered to unravel the overall complexity of interacting organisms, like those relating to associations of nitrogen-fixing bacteria with host plants.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1454346

Alternate ID(s):: OSTI ID: 1513206
OSTI ID: 1458774

Report Number(s):: PNNL-SA--127419

Journal Information:: The ISME Journal, Journal Name: The ISME Journal Journal Issue: 9 Vol. 12; ISSN 1751-7362

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (13)

Three-Dimensional Vizualization of Mouse Brain by Lipid Analysis Using Ambient Ionization Mass Spectrometry Eberlin, Livia S.; Ifa, Demian R.; Wu, Chunping Angewandte Chemie International Edition, Vol. 49, Issue 5 https://doi.org/10.1002/anie.200906283	journal	December 2009
Multifaceted Investigation of Metabolites During Nitrogen Fixation in Medicago via High Resolution MALDI-MS Imaging and ESI-MS Gemperline, Erin; Jayaraman, Dhileepkumar; Maeda, Junko Journal of The American Society for Mass Spectrometry, Vol. 26, Issue 1 https://doi.org/10.1007/s13361-014-1010-0	journal	October 2014
Feasibility Assessment of a MALDI FTICR Imaging Approach for the 3D Reconstruction of a Mouse Lung Jones, E. Ellen; Quiason, Cristine; Dale, Stephanie Journal of The American Society for Mass Spectrometry, Vol. 28, Issue 8 https://doi.org/10.1007/s13361-017-1658-3	journal	April 2017
Mass spectrometry imaging: Towards mapping the elemental and molecular composition of the rhizosphere Veličković, Dušan; Anderton, Christopher R. Rhizosphere, Vol. 3 https://doi.org/10.1016/j.rhisph.2017.03.003	journal	June 2017
Structure and Function of S -Adenosylmethionine Synthetase: Crystal Structures of S -Adenosylmethionine Synthetase with ADP, BrADP, and PP _i at 2.8 Å Resolution ^† ^, ^‡ Takusagawa, Fusao; Kamitori, Shigehiro; Markham, George D. Biochemistry, Vol. 35, Issue 8 https://doi.org/10.1021/bi952604z	journal	January 1996
Microbial metabolic exchange in 3D Watrous, Jeramie D.; Phelan, Vanessa V.; Hsu, Cheng-Chih The ISME Journal, Vol. 7, Issue 4 https://doi.org/10.1038/ismej.2012.155	journal	January 2013
Experimental evolution of nodule intracellular infection in legume symbionts Guan, Su Hua; Gris, Carine; Cruveiller, Stéphane The ISME Journal, Vol. 7, Issue 7 https://doi.org/10.1038/ismej.2013.24	journal	February 2013
The Site of Oxygen Limitation in Soybean Nodules Kuzma, Monika M.; Winter, Heike; Storer, Paul Plant Physiology, Vol. 119, Issue 2 https://doi.org/10.1104/pp.119.2.399	journal	February 1999
Phosphatidylcholine levels in Bradyrhizobium japonicum membranes are critical for an efficient symbiosis with the soybean host plant: Phosphatidylcholine biosynthesis in Bradyrhizobium japonicum Minder, Alexander C.; De Rudder, Karel E. E.; Narberhaus, Franz Molecular Microbiology, Vol. 39, Issue 5 https://doi.org/10.1111/j.1365-2958.2001.02325.x	journal	March 2001
MALDI mass spectrometry-assisted molecular imaging of metabolites during nitrogen fixation in the Medicago truncatula - Sinorhizobium meliloti symbiosis Ye, Hui; Gemperline, Erin; Venkateshwaran, Muthusubramanian The Plant Journal, Vol. 75, Issue 1 https://doi.org/10.1111/tpj.12191	journal	May 2013
Laser-ablation electrospray ionization mass spectrometry with ion mobility separation reveals metabolites in the symbiotic interactions of soybean roots and rhizobia Stopka, Sylwia A.; Agtuca, Beverly J.; Koppenaal, David W. The Plant Journal, Vol. 91, Issue 2 https://doi.org/10.1111/tpj.13569	journal	May 2017
Leghemoglobin and Rhizobium Respiration Appleby, C. A. Annual Review of Plant Physiology, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.pp.35.060184.002303	journal	June 1984
Involvement of polyamines in the root nodule regulation of soybeans (Glycine max) Terakado-Tonooka, Junko; Fujihara, Shinsuke Plant Root, Vol. 2 https://doi.org/10.3117/plantroot.2.46	journal	January 2008

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Observed metabolic asymmetry within soybean root nodules reflects unexpected complexity in rhizobacteria-legume metabolite exchange

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