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Title: Integrated Proteomics and Metabolomics Suggests Symbiotic Metabolism and Multimodal Regulation in a Fungal-Endobacterial System: Symbiotic Metabolism and Multimodal Regulation

Abstract

Many plant-associated fungi host endosymbiotic endobacteria with reduced genomes. While endobacteria play important roles in these tri-partite plant-fungal-endobacterial systems, the active physiology of fungal endobacteria has not been characterized extensively by systems biology approaches. Here in this paper, we use integrated proteomics and metabolomics to characterize the relationship between the endobacterium Mycoavidus sp. and the root-associated fungus Mortierella elongata. In nitrogen-poor media, M. elongata had decreased growth but hosted a large and growing endobacterial population. The active endobacterium likely extracted malate from the fungal host as the primary carbon substrate for energy production and biosynthesis of phospho-sugars, nucleobases, peptidoglycan, and some amino acids. The endobacterium obtained nitrogen by importing a variety of nitrogen-containing compounds. Further, nitrogen limitation significantly perturbed the carbon and nitrogen flows in the fungal metabolic network. M. elongata regulated many pathways by concordant changes on enzyme abundances, post-translational modifications, reactant concentrations, and allosteric effectors. Lastly, such multimodal regulations may be a general mechanism for metabolic modulation.

Authors:
 [1];  [1];  [2];  [3];  [2];  [4];  [4];  [1];  [2];  [1];  [1]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  2. Univ. of Tennessee, Knoxville, TN (United States)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of Tennessee, Knoxville, TN (United States)
  4. Duke Univ., Durham, NC (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1339384
Alternate Identifier(s):
OSTI ID: 1399551
Grant/Contract Number:  
AC05-00OR22725; SC10010566
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 12; Journal Issue: 1; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; proteomics; metabolomics; fungus; endobacterium; symbiotic metabolism; multimodal regulation

Citation Formats

Li, Zhou, Yao, Qiuming, Dearth, Stephen P., Entler, Matthew R., Castro Gonzalez, Hector F., Uehling, Jessie K., Vilgalys, Rytas J., Hurst, Gregory B., Campagna, Shawn R., Labbé, Jessy L., and Pan, Chongle. Integrated Proteomics and Metabolomics Suggests Symbiotic Metabolism and Multimodal Regulation in a Fungal-Endobacterial System: Symbiotic Metabolism and Multimodal Regulation. United States: N. p., 2016. Web. doi:10.1111/1462-2920.13605.
Li, Zhou, Yao, Qiuming, Dearth, Stephen P., Entler, Matthew R., Castro Gonzalez, Hector F., Uehling, Jessie K., Vilgalys, Rytas J., Hurst, Gregory B., Campagna, Shawn R., Labbé, Jessy L., & Pan, Chongle. Integrated Proteomics and Metabolomics Suggests Symbiotic Metabolism and Multimodal Regulation in a Fungal-Endobacterial System: Symbiotic Metabolism and Multimodal Regulation. United States. doi:10.1111/1462-2920.13605.
Li, Zhou, Yao, Qiuming, Dearth, Stephen P., Entler, Matthew R., Castro Gonzalez, Hector F., Uehling, Jessie K., Vilgalys, Rytas J., Hurst, Gregory B., Campagna, Shawn R., Labbé, Jessy L., and Pan, Chongle. Mon . "Integrated Proteomics and Metabolomics Suggests Symbiotic Metabolism and Multimodal Regulation in a Fungal-Endobacterial System: Symbiotic Metabolism and Multimodal Regulation". United States. doi:10.1111/1462-2920.13605. https://www.osti.gov/servlets/purl/1339384.
@article{osti_1339384,
title = {Integrated Proteomics and Metabolomics Suggests Symbiotic Metabolism and Multimodal Regulation in a Fungal-Endobacterial System: Symbiotic Metabolism and Multimodal Regulation},
author = {Li, Zhou and Yao, Qiuming and Dearth, Stephen P. and Entler, Matthew R. and Castro Gonzalez, Hector F. and Uehling, Jessie K. and Vilgalys, Rytas J. and Hurst, Gregory B. and Campagna, Shawn R. and Labbé, Jessy L. and Pan, Chongle},
abstractNote = {Many plant-associated fungi host endosymbiotic endobacteria with reduced genomes. While endobacteria play important roles in these tri-partite plant-fungal-endobacterial systems, the active physiology of fungal endobacteria has not been characterized extensively by systems biology approaches. Here in this paper, we use integrated proteomics and metabolomics to characterize the relationship between the endobacterium Mycoavidus sp. and the root-associated fungus Mortierella elongata. In nitrogen-poor media, M. elongata had decreased growth but hosted a large and growing endobacterial population. The active endobacterium likely extracted malate from the fungal host as the primary carbon substrate for energy production and biosynthesis of phospho-sugars, nucleobases, peptidoglycan, and some amino acids. The endobacterium obtained nitrogen by importing a variety of nitrogen-containing compounds. Further, nitrogen limitation significantly perturbed the carbon and nitrogen flows in the fungal metabolic network. M. elongata regulated many pathways by concordant changes on enzyme abundances, post-translational modifications, reactant concentrations, and allosteric effectors. Lastly, such multimodal regulations may be a general mechanism for metabolic modulation.},
doi = {10.1111/1462-2920.13605},
journal = {Environmental Microbiology},
number = 1,
volume = 12,
place = {United States},
year = {Mon Nov 21 00:00:00 EST 2016},
month = {Mon Nov 21 00:00:00 EST 2016}
}

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