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

Jessie K. Uehling; Matthew R. Entler; Hannah R. Meredith; Larry J. Millet; Collin M. Timm; Jayde A. Aufrecht; Gregory M. Bonito; Nancy L. Engle; Jessy L. Labbé; Mitchel J. Doktycz; Scott T. Retterer; Joseph W. Spatafora; Jason E. Stajich; Timothy J. Tschaplinski; Rytas J. Vilgalys

doi:10.3389/fmicb.2019.02163

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

Jessie K. Uehling, Matthew R. Entler, Hannah R. Meredith, Larry J. Millet, Collin M. Timm, Jayde A. Aufrecht, Gregory M. Bonito, Nancy L. Engle, Jessy L. Labbé, Mitchel J. Doktycz, Scott T. Retterer, Joseph W. Spatafora, Jason E. Stajich, Timothy J. Tschaplinski, Rytas J. Vilgalys

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38 Scopus citations

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.

Original language	English
Article number	2163
Journal	Frontiers in Microbiology
Volume	10
DOIs	https://doi.org/10.3389/fmicb.2019.02163
State	Published - Oct 1 2019

Funding

Funding. This work was supported in part by the Genomic Science Program, U.S. Department of Energy, Office of Science, Biological and Environmental Research, as part of the Plant Microbe Interfaces Scientific Focus Area (http://pmi.ornl.gov). This manuscript has been co-authored by UT-Battelle, LLC under Contract No. DE-AC05-00OR22725 with the U.S. Department of Energy. The fabrication of the microfluidic devices was carried out in the Nanofabrication Research Laboratory at the Center for Nanophase Materials Sciences, which is a DOE Office of Science User Facility under CNMS grant CNMS2015-308. GB acknowledges support from the National Science Foundation (NSF) DEB1737898. The Zygomycetes Genealogy of Life (ZyGoLife) Project supported JU, JES, and RV with NSF DEB-1441715 and JWS was supported by DEB-1441604.

Keywords

Burkholderia
Mortierella elongata
bacterial–fungal interactions
fatty acid
metabolomics
microfluidics
plant associated microbes
symbiotic evolution

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10.3389/fmicb.2019.02163

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Uehling, J. K., Entler, M. R., Meredith, H. R., Millet, L. J., Timm, C. M., Aufrecht, J. A., Bonito, G. M., Engle, N. L., Labbé, J. L., Doktycz, M. J., Retterer, S. T., Spatafora, J. W., Stajich, J. E., Tschaplinski, T. J., & Vilgalys, R. J. (2019). Microfluidics and Metabolomics Reveal Symbiotic Bacterial–Fungal Interactions Between Mortierella elongata and Burkholderia Include Metabolite Exchange. Frontiers in Microbiology, 10, Article 2163. https://doi.org/10.3389/fmicb.2019.02163

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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{\textquoteright}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.",

keywords = "Burkholderia, Mortierella elongata, bacterial–fungal interactions, fatty acid, metabolomics, microfluidics, plant associated microbes, symbiotic evolution",

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 Labb{\'e}, \{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.\}",

note = "Publisher Copyright: {\textcopyright} Copyright {\textcopyright} 2019 Uehling, Entler, Meredith, Millet, Timm, Aufrecht, Bonito, Engle, Labb{\'e}, Doktycz, Retterer, Spatafora, Stajich, Tschaplinski and Vilgalys.",

year = "2019",

month = oct,

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doi = "10.3389/fmicb.2019.02163",

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Uehling, JK, Entler, MR, Meredith, HR, Millet, LJ, Timm, CM, Aufrecht, JA, Bonito, GM, Engle, NL, Labbé, JL, Doktycz, MJ , Retterer, ST, Spatafora, JW, Stajich, JE, Tschaplinski, TJ & Vilgalys, RJ 2019, 'Microfluidics and Metabolomics Reveal Symbiotic Bacterial–Fungal Interactions Between Mortierella elongata and Burkholderia Include Metabolite Exchange', Frontiers in Microbiology, vol. 10, 2163. https://doi.org/10.3389/fmicb.2019.02163

TY - JOUR

T1 - Microfluidics and Metabolomics Reveal Symbiotic Bacterial–Fungal Interactions Between Mortierella elongata and Burkholderia Include Metabolite Exchange

AU - Uehling, Jessie K.

AU - Entler, Matthew R.

AU - Meredith, Hannah R.

AU - Millet, Larry J.

AU - Timm, Collin M.

AU - Aufrecht, Jayde A.

AU - Bonito, Gregory M.

AU - Engle, Nancy L.

AU - Labbé, Jessy L.

AU - Doktycz, Mitchel J.

AU - Retterer, Scott T.

AU - Spatafora, Joseph W.

AU - Stajich, Jason E.

AU - Tschaplinski, Timothy J.

AU - Vilgalys, Rytas J.

PY - 2019/10/1

Y1 - 2019/10/1

N2 - 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.

AB - 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.

KW - Burkholderia

KW - Mortierella elongata

KW - bacterial–fungal interactions

KW - fatty acid

KW - metabolomics

KW - microfluidics

KW - plant associated microbes

KW - symbiotic evolution

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VL - 10

JO - Frontiers in Microbiology

JF - Frontiers in Microbiology

M1 - 2163

ER -

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

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