In Situ Detection of Amino Acids from Bacterial Biofilms and Plant Root Exudates by Liquid Microjunction Surface-Sampling Probe Mass Spectrometry
Abstract
The plant rhizosphere is a complex and dynamic chemical environment where the exchange of molecular signals between plants, microbes, and fungi drives the development of the entire biological system. Exogenous compounds in the rhizosphere are known to affect plant-microbe organization, interactions between organisms, and ultimately, growth and survivability. The function of exogenous compounds in the rhizosphere is still under much investigation, specifically with respect to their roles in plant growth and development, the assembly of the associated microbial community, and the spatiotemporal distribution of molecular components. A major challenge for spatiotemporal measurements is developing a nondisruptive and nondestructive technique capable of analyzing the exogenous compounds contained within the environment. A methodology using liquid microjunction-surface sampling probe-mass spectrometry (LMJ-SSP-MS) and microfluidic devices with attached microporous membranes was developed for in situ, spatiotemporal measurement of amino acids (AAs) from bacterial biofilms and plant roots. Exuded arginine was measured from a living Pantoea YR343 biofilm, which resulted in a chemical image indicative of biofilm growth within the device. Spot sampling along the roots of Populus trichocarpa with the LMJ-SSP-MS resulted in the detection of 15 AAs. Of note, variation in AA concentrations across the root system was observed, indicating that exudation is notmore »
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1883896
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Journal of the American Society for Mass Spectrometry
- Additional Journal Information:
- Journal Volume: 33; Journal Issue: 9; Journal ID: ISSN 1044-0305
- Publisher:
- American Society for Mass Spectrometry
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; biofilms; computer simulations; membranes; microfluidic devices; plants
Citation Formats
Walton, Courtney L., Khalid, Muneeba, Bible, Amber N., Kertesz, Vilmos, Retterer, Scott T., Morrell-Falvey, Jennifer, and Cahill, John F. In Situ Detection of Amino Acids from Bacterial Biofilms and Plant Root Exudates by Liquid Microjunction Surface-Sampling Probe Mass Spectrometry. United States: N. p., 2022.
Web. doi:10.1021/jasms.2c00081.
Walton, Courtney L., Khalid, Muneeba, Bible, Amber N., Kertesz, Vilmos, Retterer, Scott T., Morrell-Falvey, Jennifer, & Cahill, John F. In Situ Detection of Amino Acids from Bacterial Biofilms and Plant Root Exudates by Liquid Microjunction Surface-Sampling Probe Mass Spectrometry. United States. https://doi.org/10.1021/jasms.2c00081
Walton, Courtney L., Khalid, Muneeba, Bible, Amber N., Kertesz, Vilmos, Retterer, Scott T., Morrell-Falvey, Jennifer, and Cahill, John F. Fri .
"In Situ Detection of Amino Acids from Bacterial Biofilms and Plant Root Exudates by Liquid Microjunction Surface-Sampling Probe Mass Spectrometry". United States. https://doi.org/10.1021/jasms.2c00081. https://www.osti.gov/servlets/purl/1883896.
@article{osti_1883896,
title = {In Situ Detection of Amino Acids from Bacterial Biofilms and Plant Root Exudates by Liquid Microjunction Surface-Sampling Probe Mass Spectrometry},
author = {Walton, Courtney L. and Khalid, Muneeba and Bible, Amber N. and Kertesz, Vilmos and Retterer, Scott T. and Morrell-Falvey, Jennifer and Cahill, John F.},
abstractNote = {The plant rhizosphere is a complex and dynamic chemical environment where the exchange of molecular signals between plants, microbes, and fungi drives the development of the entire biological system. Exogenous compounds in the rhizosphere are known to affect plant-microbe organization, interactions between organisms, and ultimately, growth and survivability. The function of exogenous compounds in the rhizosphere is still under much investigation, specifically with respect to their roles in plant growth and development, the assembly of the associated microbial community, and the spatiotemporal distribution of molecular components. A major challenge for spatiotemporal measurements is developing a nondisruptive and nondestructive technique capable of analyzing the exogenous compounds contained within the environment. A methodology using liquid microjunction-surface sampling probe-mass spectrometry (LMJ-SSP-MS) and microfluidic devices with attached microporous membranes was developed for in situ, spatiotemporal measurement of amino acids (AAs) from bacterial biofilms and plant roots. Exuded arginine was measured from a living Pantoea YR343 biofilm, which resulted in a chemical image indicative of biofilm growth within the device. Spot sampling along the roots of Populus trichocarpa with the LMJ-SSP-MS resulted in the detection of 15 AAs. Of note, variation in AA concentrations across the root system was observed, indicating that exudation is not homogeneous and may be linked to local rhizosphere architecture and different biological processes along the root.},
doi = {10.1021/jasms.2c00081},
journal = {Journal of the American Society for Mass Spectrometry},
number = 9,
volume = 33,
place = {United States},
year = {Fri Jul 29 00:00:00 EDT 2022},
month = {Fri Jul 29 00:00:00 EDT 2022}
}
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Works referenced in this record:
Stimulating the In Situ Activity of Geobacter Species To Remove Uranium from the Groundwater of a Uranium-Contaminated Aquifer
journal, October 2003
- Anderson, R. T.; Vrionis, H. A.; Ortiz-Bernad, I.
- Applied and Environmental Microbiology, Vol. 69, Issue 10
Effect of shear stress on the formation of bacterial biofilm in a microfluidic channel
journal, September 2011
- Park, Aeri; Jeong, Heon-Ho; Lee, Jintae
- BioChip Journal, Vol. 5, Issue 3
Evolution of the amino acid fingerprint in the unsterilized rhizosphere of a legume in relation to plant maturity
journal, October 2016
- Bobille, Hélène; Limami, Anis M.; Robins, Richard J.
- Soil Biology and Biochemistry, Vol. 101
Metabolic Profiling Directly from the Petri Dish Using Nanospray Desorption Electrospray Ionization Imaging Mass Spectrometry
journal, October 2013
- Watrous, Jeramie; Roach, Patrick; Heath, Brandi
- Analytical Chemistry, Vol. 85, Issue 21, p. 10385-10391
Use of MALDI-TOF mass spectrometry to analyze the molecular profile of Pseudomonas aeruginosa biofilms grown on glass and plastic surfaces
journal, September 2015
- Pereira, Flávio D. E. S.; Bonatto, Cínthia C.; Lopes, Cláudio A. P.
- Microbial Pathogenesis, Vol. 86
Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly
journal, March 2018
- Zhalnina, Kateryna; Louie, Katherine B.; Hao, Zhao
- Nature Microbiology, Vol. 3, Issue 4
Strategies and methods for studying the rhizosphere—the plant science toolbox
journal, April 2009
- Neumann, Günter; George, Timothy S.; Plassard, Claude
- Plant and Soil, Vol. 321, Issue 1-2
Rapid in situ detection of alkaloids in plant tissue under ambient conditions using desorption electrospray ionization
journal, January 2005
- Talaty, Nari; Takáts, Zoltán; Cooks, R. Graham
- The Analyst, Vol. 130, Issue 12
AraCyc: A Biochemical Pathway Database for Arabidopsis
journal, June 2003
- Mueller, Lukas A.; Zhang, Peifen; Rhee, Seung Y.
- Plant Physiology, Vol. 132, Issue 2
A Carotenoid-Deficient Mutant in Pantoea sp. YR343, a Bacteria Isolated from the Rhizosphere of Populus deltoides, Is Defective in Root Colonization
journal, April 2016
- Bible, Amber N.; Fletcher, Sarah J.; Pelletier, Dale A.
- Frontiers in Microbiology, Vol. 7
Mass Spectrometry Imaging of Complex Microbial Communities
journal, December 2016
- Dunham, Sage J. B.; Ellis, Joseph F.; Li, Bin
- Accounts of Chemical Research, Vol. 50, Issue 1
Amino-acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere
journal, June 1994
- Jones, D. L.; Darrah, P. R.
- Plant and Soil, Vol. 163, Issue 1
Spatially resolved analysis of glycolipids and metabolites in living Synechococcus sp. PCC 7002 using nanospray desorption electrospray ionization
journal, January 2013
- Lanekoff, Ingela; Geydebrekht, Oleg; Pinchuk, Grigoriy E.
- The Analyst, Vol. 138, Issue 7
Characterization of Indole-3-acetic Acid Biosynthesis and the Effects of This Phytohormone on the Proteome of the Plant-Associated Microbe Pantoea sp. YR343
journal, February 2018
- Estenson, Kasey; Hurst, Gregory B.; Standaert, Robert F.
- Journal of Proteome Research, Vol. 17, Issue 4
Investigation of organic anions in tree root exudates and rhizosphere microbial communities using in situ and destructive sampling techniques
journal, March 2012
- Shi, Shengjing; O’Callaghan, Maureen; Jones, E. Eirian
- Plant and Soil, Vol. 359, Issue 1-2
Corrigendum: Root Exudation of Primary Metabolites: Mechanisms and Their Roles in Plant Responses to Environmental Stimuli
journal, April 2019
- Canarini, Alberto; Kaiser, Christina; Merchant, Andrew
- Frontiers in Plant Science, Vol. 10
Spatially resolved in vivo plant metabolomics by laser ablation-based mass spectrometry imaging (MSI) techniques: LDI-MSI and LAESI
journal, July 2015
- Bartels, Benjamin; Svatoš, Aleš
- Frontiers in Plant Science, Vol. 6
Hydrodynamic effects on bacterial biofilm development in a microfluidic environment
journal, January 2013
- Kim, Junghyun; Kim, Han-Shin; Han, Sewoon
- Lab on a Chip, Vol. 13, Issue 10
Integrated omics approaches in plant systems biology
journal, December 2009
- Fukushima, Atsushi; Kusano, Miyako; Redestig, Henning
- Current Opinion in Chemical Biology, Vol. 13, Issue 5-6
Development of a relative quantification method for infrared matrix‐assisted laser desorption electrospray ionization mass spectrometry imaging of
Arabidopsis
seedlings
journal, February 2020
- Bagley, M. Caleb; Stepanova, Anna N.; Ekelöf, Måns
- Rapid Communications in Mass Spectrometry, Vol. 34, Issue 6
Advances in Imaging Secondary Ion Mass Spectrometry for Biological Samples
journal, June 2009
- Boxer, Steven G.; Kraft, Mary L.; Weber, Peter K.
- Annual Review of Biophysics, Vol. 38, Issue 1
Exometabolite niche partitioning among sympatric soil bacteria
journal, September 2015
- Baran, Richard; Brodie, Eoin L.; Mayberry-Lewis, Jazmine
- Nature Communications, Vol. 6, Issue 1
Molecular communication in the rhizosphere
journal, December 2008
- Faure, Denis; Vereecke, Danny; Leveau, Johan H. J.
- Plant and Soil, Vol. 321, Issue 1-2
The role of root Exudates in Rhizosphere Interactions with Plants and Other Organisms
journal, June 2006
- Bais, Harsh P.; Weir, Tiffany L.; Perry, Laura G.
- Annual Review of Plant Biology, Vol. 57, Issue 1
Role of sdhA and pfkA and catabolism of reduced carbon during colonization of cucumber roots by Enterobacter cloacae
journal, September 2007
- Liu, Shengyi; Hu, Xiaojia; Lohrke, Scott M.
- Microbiology, Vol. 153, Issue 9
Mass spectrometry imaging for plant biology: a review
journal, October 2015
- Boughton, Berin A.; Thinagaran, Dinaiz; Sarabia, Daniel
- Phytochemistry Reviews, Vol. 15, Issue 3
Twenty-One Genome Sequences from Pseudomonas Species and 19 Genome Sequences from Diverse Bacteria Isolated from the Rhizosphere and Endosphere of Populus deltoides
journal, October 2012
- Brown, S. D.; Utturkar, S. M.; Klingeman, D. M.
- Journal of Bacteriology, Vol. 194, Issue 21
Plant–Microbe Interactions: From Genes to Ecosystems Using Populus as a Model System
journal, January 2021
- Cregger, Melissa A.; Carper, Dana L.; Christel, Stephan
- Phytobiomes Journal, Vol. 5, Issue 1
Label-free time- and space-resolved exometabolite sampling of growing plant roots through nanoporous interfaces
journal, July 2019
- Patabadige, Damith E. W.; Millet, Larry J.; Aufrecht, Jayde A.
- Scientific Reports, Vol. 9, Issue 1
Identification of a diguanylate cyclase expressed in the presence of plants and its application for discovering candidate gene products involved in plant colonization by Pantoea sp. YR343
journal, July 2021
- Bible, Amber N.; Chang, Mang; Morrell-Falvey, Jennifer L.
- PLOS ONE, Vol. 16, Issue 7
Regulation and function of root exudates
journal, June 2009
- Badri, Dayakar V.; Vivanco, Jorge M.
- Plant, Cell & Environment, Vol. 32, Issue 6
Two-dimensional and three-dimensional dynamic imaging of live biofilms in a microchannel by time-of-flight secondary ion mass spectrometry
journal, May 2015
- Hua, Xin; Marshall, Matthew J.; Xiong, Yijia
- Biomicrofluidics, Vol. 9, Issue 3
In Situ Chemical Monitoring and Imaging of Contents within Microfluidic Devices Having a Porous Membrane Wall Using Liquid Microjunction Surface Sampling Probe Mass Spectrometry
journal, February 2020
- Cahill, John F.; Khalid, Muneeba; Retterer, Scott T.
- Journal of the American Society for Mass Spectrometry, Vol. 31, Issue 4
Culture-Independent Molecular Tools for Soil and Rhizosphere Microbiology
journal, August 2013
- Rincon-Florez, Vivian; Carvalhais, Lilia; Schenk, Peer
- Diversity, Vol. 5, Issue 3
A critical review of labelling techniques used to quantify rhizosphere carbon-flow
journal, March 1994
- Meharg, Andrew A.
- Plant and Soil, Vol. 166, Issue 1
Liquid Microjunction Surface Sampling Probe Fluid Dynamics: Computational and Experimental Analysis of Coaxial Intercapillary Positioning Effects on Sample Manipulation
journal, April 2011
- ElNaggar, Mariam S.; Barbier, Charlotte; Van Berkel, Gary J.
- Journal of The American Society for Mass Spectrometry, Vol. 22, Issue 7
Spatiotemporal Monitoring of the Antibiome Secreted by Bacillus Biofilms on Plant Roots Using MALDI Mass Spectrometry Imaging
journal, April 2014
- Debois, Delphine; Jourdan, Emmanuel; Smargiasso, Nicolas
- Analytical Chemistry, Vol. 86, Issue 9
Foraging in the Dark – Chemically Mediated Host Plant Location by Belowground Insect Herbivores
journal, April 2012
- Johnson, Scott N.; Nielsen, Uffe N.
- Journal of Chemical Ecology, Vol. 38, Issue 6
New Methods To Unravel Rhizosphere Processes
journal, March 2016
- Oburger, Eva; Schmidt, Hannes
- Trends in Plant Science, Vol. 21, Issue 3
Real-Time Metabolomics on Living Microorganisms Using Ambient Electrospray Ionization Flow-Probe
journal, July 2013
- Hsu, Cheng-Chih; ElNaggar, Mariam S.; Peng, Yao
- Analytical Chemistry, Vol. 85, Issue 15
Mass spectrometry imaging of plant metabolites – principles and possibilities
journal, January 2014
- Bjarnholt, Nanna; Li, Bin; D'Alvise, Janina
- Nat. Prod. Rep., Vol. 31, Issue 6
Manipulating the soil microbiome to increase soil health and plant fertility
journal, May 2012
- Chaparro, Jacqueline M.; Sheflin, Amy M.; Manter, Daniel K.
- Biology and Fertility of Soils, Vol. 48, Issue 5
Analysis of Secondary Plant Metabolites by Indirect Desorption Electrospray Ionization Imaging Mass Spectrometry
journal, May 2011
- Thunig, Janina; Hansen, Steen H.; Janfelt, Christian
- Analytical Chemistry, Vol. 83, Issue 9
Quantifying the Spatiotemporal Dynamics of Plant Root Colonization by Beneficial Bacteria in a Microfluidic Habitat
journal, April 2018
- Aufrecht, Jayde A.; Timm, Collin M.; Bible, Amber
- Advanced Biosystems, Vol. 2, Issue 6
Direct Plant Tissue Analysis and Imprint Imaging by Desorption Electrospray Ionization Mass Spectrometry
journal, July 2011
- Müller, Thomas; Oradu, Sheran; Ifa, Demian R.
- Analytical Chemistry, Vol. 83, Issue 14
The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms
journal, September 2013
- Mendes, Rodrigo; Garbeva, Paolina; Raaijmakers, Jos M.
- FEMS Microbiology Reviews, Vol. 37, Issue 5
Pore-scale hydrodynamics influence the spatial evolution of bacterial biofilms in a microfluidic porous network
journal, June 2019
- Aufrecht, Jayde A.; Fowlkes, Jason D.; Bible, Amber N.
- PLOS ONE, Vol. 14, Issue 6
Hotspots of root-exuded amino acids are created within a rhizosphere-on-a-chip
journal, January 2022
- Aufrecht, Jayde; Khalid, Muneeba; Walton, Courtney L.
- Lab on a Chip, Vol. 22, Issue 5
Amino acids in the rhizosphere: From plants to microbes
journal, September 2013
- Moe, Luke A.
- American Journal of Botany, Vol. 100, Issue 9
Biofilm Formation by Plant-Associated Bacteria
journal, October 2007
- Danhorn, Thomas; Fuqua, Clay
- Annual Review of Microbiology, Vol. 61, Issue 1
Liquid microjunction surface sampling probe electrospray mass spectrometry for detection of drugs and metabolites in thin tissue sections
journal, April 2008
- Van Berkel, Gary J.; Kertesz, Vilmos; Koeplinger, Kenneth A.
- Journal of Mass Spectrometry, Vol. 43, Issue 4
High resolution mass spectrometry imaging of plant tissues: towards a plant metabolite atlas
journal, January 2015
- Bhandari, Dhaka Ram; Wang, Qing; Friedt, Wolfgang
- The Analyst, Vol. 140, Issue 22
Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review
journal, April 2011
- Doornbos, Rogier F.; van Loon, Leendert Cornelis; Bakker, Peter A. H. M.
- Agronomy for Sustainable Development, Vol. 32, Issue 1
Matrix assisted laser desorption/ionization-mass spectrometry imaging (MALDI-MSI) for direct visualization of plant metabolites in situ
journal, February 2016
- Sturtevant, Drew; Lee, Young-Jin; Chapman, Kent D.
- Current Opinion in Biotechnology, Vol. 37