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Title: Microfluidics and Metabolomics Reveal Symbiotic Bacterial–Fungal Interactions Between Mortierella elongata and Burkholderia Include Metabolite Exchange

Abstract

We identified two poplar (Populus sp.)-associated microbes, the fungus, Mortierella elongata strain AG77, and the bacterium, Burkholderia strain BT03, that mutually promote each other’s growth. Using culture assays in concert with a novel microfluidic device to generate time-lapse videos, we found growth specific media differing in pH and pre-conditioned by microbial growth led to increased fungal and bacterial growth rates. Coupling microfluidics and comparative metabolomics data results indicated that observed microbial growth stimulation involves metabolic exchange during two ordered events. The first is an emission of fungal metabolites, including organic acids used or modified by bacteria. A second signal of unknown nature is produced by bacteria which increases fungal growth rates. We find this symbiosis is initiated in part by metabolic exchange involving fungal organic acids.

Authors:
 [1];  [2];  [3];  [4];  [2];  [2];  [5];  [2];  [6];  [7];  [8];  [9];  [10];  [2];  [11]
  1. Oregon State Univ., Corvallis, OR (United States). Dept. of Botany and Plant Pathology; Duke Univ., Durham, NC (United States). Dept. of Biology
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  3. Johns Hopkins Bloomberg School of Public Health, Baltimore, MD (United States). Dept. of Epidemiology; Duke Univ., Durham, NC (United States). Dept. of Biomedical Engineering
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). The Bredesen Center
  5. Michigan State Univ., East Lansing, MI (United States). Dept. of Plant, Soil and Microbial Sciences
  6. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Genome Science & Technology
  7. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). Genome Science & Technology; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Nanophase Materials Sciences
  8. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Nanophase Materials Sciences
  9. Oregon State Univ., Corvallis, OR (United States). Dept. of Botany and Plant Pathology
  10. Univ. of California, Riverside, CA (United States). Dept. of Microbiology and Plant Pathology, Inst. for Integrative Genome Biology
  11. Duke Univ., Durham, NC (United States). Dept. of Biology
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:
1569368
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; bacterial-fungal interactions; microfluidics; metabolomics; fatty acid; symbiotic evolution; Mortierella elongata; Burkholderia; plant associated microbes

Citation Formats

Uehling, Jessie K., Entler, Matthew R., Meredith, Hannah R., Millet, Larry J., Timm, Collin M., Aufrecht, Jayde A., Bonito, Gregory M., Engle, Nancy L., Labbé, Jessy L., Doktycz, Mitchel J., Retterer, Scott T., Spatafora, Joseph W., Stajich, Jason E., Tschaplinski, Timothy J., and Vilgalys, Rytas J. Microfluidics and Metabolomics Reveal Symbiotic Bacterial–Fungal Interactions Between Mortierella elongata and Burkholderia Include Metabolite Exchange. United States: N. p., 2019. Web. doi:10.3389/fmicb.2019.02163.
Uehling, Jessie K., Entler, Matthew R., Meredith, Hannah R., Millet, Larry J., Timm, Collin M., Aufrecht, Jayde A., Bonito, Gregory M., Engle, Nancy L., Labbé, Jessy L., Doktycz, Mitchel J., Retterer, Scott T., Spatafora, Joseph W., Stajich, Jason E., Tschaplinski, Timothy J., & Vilgalys, Rytas J. Microfluidics and Metabolomics Reveal Symbiotic Bacterial–Fungal Interactions Between Mortierella elongata and Burkholderia Include Metabolite Exchange. United States. doi:10.3389/fmicb.2019.02163.
Uehling, Jessie K., Entler, Matthew R., Meredith, Hannah R., Millet, Larry J., Timm, Collin M., Aufrecht, Jayde A., Bonito, Gregory M., Engle, Nancy L., Labbé, Jessy L., Doktycz, Mitchel J., Retterer, Scott T., Spatafora, Joseph W., Stajich, Jason E., Tschaplinski, Timothy J., and Vilgalys, Rytas J. Tue . "Microfluidics and Metabolomics Reveal Symbiotic Bacterial–Fungal Interactions Between Mortierella elongata and Burkholderia Include Metabolite Exchange". United States. doi:10.3389/fmicb.2019.02163. https://www.osti.gov/servlets/purl/1569368.
@article{osti_1569368,
title = {Microfluidics and Metabolomics Reveal Symbiotic Bacterial–Fungal Interactions Between Mortierella elongata and Burkholderia Include Metabolite Exchange},
author = {Uehling, Jessie K. and Entler, Matthew R. and Meredith, Hannah R. and Millet, Larry J. and Timm, Collin M. and Aufrecht, Jayde A. and Bonito, Gregory M. and Engle, Nancy L. and Labbé, Jessy L. and Doktycz, Mitchel J. and Retterer, Scott T. and Spatafora, Joseph W. and Stajich, Jason E. and Tschaplinski, Timothy J. and Vilgalys, Rytas J.},
abstractNote = {We identified two poplar (Populus sp.)-associated microbes, the fungus, Mortierella elongata strain AG77, and the bacterium, Burkholderia strain BT03, that mutually promote each other’s growth. Using culture assays in concert with a novel microfluidic device to generate time-lapse videos, we found growth specific media differing in pH and pre-conditioned by microbial growth led to increased fungal and bacterial growth rates. Coupling microfluidics and comparative metabolomics data results indicated that observed microbial growth stimulation involves metabolic exchange during two ordered events. The first is an emission of fungal metabolites, including organic acids used or modified by bacteria. A second signal of unknown nature is produced by bacteria which increases fungal growth rates. We find this symbiosis is initiated in part by metabolic exchange involving fungal organic acids.},
doi = {10.3389/fmicb.2019.02163},
journal = {Frontiers in Microbiology},
number = 1,
volume = 10,
place = {United States},
year = {2019},
month = {10}
}

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Figures / Tables:

FIGURE 1 FIGURE 1: M. elongata and Burkholderia co-culture experiments and radial growth rate data from plate-based co-culture experiments. Experiments performed on malt extract agar (MEA, dark) and P20 (light) media. In each image, the perimeter of the fungal colony is outlined in black. (A) M. elongata grown in monoculture and co-culturemore » with Burkholderia on solid P20 and MEA media. (B) Radial growth rates in mm/day. Box plots correspond to plate images above from left to right for M. elongata without and with Burkholderia on P20 and MEA media. ***$p$ < 0.005, Student’s t-tests.« less

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