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:
-
- Oregon State Univ., Corvallis, OR (United States). Dept. of Botany and Plant Pathology; Duke Univ., Durham, NC (United States). Dept. of Biology
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
- Johns Hopkins Bloomberg School of Public Health, Baltimore, MD (United States). Dept. of Epidemiology; Duke Univ., Durham, NC (United States). Dept. of Biomedical Engineering
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Univ. of Tennessee, Knoxville, TN (United States). The Bredesen Center
- Michigan State Univ., East Lansing, MI (United States). Dept. of Plant, Soil and Microbial Sciences
- 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). 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
- 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
- Oregon State Univ., Corvallis, OR (United States). Dept. of Botany and Plant Pathology
- Univ. of California, Riverside, CA (United States). Dept. of Microbiology and Plant Pathology, Inst. for Integrative Genome Biology
- 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}
}
Web of Science
Figures / Tables:
Works referenced in this record:
Symbiosis and Insect Diversification: an Ancient Symbiont of Sap-Feeding Insects from the Bacterial Phylum Bacteroidetes
journal, December 2005
- Moran, N. A.; Tran, P.; Gerardo, N. M.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
Relationship Between Host Acidification and Virulence of Penicillium spp. on Apple and Citrus Fruit
journal, January 2004
- Prusky, Dov; McEvoy, James L.; Saftner, Robert
- Phytopathology, Vol. 94, Issue 1
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
Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen
journal, January 2011
- Hess, M.; Sczyrba, A.; Egan, R.
- Science, Vol. 331, Issue 6016
Combining microfluidics and RNA-sequencing to assess the inducible defensome of a mushroom against nematodes
text, January 2019
- Tayyrov, Annageldi; Stanley, Claire E.; Azevedo, Sophie
- ETH Zurich
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
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
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
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
A Kinetic Study of the Growth of Aspergillus nidulans and Other Fungi
journal, July 1969
- Trinci, A. P. J.
- Journal of General Microbiology, Vol. 57, Issue 1
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
The Endosymbiont Hamiltonella Increases the Growth Rate of Its Host Bemisia tabaci during Periods of Nutritional Stress
journal, February 2014
- Su, Qi; Xie, Wen; Wang, Shaoli
- PLoS ONE, Vol. 9, Issue 2
Molecular Evolution in Bacterial Endosymbionts of Fungi
journal, November 2009
- Castillo, D. M.; Pawlowska, T. E.
- Molecular Biology and Evolution, Vol. 27, Issue 3
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
'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
The mycorrhiza helper bacteria revisited
journal, October 2007
- Frey-Klett, P.; Garbaye, J.; Tarkka, M.
- New Phytologist, Vol. 176, Issue 1
Diversity and occurrence of Burkholderia spp. in the natural environment
journal, July 2008
- Compant, Stéphane; Nowak, Jerzy; Coenye, Tom
- FEMS Microbiology Reviews, Vol. 32, Issue 4
Aldonic Acids: A Novel Family of nod Gene Inducers of Mesorhizobium loti, Rhizobium lupini , and Sinorhizobium meliloti
journal, October 1998
- Gagnon, Hubert; Ibrahim, Ragai K.
- Molecular Plant-Microbe Interactions, Vol. 11, Issue 10
The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N
journal, September 2007
- Deveau, A.; Palin, B.; Delaruelle, C.
- New Phytologist, Vol. 175, Issue 4
Pseudomonas-Candida Interactions: An Ecological Role for Virulence Factors
journal, June 2002
- Hogan, D. A.
- Science, Vol. 296, Issue 5576
Polyphony in the rhizosphere: presymbiotic communication in arbuscular mycorrhizal symbiosis
journal, August 2013
- Nadal, Marina; Paszkowski, Uta
- Current Opinion in Plant Biology, Vol. 16, Issue 4
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
Combined inactivation of the Clostridium cellulolyticum lactate and malate dehydrogenase genes substantially increases ethanol yield from cellulose and switchgrass fermentations
journal, January 2012
- Li, Yongchao; Tschaplinski, Timothy J.; Engle, Nancy L.
- Biotechnology for Biofuels, Vol. 5, Issue 1
Low-Volume Toolbox for the Discovery of Immunosuppressive Fungal Secondary Metabolites
journal, April 2013
- Berthier, Erwin; Lim, Fang Yun; Deng, Qing
- PLoS Pathogens, Vol. 9, Issue 4
Evolutionary Stability in a 400-Million-Year-Old Heritable Facultative Mutualism: Evolution in Glomeromycota-Glomeribacter Symbiosis
journal, March 2012
- Mondo, Stephen J.; Toomer, Kevin H.; Morton, Joseph B.
- Evolution, Vol. 66, Issue 8
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
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
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
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
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
Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus by the helper bacterium Paenibacillus sp
journal, February 2013
- Aspray, T. J.; Jones, E. E.; Davies, M. W.
- Mycorrhiza, Vol. 23, Issue 5
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
Sugar for my honey: Carbohydrate partitioning in ectomycorrhizal symbiosis
journal, January 2007
- Nehls, Uwe; Grunze, Nina; Willmann, Martin
- Phytochemistry, Vol. 68, Issue 1
An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria.
journal, January 1996
- Bianciotto, V.; Bandi, C.; Minerdi, D.
- Applied and environmental microbiology, Vol. 62, Issue 8
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
Variations in symbiotic efficiency, phenotypic characters and ploidy level among different isolates of the ectomycorrhizal basidiomycete Laccaria bicolor strain S 238
journal, November 1996
- Di Battista, Céline; Selosse, Marc-André; Bouchard, Daniel
- Mycological Research, Vol. 100, Issue 11
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
Pairwise Transcriptomic Analysis of the Interactions Between the Ectomycorrhizal Fungus Laccaria bicolor S238N and Three Beneficial, Neutral and Antagonistic Soil Bacteria
journal, August 2014
- Deveau, Aurélie; Barret, Matthieu; Diedhiou, Abdala G.
- Microbial Ecology, Vol. 69, Issue 1
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
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
Draft Genome Sequence of the Betaproteobacterial Endosymbiont Associated with the Fungus Mortierella elongata FMR23-6
journal, November 2014
- Fujimura, R.; Nishimura, A.; Ohshima, S.
- Genome Announcements, Vol. 2, Issue 6
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
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
Inter-organismal signaling and management of the phytomicrobiome
journal, September 2015
- Smith, Donald L.; Praslickova, Dana; Ilangumaran, Gayathri
- Frontiers in Plant Science, Vol. 6
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
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
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
Aldonic Acids: A Novel Family of nod Gene Inducers of Mesorhizobium loti, Rhizobium lupini , and Sinorhizobium meliloti
journal, October 1998
- Gagnon, Hubert; Ibrahim, Ragai K.
- Molecular Plant-Microbe Interactions, Vol. 11, Issue 10
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
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
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
Diversity and occurrence of Burkholderia spp. in the natural environment
journal, July 2008
- Compant, Stéphane; Nowak, Jerzy; Coenye, Tom
- FEMS Microbiology Reviews, Vol. 32, Issue 4
Kinetics of Bacterial Growth: Relationship between Population Density and Specific Growth Rate of Continuous Cultures
journal, August 1959
- Contois, D. E.
- Journal of General Microbiology, Vol. 21, Issue 1
Symbiosis and Insect Diversification: an Ancient Symbiont of Sap-Feeding Insects from the Bacterial Phylum Bacteroidetes
journal, December 2005
- Moran, N. A.; Tran, P.; Gerardo, N. M.
- Applied and Environmental Microbiology, Vol. 71, Issue 12
Transcriptomics of the Rice Blast Fungus Magnaporthe oryzae in Response to the Bacterial Antagonist Lysobacter enzymogenes Reveals Candidate Fungal Defense Response Genes
journal, October 2013
- Mathioni, Sandra M.; Patel, Nrupali; Riddick, Bianca
- PLoS ONE, Vol. 8, Issue 10
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
Bacterial–fungal interactions: ecology, mechanisms and challenges
journal, February 2018
- Deveau, Aurélie; Bonito, Gregory; Uehling, Jessie
- FEMS Microbiology Reviews, Vol. 42, Issue 3
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
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
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
The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N
journal, September 2007
- Deveau, A.; Palin, B.; Delaruelle, C.
- New Phytologist, Vol. 175, Issue 4
Inter-organismal signaling and management of the phytomicrobiome
journal, September 2015
- Smith, Donald L.; Praslickova, Dana; Ilangumaran, Gayathri
- Frontiers in Plant Science, Vol. 6
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
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
Combined inactivation of the Clostridium cellulolyticum lactate and malate dehydrogenase genes substantially increases ethanol yield from cellulose and switchgrass fermentations
journal, January 2012
- Li, Yongchao; Tschaplinski, Timothy J.; Engle, Nancy L.
- Biotechnology for Biofuels, Vol. 5, Issue 1
Polyphony in the rhizosphere: presymbiotic communication in arbuscular mycorrhizal symbiosis
journal, August 2013
- Nadal, Marina; Paszkowski, Uta
- Current Opinion in Plant Biology, Vol. 16, Issue 4
Rhizobium fix genes mediate at least two communication steps in symbiotic nodule development
journal, March 1988
- Putnoky, P.
- The Journal of Cell Biology, Vol. 106, Issue 3
The Tiniest Tiny Genomes
journal, September 2014
- Moran, Nancy A.; Bennett, Gordon M.
- Annual Review of Microbiology, Vol. 68, Issue 1
Honeyguides and Honey Gatherers: Interspecific Communication in a Symbiotic Relationship
journal, March 1989
- Isack, H. A.; Reyer, H. -U.
- Science, Vol. 243, Issue 4896
Variations in symbiotic efficiency, phenotypic characters and ploidy level among different isolates of the ectomycorrhizal basidiomycete Laccaria bicolor strain S 238
journal, November 1996
- Di Battista, Céline; Selosse, Marc-André; Bouchard, Daniel
- Mycological Research, Vol. 100, Issue 11
The mycorrhiza helper bacteria revisited
journal, October 2007
- Frey-Klett, P.; Garbaye, J.; Tarkka, M.
- New Phytologist, Vol. 176, Issue 1
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
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
The Endosymbiont Hamiltonella Increases the Growth Rate of Its Host Bemisia tabaci during Periods of Nutritional Stress
journal, February 2014
- Su, Qi; Xie, Wen; Wang, Shaoli
- PLoS ONE, Vol. 9, Issue 2
Genome evolution in bacterial endosymbionts of insects
journal, November 2002
- Wernegreen, Jennifer J.
- Nature Reviews Genetics, Vol. 3, Issue 11
Combining microfluidics and RNA-sequencing to assess the inducible defensome of a mushroom against nematodes
journal, March 2019
- Tayyrov, Annageldi; Stanley, Claire E.; Azevedo, Sophie
- BMC Genomics, Vol. 20, Issue 1
Robust Spatial Sensing of Mating Pheromone Gradients by Yeast Cells
journal, December 2008
- Moore, Travis I.; Chou, Ching-Shan; Nie, Qing
- PLoS ONE, Vol. 3, Issue 12
Fungal Innate Immunity Induced by Bacterial Microbe-Associated Molecular Patterns (MAMPs)
journal, March 2016
- Ipcho, Simon; Sundelin, Thomas; Erbs, Gitte
- G3: Genes|Genomes|Genetics, Vol. 6, Issue 6
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
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
'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
Molecular Evolution in Bacterial Endosymbionts of Fungi
journal, November 2009
- Castillo, D. M.; Pawlowska, T. E.
- Molecular Biology and Evolution, Vol. 27, Issue 3
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
A Multifactor Analysis of Fungal and Bacterial Community Structure in the Root Microbiome of Mature Populus deltoides Trees
journal, October 2013
- Shakya, Migun; Gottel, Neil; Castro, Hector
- PLoS ONE, Vol. 8, Issue 10
Sugar for my honey: Carbohydrate partitioning in ectomycorrhizal symbiosis
journal, January 2007
- Nehls, Uwe; Grunze, Nina; Willmann, Martin
- Phytochemistry, Vol. 68, Issue 1
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
Kinetics of Bacterial Growth: Relationship between Population Density and Specific Growth Rate of Continuous Cultures
journal, August 1959
- Contois, D. E.
- Journal of General Microbiology, Vol. 21, Issue 1
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
Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus by the helper bacterium Paenibacillus sp
journal, February 2013
- Aspray, T. J.; Jones, E. E.; Davies, M. W.
- Mycorrhiza, Vol. 23, Issue 5
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
Low-Volume Toolbox for the Discovery of Immunosuppressive Fungal Secondary Metabolites
journal, April 2013
- Berthier, Erwin; Lim, Fang Yun; Deng, Qing
- PLoS Pathogens, Vol. 9, Issue 4
Application of bacteria as self-healing agent for the development of sustainable concrete
journal, February 2010
- Jonkers, Henk M.; Thijssen, Arjan; Muyzer, Gerard
- Ecological Engineering, Vol. 36, Issue 2
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
Fungal Innate Immunity Induced by Bacterial Microbe-Associated Molecular Patterns (MAMPs)
journal, March 2016
- Ipcho, Simon; Sundelin, Thomas; Erbs, Gitte
- G3: Genes|Genomes|Genetics, Vol. 6, Issue 6
Genome evolution in bacterial endosymbionts of insects
journal, November 2002
- Wernegreen, Jennifer J.
- Nature Reviews Genetics, Vol. 3, Issue 11
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
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
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
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
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
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
Evolutionary Stability in a 400-Million-Year-Old Heritable Facultative Mutualism: Evolution in Glomeromycota-Glomeribacter Symbiosis
journal, March 2012
- Mondo, Stephen J.; Toomer, Kevin H.; Morton, Joseph B.
- Evolution, Vol. 66, Issue 8
Rhizobium fix genes mediate at least two communication steps in symbiotic nodule development
journal, March 1988
- Putnoky, P.
- The Journal of Cell Biology, Vol. 106, Issue 3
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
Transcriptomics of the Rice Blast Fungus Magnaporthe oryzae in Response to the Bacterial Antagonist Lysobacter enzymogenes Reveals Candidate Fungal Defense Response Genes
journal, October 2013
- Mathioni, Sandra M.; Patel, Nrupali; Riddick, Bianca
- PLoS ONE, Vol. 8, Issue 10
Mycelial growth and substrate acidification of ectomycorrhizal fungi in response to different minerals
journal, January 2004
- Rosling, Anna; Lindahl, Björn D.; Taylor, Andy F. S.
- FEMS Microbiology Ecology, Vol. 47, Issue 1
The Tiniest Tiny Genomes
journal, September 2014
- Moran, Nancy A.; Bennett, Gordon M.
- Annual Review of Microbiology, Vol. 68, Issue 1
Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen
journal, January 2011
- Hess, M.; Sczyrba, A.; Egan, R.
- Science, Vol. 331, Issue 6016
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
Towards an Ecosystem Approach to Cheese Microbiology
journal, October 2013
- Wolfe, Benjamin E.; Dutton, Rachel J.
- Microbiology Spectrum, Vol. 1, Issue 1
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