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Title: Untargeted metabolomics studies employing NMR and LC–MS reveal metabolic coupling between Nanoarcheum equitans and its archaeal host Ignicoccus hospitalis

Abstract

Interactions between species are the basis of microbial community formation and infectious diseases. Systems biology enables the construction of complex models describing such interactions, leading to a better understanding of disease states and communities. However, before interactions between complex organisms can be understood, metabolic and energetic implications of simpler real-world host-microbe systems must be worked out. To this effect, untargeted metabolomics experiments were conducted and integrated with proteomics data to characterize key molecular-level interactions between two hyperthermophilic microbial species, both of which have reduced genomes. Metabolic changes and transfer of metabolites between the archaea Ignicoccus hospitalis and Nanoarcheum equitans were investigated using integrated LC–MS and NMR metabolomics. The study of such a system is challenging, as no genetic tools are available, growth in the laboratory is challenging, and mechanisms by which they interact are unknown. Together with information about relative enzyme levels obtained from shotgun proteomics, the metabolomics data provided useful insights into metabolic pathways and cellular networks of I. hospitalis that are impacted by the presence of N. equitans, including arginine, isoleucine, and CTP biosynthesis. On the organismal level, the data indicate that N. equitans exploits metabolites generated by I. hospitalis to satisfy its own metabolic needs. Lastly, thismore » finding is based on N. equitans’s consumption of a significant fraction of the metabolite pool in I. hospitalis that cannot solely be attributed to increased biomass production for N. equitans. Combining LC–MS and NMR metabolomics datasets improved coverage of the metabolome and enhanced the identification and quantitation of cellular metabolites.« less

Authors:
 [1];  [1];  [1];  [2];  [3];  [2];  [3];  [4];  [5]
+ Show Author Affiliations
  1. Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Microbiology
  4. Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry; Montana State Univ., Bozeman, MT (United States). Thermal Biology Inst.
  5. Montana State Univ., Bozeman, MT (United States). Dept. of Chemistry and Biochemistry; Montana State Univ., Bozeman, MT (United States). Thermal Biology Inst.
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:
1286759
Grant/Contract Number:  
AC05-00OR22725; SC0006654; 1S10-RR13878-01; 1S10-RR026659-01; 5P20RR02437
Resource Type:
Accepted Manuscript
Journal Name:
Metabolomics
Additional Journal Information:
Journal Volume: 11; Journal Issue: 4; Journal ID: ISSN 1573-3882
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; LC–MS and NMR; Metabolomics; Ignicoccus hospitalis-Nanoarcheum equitans; Interspecies interactions; Hyperthermophilic archea; Systems biology

Citation Formats

Hamerly, Timothy, Tripet, Brian P., Tigges, Michelle, Giannone, Richard J., Wurch, Louie, Hettich, Robert L., Podar, Mircea, Copié, Valerie, and Bothner, Brian. Untargeted metabolomics studies employing NMR and LC–MS reveal metabolic coupling between Nanoarcheum equitans and its archaeal host Ignicoccus hospitalis. United States: N. p., 2014. Web. doi:10.1007/s11306-014-0747-6.
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Hamerly, Timothy, Tripet, Brian P., Tigges, Michelle, Giannone, Richard J., Wurch, Louie, Hettich, Robert L., Podar, Mircea, Copié, Valerie, & Bothner, Brian. Untargeted metabolomics studies employing NMR and LC–MS reveal metabolic coupling between Nanoarcheum equitans and its archaeal host Ignicoccus hospitalis. United States. https://doi.org/10.1007/s11306-014-0747-6
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Hamerly, Timothy, Tripet, Brian P., Tigges, Michelle, Giannone, Richard J., Wurch, Louie, Hettich, Robert L., Podar, Mircea, Copié, Valerie, and Bothner, Brian. Wed . "Untargeted metabolomics studies employing NMR and LC–MS reveal metabolic coupling between Nanoarcheum equitans and its archaeal host Ignicoccus hospitalis". United States. https://doi.org/10.1007/s11306-014-0747-6. https://www.osti.gov/servlets/purl/1286759.
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@article{osti_1286759,
title = {Untargeted metabolomics studies employing NMR and LC–MS reveal metabolic coupling between Nanoarcheum equitans and its archaeal host Ignicoccus hospitalis},
author = {Hamerly, Timothy and Tripet, Brian P. and Tigges, Michelle and Giannone, Richard J. and Wurch, Louie and Hettich, Robert L. and Podar, Mircea and Copié, Valerie and Bothner, Brian},
abstractNote = {Interactions between species are the basis of microbial community formation and infectious diseases. Systems biology enables the construction of complex models describing such interactions, leading to a better understanding of disease states and communities. However, before interactions between complex organisms can be understood, metabolic and energetic implications of simpler real-world host-microbe systems must be worked out. To this effect, untargeted metabolomics experiments were conducted and integrated with proteomics data to characterize key molecular-level interactions between two hyperthermophilic microbial species, both of which have reduced genomes. Metabolic changes and transfer of metabolites between the archaea Ignicoccus hospitalis and Nanoarcheum equitans were investigated using integrated LC–MS and NMR metabolomics. The study of such a system is challenging, as no genetic tools are available, growth in the laboratory is challenging, and mechanisms by which they interact are unknown. Together with information about relative enzyme levels obtained from shotgun proteomics, the metabolomics data provided useful insights into metabolic pathways and cellular networks of I. hospitalis that are impacted by the presence of N. equitans, including arginine, isoleucine, and CTP biosynthesis. On the organismal level, the data indicate that N. equitans exploits metabolites generated by I. hospitalis to satisfy its own metabolic needs. Lastly, this finding is based on N. equitans’s consumption of a significant fraction of the metabolite pool in I. hospitalis that cannot solely be attributed to increased biomass production for N. equitans. Combining LC–MS and NMR metabolomics datasets improved coverage of the metabolome and enhanced the identification and quantitation of cellular metabolites.},
doi = {10.1007/s11306-014-0747-6},
journal = {Metabolomics},
number = 4,
volume = 11,
place = {United States},
year = {Wed Nov 05 00:00:00 EST 2014},
month = {Wed Nov 05 00:00:00 EST 2014}
}
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Publisher's Version of Record
https://doi.org/10.1007/s11306-014-0747-6
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    Works referencing / citing this record:

    1H NMR metabolomic study of auxotrophic starvation in yeast using Multivariate Curve Resolution-Alternating Least Squares for Pathway Analysis
    journal, August 2016

    • Puig-Castellví, Francesc; Alfonso, Ignacio; Piña, Benjamin
    • Scientific Reports, Vol. 6, Issue 1
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    Genomic diversity, lifestyles and evolutionary origins of DPANN archaea
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    • Dombrowski, Nina; Lee, Jun-Hoe; Williams, Tom A.
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    Evaluation of extraction solvents for untargeted metabolomics analysis of enrichment reactor cultures performing enhanced biological phosphorus removal (EBPR)
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    • Thaw Saw, Nay Min Min; Suwanchaikasem, Pipob; Zuniga-Montanez, Rogelio
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    Conceptual Model of Biofilm Antibiotic Tolerance That Integrates Phenomena of Diffusion, Metabolism, Gene Expression, and Physiology
    journal, September 2019

    • Stewart, Philip S.; White, Ben; Boegli, Laura
    • Journal of Bacteriology, Vol. 201, Issue 22
    • DOI: 10.1128/jb.00307-19

    Single-cell genomics of co-sorted Nanoarchaeota suggests novel putative host associations and diversification of proteins involved in symbiosis
    journal, September 2018

    A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans
    journal, June 2017

    1H NMR metabolomic study of auxotrophic starvation in yeast using Multivariate Curve Resolution-Alternating Least Squares for Pathway Analysis
    journal, August 2016

    • Puig-Castellví, Francesc; Alfonso, Ignacio; Piña, Benjamin
    • Scientific Reports, Vol. 6, Issue 1
    • DOI: 10.1038/srep30982

    Genomic diversity, lifestyles and evolutionary origins of DPANN archaea
    journal, January 2019

    • Dombrowski, Nina; Lee, Jun-Hoe; Williams, Tom A.
    • FEMS Microbiology Letters, Vol. 366, Issue 2
    • DOI: 10.1093/femsle/fnz008

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    A Complex Endomembrane System in the Archaeon Ignicoccus hospitalis Tapped by Nanoarchaeum equitans
    journal, June 2017

    Metabolic Implications of Using BioOrthogonal Non-Canonical Amino Acid Tagging (BONCAT) for Tracking Protein Synthesis
    journal, February 2020

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