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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 Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
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. https://doi.org/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. https://doi.org/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 = {Tue Oct 01 00:00:00 EDT 2019},
month = {Tue Oct 01 00:00:00 EDT 2019}
}

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Cited by: 18 works
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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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Works referenced in this record:

Symbiosis and Insect Diversification: an Ancient Symbiont of Sap-Feeding Insects from the Bacterial Phylum Bacteroidetes
journal, December 2005


Relationship Between Host Acidification and Virulence of Penicillium spp. on Apple and Citrus Fruit
journal, January 2004


Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants
journal, June 2014

  • Bonito, Gregory; Reynolds, Hannah; Robeson, Michael S.
  • Molecular Ecology, Vol. 23, Issue 13
  • DOI: 10.1111/mec.12821

Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen
journal, January 2011


Combining microfluidics and RNA-sequencing to assess the inducible defensome of a mushroom against nematodes
text, January 2019


Bacterial endosymbionts influence host sexuality and reveal reproductive genes of early divergent fungi
journal, November 2017

  • Mondo, Stephen J.; Lastovetsky, Olga A.; Gaspar, Maria L.
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/s41467-017-02052-8

Microfluidics structures for probing the dynamic behaviour of filamentous fungi
journal, May 2010

  • Held, Marie; Lee, Abraham P.; Edwards, Clive
  • Microelectronic Engineering, Vol. 87, Issue 5-8
  • DOI: 10.1016/j.mee.2009.11.096

Extraction and quantification of ergosterol as a measure of fungal biomass in leaf litter
journal, December 1991

  • Gessner, Mark O.; Bauchrowitz, Martina A.; Escautier, Michèle
  • Microbial Ecology, Vol. 22, Issue 1
  • DOI: 10.1007/bf02540230

Mycoavidus cysteinexigens gen. nov., sp. nov., an endohyphal bacterium isolated from a soil isolate of the fungus Mortierella elongata
journal, May 2016

  • Nishizawa, Tomoyasu; Ohshima, Shoko; Hamada, Moriyuki
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 5
  • DOI: 10.1099/ijsem.0.000990

A Kinetic Study of the Growth of Aspergillus nidulans and Other Fungi
journal, July 1969


Detection of Betaproteobacteria inside the Mycelium of the Fungus Mortierella elongata
journal, January 2010

  • Sato, Yoshinori; Narisawa, Kazuhiko; Tsuruta, Kazuto
  • Microbes and Environments, Vol. 25, Issue 4
  • DOI: 10.1264/jsme2.me10134

Molecular Evolution in Bacterial Endosymbionts of Fungi
journal, November 2009

  • Castillo, D. M.; Pawlowska, T. E.
  • Molecular Biology and Evolution, Vol. 27, Issue 3
  • DOI: 10.1093/molbev/msp280

Role of secondary metabolites in the interaction between Pseudomonas fluorescens and soil microorganisms under iron-limited conditions
journal, May 2016

  • Deveau, Aurélie; Gross, Harald; Palin, Béatrice
  • FEMS Microbiology Ecology, Vol. 92, Issue 8
  • DOI: 10.1093/femsec/fiw107

'Candidatus Glomeribacter gigasporarum' gen. nov., sp. nov., an endosymbiont of arbuscular mycorrhizal fungi
journal, January 2003

  • Bianciotto, V.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 53, Issue 1
  • DOI: 10.1099/ijs.0.02382-0

The mycorrhiza helper bacteria revisited
journal, October 2007


Diversity and occurrence of Burkholderia spp. in the natural environment
journal, July 2008


Aldonic Acids: A Novel Family of nod Gene Inducers of Mesorhizobium loti, Rhizobium lupini , and Sinorhizobium meliloti
journal, October 1998


Mitochondrial Evolution
journal, March 1999


Pseudomonas-Candida Interactions: An Ecological Role for Virulence Factors
journal, June 2002


Polyphony in the rhizosphere: presymbiotic communication in arbuscular mycorrhizal symbiosis
journal, August 2013


The genome of the obligate endobacterium of an AM fungus reveals an interphylum network of nutritional interactions
journal, August 2011

  • Ghignone, Stefano; Salvioli, Alessandra; Anca, Iulia
  • The ISME Journal, Vol. 6, Issue 1
  • DOI: 10.1038/ismej.2011.110

Low-Volume Toolbox for the Discovery of Immunosuppressive Fungal Secondary Metabolites
journal, April 2013


Evolutionary Stability in a 400-Million-Year-Old Heritable Facultative Mutualism: Evolution in Glomeromycota-Glomeribacter Symbiosis
journal, March 2012


Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential
journal, June 2015

  • Salvioli, Alessandra; Ghignone, Stefano; Novero, Mara
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.91

Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens
journal, February 2017

  • Uehling, J.; Gryganskyi, A.; Hameed, K.
  • Environmental Microbiology, Vol. 19, Issue 8
  • DOI: 10.1111/1462-2920.13669

Lipid metabolic changes in an early divergent fungus govern the establishment of a mutualistic symbiosis with endobacteria
journal, December 2016

  • Lastovetsky, Olga A.; Gaspar, Maria L.; Mondo, Stephen J.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 52
  • DOI: 10.1073/pnas.1615148113

Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger
journal, May 2011

  • Mela, Francesca; Fritsche, Kathrin; de Boer, Wietse
  • The ISME Journal, Vol. 5, Issue 9
  • DOI: 10.1038/ismej.2011.29

Lipid metabolic changes in an early divergent fungus govern the establishment of a mutualistic symbiosis with endobacteria
journal, December 2016

  • Lastovetsky, Olga A.; Gaspar, Maria L.; Mondo, Stephen J.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 52
  • DOI: 10.1073/pnas.1615148113

Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus by the helper bacterium Paenibacillus sp
journal, February 2013


Down-regulation of the caffeic acid O-methyltransferase gene in switchgrass reveals a novel monolignol analog
journal, January 2012

  • Tschaplinski, Timothy J.; Standaert, Robert F.; Engle, Nancy L.
  • Biotechnology for Biofuels, Vol. 5, Issue 1
  • DOI: 10.1186/1754-6834-5-71

Sugar for my honey: Carbohydrate partitioning in ectomycorrhizal symbiosis
journal, January 2007


An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria.
journal, January 1996


The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts
journal, April 2015

  • D. Ainsworth, Tracy; Krause, Lutz; Bridge, Thomas
  • The ISME Journal, Vol. 9, Issue 10
  • DOI: 10.1038/ismej.2015.39

Variations in symbiotic efficiency, phenotypic characters and ploidy level among different isolates of the ectomycorrhizal basidiomycete Laccaria bicolor strain S 238
journal, November 1996


Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans
journal, August 2009

  • Schroeckh, V.; Scherlach, K.; Nutzmann, H. -W.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 34
  • DOI: 10.1073/pnas.0901870106

Modular microfluidics for point-of-care protein purifications
journal, January 2015

  • Millet, L. J.; Lucheon, J. D.; Standaert, R. F.
  • Lab on a Chip, Vol. 15, Issue 8
  • DOI: 10.1039/c5lc00094g

Real-Time Quantitative PCR (QPCR) and Reverse Transcription-QPCR for Detection and Enumeration of Total Yeasts in Wine
journal, August 2006

  • Hierro, N.; Esteve-Zarzoso, B.; Gonzalez, A.
  • Applied and Environmental Microbiology, Vol. 72, Issue 11
  • DOI: 10.1128/aem.00388-06

Draft Genome Sequence of the Betaproteobacterial Endosymbiont Associated with the Fungus Mortierella elongata FMR23-6
journal, November 2014


TipChip: a modular, MEMS-based platform for experimentation and phenotyping of tip-growing cells
journal, January 2013

  • Agudelo, Carlos G.; Sanati Nezhad, Amir; Ghanbari, Mahmood
  • The Plant Journal, Vol. 73, Issue 6
  • DOI: 10.1111/tpj.12093

Fungi Use Efficient Algorithms for the Exploration of Microfluidic Networks
journal, August 2006

  • Hanson, Kristi L.; Nicolau, Dan V.; Filipponi, Luisa
  • Small, Vol. 2, Issue 10
  • DOI: 10.1002/smll.200600105

Inter-organismal signaling and management of the phytomicrobiome
journal, September 2015

  • Smith, Donald L.; Praslickova, Dana; Ilangumaran, Gayathri
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00722

Rapid Isolation and Concentration of Pathogenic Fungi Using Inertial Focusing on a Chip-Based Platform
journal, February 2019

  • Fuchs, Beth Burgwyn; Eatemadpour, Soraya; Martel-Foley, Joseph M.
  • Frontiers in Cellular and Infection Microbiology, Vol. 9
  • DOI: 10.3389/fcimb.2019.00027

Probing bacterial–fungal interactions at the single cell level
journal, January 2014

  • Stanley, Claire E.; Stöckli, Martina; van Swaay, Dirk
  • Integr. Biol., Vol. 6, Issue 10
  • DOI: 10.1039/c4ib00154k

The oxidative environment: a mediator of interspecies communication that drives symbiosis evolution
journal, June 2014

  • Moné, Yves; Monnin, David; Kremer, Natacha
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1785
  • DOI: 10.1098/rspb.2013.3112

Aldonic Acids: A Novel Family of nod Gene Inducers of Mesorhizobium loti, Rhizobium lupini , and Sinorhizobium meliloti
journal, October 1998


Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants
journal, June 2014

  • Bonito, Gregory; Reynolds, Hannah; Robeson, Michael S.
  • Molecular Ecology, Vol. 23, Issue 13
  • DOI: 10.1111/mec.12821

Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus
journal, October 2014

  • Labbé, Jessy L.; Weston, David J.; Dunkirk, Nora
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00579

Molecular mechanisms underlying the close association between soil Burkholderia and fungi
journal, May 2015

  • Stopnisek, Nejc; Zühlke, Daniela; Carlier, Aurélien
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.73

Diversity and occurrence of Burkholderia spp. in the natural environment
journal, July 2008


Kinetics of Bacterial Growth: Relationship between Population Density and Specific Growth Rate of Continuous Cultures
journal, August 1959


Symbiosis and Insect Diversification: an Ancient Symbiont of Sap-Feeding Insects from the Bacterial Phylum Bacteroidetes
journal, December 2005


Role of secondary metabolites in the interaction between Pseudomonas fluorescens and soil microorganisms under iron-limited conditions
journal, May 2016

  • Deveau, Aurélie; Gross, Harald; Palin, Béatrice
  • FEMS Microbiology Ecology, Vol. 92, Issue 8
  • DOI: 10.1093/femsec/fiw107

Bacterial–fungal interactions: ecology, mechanisms and challenges
journal, February 2018

  • Deveau, Aurélie; Bonito, Gregory; Uehling, Jessie
  • FEMS Microbiology Reviews, Vol. 42, Issue 3
  • DOI: 10.1093/femsre/fuy008

Microfluidics structures for probing the dynamic behaviour of filamentous fungi
journal, May 2010

  • Held, Marie; Lee, Abraham P.; Edwards, Clive
  • Microelectronic Engineering, Vol. 87, Issue 5-8
  • DOI: 10.1016/j.mee.2009.11.096

Probing bacterial–fungal interactions at the single cell level
journal, January 2014

  • Stanley, Claire E.; Stöckli, Martina; van Swaay, Dirk
  • Integr. Biol., Vol. 6, Issue 10
  • DOI: 10.1039/c4ib00154k

Bidirectional Propagation of Signals and Nutrients in Fungal Networks via Specialized Hyphae
journal, January 2019

  • Schmieder, Stefanie S.; Stanley, Claire E.; Rzepiela, Andrzej
  • Current Biology, Vol. 29, Issue 2
  • DOI: 10.1016/j.cub.2018.11.058

Inter-organismal signaling and management of the phytomicrobiome
journal, September 2015

  • Smith, Donald L.; Praslickova, Dana; Ilangumaran, Gayathri
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00722

Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential
journal, June 2015

  • Salvioli, Alessandra; Ghignone, Stefano; Novero, Mara
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.91

Two Poplar-Associated Bacterial Isolates Induce Additive Favorable Responses in a Constructed Plant-Microbiome System
journal, April 2016

  • Timm, Collin M.; Pelletier, Dale A.; Jawdy, Sara S.
  • Frontiers in Plant Science, Vol. 7
  • DOI: 10.3389/fpls.2016.00497

Polyphony in the rhizosphere: presymbiotic communication in arbuscular mycorrhizal symbiosis
journal, August 2013


Rhizobium fix genes mediate at least two communication steps in symbiotic nodule development
journal, March 1988


The Tiniest Tiny Genomes
journal, September 2014


Honeyguides and Honey Gatherers: Interspecific Communication in a Symbiotic Relationship
journal, March 1989


Variations in symbiotic efficiency, phenotypic characters and ploidy level among different isolates of the ectomycorrhizal basidiomycete Laccaria bicolor strain S 238
journal, November 1996


The mycorrhiza helper bacteria revisited
journal, October 2007


Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans
journal, August 2009

  • Schroeckh, V.; Scherlach, K.; Nutzmann, H. -W.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 34
  • DOI: 10.1073/pnas.0901870106

Modular microfluidics for point-of-care protein purifications
journal, January 2015

  • Millet, L. J.; Lucheon, J. D.; Standaert, R. F.
  • Lab on a Chip, Vol. 15, Issue 8
  • DOI: 10.1039/c5lc00094g

Genome evolution in bacterial endosymbionts of insects
journal, November 2002

  • Wernegreen, Jennifer J.
  • Nature Reviews Genetics, Vol. 3, Issue 11
  • DOI: 10.1038/nrg931

Combining microfluidics and RNA-sequencing to assess the inducible defensome of a mushroom against nematodes
journal, March 2019


Robust Spatial Sensing of Mating Pheromone Gradients by Yeast Cells
journal, December 2008


Fungal Innate Immunity Induced by Bacterial Microbe-Associated Molecular Patterns (MAMPs)
journal, March 2016

  • Ipcho, Simon; Sundelin, Thomas; Erbs, Gitte
  • G3&#58; Genes|Genomes|Genetics, Vol. 6, Issue 6
  • DOI: 10.1534/g3.116.027987

Fungi Use Efficient Algorithms for the Exploration of Microfluidic Networks
journal, August 2006

  • Hanson, Kristi L.; Nicolau, Dan V.; Filipponi, Luisa
  • Small, Vol. 2, Issue 10
  • DOI: 10.1002/smll.200600105

Detection of Betaproteobacteria inside the Mycelium of the Fungus Mortierella elongata
journal, January 2010

  • Sato, Yoshinori; Narisawa, Kazuhiko; Tsuruta, Kazuto
  • Microbes and Environments, Vol. 25, Issue 4
  • DOI: 10.1264/jsme2.me10134

'Candidatus Glomeribacter gigasporarum' gen. nov., sp. nov., an endosymbiont of arbuscular mycorrhizal fungi
journal, January 2003

  • Bianciotto, V.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 53, Issue 1
  • DOI: 10.1099/ijs.0.02382-0

Molecular Evolution in Bacterial Endosymbionts of Fungi
journal, November 2009

  • Castillo, D. M.; Pawlowska, T. E.
  • Molecular Biology and Evolution, Vol. 27, Issue 3
  • DOI: 10.1093/molbev/msp280

Bacterial-Fungal Interactions: Hyphens between Agricultural, Clinical, Environmental, and Food Microbiologists
journal, November 2011

  • Frey-Klett, P.; Burlinson, P.; Deveau, A.
  • Microbiology and Molecular Biology Reviews, Vol. 75, Issue 4
  • DOI: 10.1128/mmbr.00020-11

A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees
journal, October 2013


Sugar for my honey: Carbohydrate partitioning in ectomycorrhizal symbiosis
journal, January 2007


Mycoavidus cysteinexigens gen. nov., sp. nov., an endohyphal bacterium isolated from a soil isolate of the fungus Mortierella elongata
journal, May 2016

  • Nishizawa, Tomoyasu; Ohshima, Shoko; Hamada, Moriyuki
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 5
  • DOI: 10.1099/ijsem.0.000990

Kinetics of Bacterial Growth: Relationship between Population Density and Specific Growth Rate of Continuous Cultures
journal, August 1959


Live imaging of root–bacteria interactions in a microfluidics setup
journal, March 2017

  • Massalha, Hassan; Korenblum, Elisa; Malitsky, Sergey
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 17
  • DOI: 10.1073/pnas.1618584114

Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus by the helper bacterium Paenibacillus sp
journal, February 2013


Dual transcriptional profiling of a bacterial/fungal confrontation: Collimonas fungivorans versus Aspergillus niger
journal, May 2011

  • Mela, Francesca; Fritsche, Kathrin; de Boer, Wietse
  • The ISME Journal, Vol. 5, Issue 9
  • DOI: 10.1038/ismej.2011.29

Low-Volume Toolbox for the Discovery of Immunosuppressive Fungal Secondary Metabolites
journal, April 2013


Application of bacteria as self-healing agent for the development of sustainable concrete
journal, February 2010


Live imaging of root–bacteria interactions in a microfluidics setup
journal, March 2017

  • Massalha, Hassan; Korenblum, Elisa; Malitsky, Sergey
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 17
  • DOI: 10.1073/pnas.1618584114

Fungal Innate Immunity Induced by Bacterial Microbe-Associated Molecular Patterns (MAMPs)
journal, March 2016

  • Ipcho, Simon; Sundelin, Thomas; Erbs, Gitte
  • G3&#58; Genes|Genomes|Genetics, Vol. 6, Issue 6
  • DOI: 10.1534/g3.116.027987

Genome evolution in bacterial endosymbionts of insects
journal, November 2002

  • Wernegreen, Jennifer J.
  • Nature Reviews Genetics, Vol. 3, Issue 11
  • DOI: 10.1038/nrg931

Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus
journal, October 2014

  • Labbé, Jessy L.; Weston, David J.; Dunkirk, Nora
  • Frontiers in Plant Science, Vol. 5
  • DOI: 10.3389/fpls.2014.00579

Molecular mechanisms underlying the close association between soil Burkholderia and fungi
journal, May 2015

  • Stopnisek, Nejc; Zühlke, Daniela; Carlier, Aurélien
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.73

Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens
journal, February 2017

  • Uehling, J.; Gryganskyi, A.; Hameed, K.
  • Environmental Microbiology, Vol. 19, Issue 8
  • DOI: 10.1111/1462-2920.13669

The oxidative environment: a mediator of interspecies communication that drives symbiosis evolution
journal, June 2014

  • Moné, Yves; Monnin, David; Kremer, Natacha
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 281, Issue 1785
  • DOI: 10.1098/rspb.2013.3112

The genome of the obligate endobacterium of an AM fungus reveals an interphylum network of nutritional interactions
journal, August 2011

  • Ghignone, Stefano; Salvioli, Alessandra; Anca, Iulia
  • The ISME Journal, Vol. 6, Issue 1
  • DOI: 10.1038/ismej.2011.110

The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts
journal, April 2015

  • D. Ainsworth, Tracy; Krause, Lutz; Bridge, Thomas
  • The ISME Journal, Vol. 9, Issue 10
  • DOI: 10.1038/ismej.2015.39

Evolutionary Stability in a 400-Million-Year-Old Heritable Facultative Mutualism: Evolution in Glomeromycota-Glomeribacter Symbiosis
journal, March 2012


Rhizobium fix genes mediate at least two communication steps in symbiotic nodule development
journal, March 1988


Bidirectional Propagation of Signals and Nutrients in Fungal Networks via Specialized Hyphae
journal, January 2019

  • Schmieder, Stefanie S.; Stanley, Claire E.; Rzepiela, Andrzej
  • Current Biology, Vol. 29, Issue 2
  • DOI: 10.1016/j.cub.2018.11.058

Mycelial growth and substrate acidification of ectomycorrhizal fungi in response to different minerals
journal, January 2004


The Tiniest Tiny Genomes
journal, September 2014


Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen
journal, January 2011


Down-regulation of the caffeic acid O-methyltransferase gene in switchgrass reveals a novel monolignol analog
journal, January 2012

  • Tschaplinski, Timothy J.; Standaert, Robert F.; Engle, Nancy L.
  • Biotechnology for Biofuels, Vol. 5, Issue 1
  • DOI: 10.1186/1754-6834-5-71

Towards an Ecosystem Approach to Cheese Microbiology
journal, October 2013


Works referencing / citing this record:

Metabolomic Analysis Reveals Contributions of Citric and Citramalic Acids to Rare Earth Bioleaching by a Paecilomyces Fungus
journal, January 2020

  • Brisson, Vanessa L.; Zhuang, Wei-Qin; Alvarez-Cohen, Lisa
  • Frontiers in Microbiology, Vol. 10
  • DOI: 10.3389/fmicb.2019.03008