Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens

Uehling, J.; Gryganskyi, A.; Hameed, K.; Tschaplinski, T.; Misztal, P. K.; Wu, S.; Desirò, A.; Vande Pol, N.; Du, Z.; Zienkiewicz, A.; Zienkiewicz, K.; Morin, E.; Tisserant, E.; Splivallo, R.; Hainaut, M.; Henrissat, B.; Ohm, R.; Kuo, A.; Yan, J.; Lipzen, A.; Nolan, M.; LaButti, K.; Barry, K.; Goldstein, A. H.; Labbé, J.; Schadt, C.; Tuskan, G.; Grigoriev, I.; Martin, F.; Vilgalys, R.; Bonito, G.

doi:10.1111/1462-2920.13669

Title: Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens

Journal Article · Wed Jan 11 00:00:00 EST 2017 · Environmental Microbiology

DOI:https://doi.org/10.1111/1462-2920.13669· OSTI ID:1342658

Uehling, J. ^[1]; Gryganskyi, A. ^[2]; Hameed, K. ^[1]; Tschaplinski, T. ^[3]; Misztal, P. K. ^[4]; Wu, S. ^[5]; Desirò, A. ^[6]; Vande Pol, N. ^[6]; Du, Z. ^[6]; Zienkiewicz, A. ^[6]; Zienkiewicz, K. ^[6]; Morin, E. ^[7]; Tisserant, E. ^[7]; Splivallo, R. ^[8]; Hainaut, M. ^[9]; Henrissat, B. ^[9]; Ohm, R. ^[10]; Kuo, A. ^[11]; Yan, J. ^[11]; Lipzen, A. ^[11] more »

Duke Univ., Durham, NC (United States). Dept. of Biology
LF Lambert Spawn Company, Coatesville, PA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
Univ. of California, Berkeley, CA (United States)
Arizona State Univ., Tempe, AZ (United States)
Michigan State Univ., East Lansing, MI (United States). MSU-DOE Plant Research Lab.
Univ. of Lorraine, Nancy (France). National Inst. for Agricultural Research
Goethe Univ., Frankfurt (Germany). Inst. for Molecular Biosciences
Aix-Marseille Univ., and CNRS/IN2P3, Marseille (France). Architecture and Function of Biological Molecules
Utrecht Univ., (The Netherlands). Dept. of Biology
Joint Genome Inst., Oakland CA (United States)

One defining feature of cellular evolution is endosymbiosis of bacteria by eukaryotes. In addition to well-known bacterial origins for mitochondria and chloroplasts, multiple origins of bacterial endosymbiosis are known within the cells of diverse animals, plants and fungi. Early-diverging lineages of terrestrial fungi harbor endosymbiotic bacteria belonging to the Burkholderiaceae. We sequenced the metagenome of the soil-inhabiting fungus Mortierella elongata and assembled the complete circular chromosome of its endosymbiont, Mycoavidus cysteinexigens, which we place within a lineage of endofungal symbionts that are sister clade to Burkholderia. Furthermore, the genome of M. elongata strain AG77 features a core set of primary metabolic pathways for degradation of simple carbohydrates and lipid biosynthesis, while the M. cysteinexigens (AG77) genome is reduced in size and function. Our experiments using antibiotics to cure the endobacterium from the host demonstrate that the fungal host metabolism is highly modulated by presence/absence of M. cysteinexigens. Independent comparative phylogenomic analyses of fungal and bacterial genomes are consistent with an ancient origin for M. elongata – M. cysteinexigens symbiosis, most likely over 350 million years ago and concomitant with the terrestrialization of Earth and diversification of land fungi and plants.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725; AC02-05CH11231

OSTI ID:: 1342658

Alternate ID(s):: OSTI ID: 1342680; OSTI ID: 1375465

Journal Information:: Environmental Microbiology, Vol. 19, Issue 8; ISSN 1462-2912

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 102 works

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References (99)

Phylogenomic Analyses Indicate that Early Fungi Evolved Digesting Cell Walls of Algal Ancestors of Land Plants Chang, Ying; Wang, Sishuo; Sekimoto, Satoshi Genome Biology and Evolution, Vol. 7, Issue 6 https://doi.org/10.1093/gbe/evv090	journal	May 2015
Bacterial Membrane Lipids: Where Do We Stand? Cronan, John E. Annual Review of Microbiology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.micro.57.030502.090851	journal	October 2003
Endofungal bacterium controls its host by an hrp type III secretion system Lackner, Gerald; Moebius, Nadine; Hertweck, Christian The ISME Journal, Vol. 5, Issue 2 https://doi.org/10.1038/ismej.2010.126	journal	August 2010
The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4) Huntemann, Marcel; Ivanova, Natalia N.; Mavromatis, Konstantinos Standards in Genomic Sciences, Vol. 10, Issue 1 https://doi.org/10.1186/s40793-015-0077-y	journal	October 2015
A novel intracellular nitrogen-fixing symbiosis made by Ustilago maydis and Bacillus spp. Ruiz-Herrera, José; León-Ramírez, Claudia; Vera-Nuñez, Antonio New Phytologist, Vol. 207, Issue 3 https://doi.org/10.1111/nph.13359	journal	March 2015
Genome Characterization of the Oleaginous Fungus Mortierella alpina Wang, Lei; Chen, Wei; Feng, Yun PLoS ONE, Vol. 6, Issue 12 https://doi.org/10.1371/journal.pone.0028319	journal	December 2011
Review and re-analysis of domain-specific 16S primers Baker, G. C.; Smith, J. J.; Cowan, D. A. Journal of Microbiological Methods, Vol. 55, Issue 3 https://doi.org/10.1016/j.mimet.2003.08.009	journal	December 2003
TagFinder for the quantitative analysis of gas chromatography—mass spectrometry (GC-MS)-based metabolite profiling experiments Luedemann, Alexander; Strassburg, Katrin; Erban, Alexander Bioinformatics, Vol. 24, Issue 5 https://doi.org/10.1093/bioinformatics/btn023	journal	January 2008
Mycoavidus cysteinexigens gen. nov., sp. nov., an endohyphal bacterium isolated from a soil isolate of the fungus Mortierella elongata Nishizawa, Tomoyasu; Ohshima, Shoko; Hamada, Moriyuki International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 5 https://doi.org/10.1099/ijsem.0.000990	journal	May 2016
Analysis of the chemical composition of organic aerosol at the Mt. Sonnblick observatory using a novel high mass resolution thermal-desorption proton-transfer-reaction mass-spectrometer (hr-TD-PTR-MS) Holzinger, R.; Kasper-Giebl, A.; Staudinger, M. Atmospheric Chemistry and Physics, Vol. 10, Issue 20 https://doi.org/10.5194/acp-10-10111-2010	journal	January 2010
A Gene Cluster Encoding Rhizoxin Biosynthesis in “Burkholderia rhizoxina”, the Bacterial Endosymbiont of the FungusRhizopus microsporus Partida-Martinez, Laila P.; Hertweck, Christian ChemBioChem, Vol. 8, Issue 1 https://doi.org/10.1002/cbic.200600393	journal	January 2007
High-quality draft assemblies of mammalian genomes from massively parallel sequence data Gnerre, S.; MacCallum, I.; Przybylski, D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 4 https://doi.org/10.1073/pnas.1017351108	journal	December 2010
Fine-scale spatial genetic structure analysis of the black truffle T uber aestivum and its link to aroma variability : Tuber aestivum: genetic and aroma variability Molinier, Virginie; Murat, Claude; Frochot, Henri Environmental Microbiology, Vol. 17, Issue 8 https://doi.org/10.1111/1462-2920.12910	journal	July 2015
'Candidatus Glomeribacter gigasporarum' gen. nov., sp. nov., an endosymbiont of arbuscular mycorrhizal fungi Bianciotto, V. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 53, Issue 1 https://doi.org/10.1099/ijs.0.02382-0	journal	January 2003
The Fungi Stajich, Jason E.; Berbee, Mary L.; Blackwell, Meredith Current Biology, Vol. 19, Issue 18 https://doi.org/10.1016/j.cub.2009.07.004	journal	September 2009
A Mammalian Type I Fatty Acid Synthase Acyl Carrier Protein Domain Does Not Sequester Acyl Chains Ploskoń, Eliza; Arthur, Christopher J.; Evans, Simon E. Journal of Biological Chemistry, Vol. 283, Issue 1 https://doi.org/10.1074/jbc.M703454200	journal	October 2007
Freeze-Substitution of Fungi Hoch, Harvey C. Ultrastructure Techniques for Microorganisms https://doi.org/10.1007/978-1-4684-5119-1_7	book	January 1986
Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments Talavera, Gerard; Castresana, Jose Systematic Biology, Vol. 56, Issue 4 https://doi.org/10.1080/10635150701472164	journal	August 2007
antiSMASH: rapid identification, annotation and analysis of secondary metabolite biosynthesis gene clusters in bacterial and fungal genome sequences Medema, Marnix H.; Blin, Kai; Cimermancic, Peter Nucleic Acids Research, Vol. 39, Issue suppl_2 https://doi.org/10.1093/nar/gkr466	journal	June 2011
Draft Genome Sequence of the Betaproteobacterial Endosymbiont Associated with the Fungus Mortierella elongata FMR23-6 Fujimura, R.; Nishimura, A.; Ohshima, S. Genome Announcements, Vol. 2, Issue 6 https://doi.org/10.1128/genomeA.01272-14	journal	November 2014
Roles of the FabA and FabZ β-Hydroxyacyl-Acyl Carrier Protein Dehydratases in Escherichia coli Fatty Acid Biosynthesis Heath, Richard J.; Rock, Charles O. Journal of Biological Chemistry, Vol. 271, Issue 44 https://doi.org/10.1074/jbc.271.44.27795	journal	November 1996
CAFE: a computational tool for the study of gene family evolution De Bie, T.; Cristianini, N.; Demuth, J. P. Bioinformatics, Vol. 22, Issue 10 https://doi.org/10.1093/bioinformatics/btl097	journal	March 2006
Evolutionary Stability in a 400-Million-Year-Old Heritable Facultative Mutualism: Evolution in Glomeromycota-Glomeribacter Symbiosis Mondo, Stephen J.; Toomer, Kevin H.; Morton, Joseph B. Evolution, Vol. 66, Issue 8 https://doi.org/10.1111/j.1558-5646.2012.01611.x	journal	March 2012
Differential amplification of rRNA genes by polymerase chain reaction. Reysenbach, A. L.; Giver, L. J.; Wickham, G. S. Applied and Environmental Microbiology, Vol. 58, Issue 10 https://doi.org/10.1128/AEM.58.10.3417-3418.1992	journal	January 1992
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Fatty Acid and Phospholipid Biosynthesis in Prokaryotes Zhang, Yong-Mei; Rock, Charles O. Biochemistry of Lipids, Lipoproteins and Membranes https://doi.org/10.1016/B978-0-444-63438-2.00003-1	book	January 2016
Minimal genomes of mycoplasma-related endobacteria are plastic and contain host-derived genes for sustained life within Glomeromycota Naito, Mizue; Morton, Joseph B.; Pawlowska, Teresa E. Proceedings of the National Academy of Sciences, Vol. 112, Issue 25 https://doi.org/10.1073/pnas.1501676112	journal	May 2015
Phosphatidic acid synthesis in bacteria Yao, Jiangwei; Rock, Charles O. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1831, Issue 3 https://doi.org/10.1016/j.bbalip.2012.08.018	journal	March 2013
Isolation, Free-Living Capacities, and Genome Structure of "Candidatus Glomeribacter gigasporarum," the Endocellular Bacterium of the Mycorrhizal Fungus Gigaspora margarita Jargeat, P.; Cosseau, C.; Ola'h, B. Journal of Bacteriology, Vol. 186, Issue 20 https://doi.org/10.1128/JB.186.20.6876-6884.2004	journal	October 2004
Succession of microbial consortia in the developing infant gut microbiome Koenig, J. E.; Spor, A.; Scalfone, N. Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1 https://doi.org/10.1073/pnas.1000081107	journal	July 2010
Global diversity and geography of soil fungi Tedersoo, Leho; Bahram, Mohammad; Põlme, Sergei Science, Vol. 346, Issue 6213 https://doi.org/10.1126/science.1256688	journal	November 2014
Mechanistic diversity and regulation of Type II fatty acid synthesis Marrakchi, H.; Zhang, Y.-M.; Rock, C. O. Biochemical Society Transactions, Vol. 30, Issue 6, p. 1050-1055 https://doi.org/10.1042/bst0301050	journal	November 2002
Phylogenetic mixture models for proteins Le, Si Quang; Lartillot, Nicolas; Gascuel, Olivier Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1512 https://doi.org/10.1098/rstb.2008.0180	journal	October 2008
Creating the CIPRES Science Gateway for inference of large phylogenetic trees Miller, Mark A.; Pfeiffer, Wayne; Schwartz, Terri 2010 Gateway Computing Environments Workshop (GCE) https://doi.org/10.1109/GCE.2010.5676129	conference	November 2010
Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: Transkingdom gene transfer in an ancient mycoplasma-fungus association Torres-Cortés, Gloria; Ghignone, Stefano; Bonfante, Paola Proceedings of the National Academy of Sciences, Vol. 112, Issue 25 https://doi.org/10.1073/pnas.1501540112	journal	May 2015
Pathogenic fungus harbours endosymbiotic bacteria for toxin production Partida-Martinez, Laila P.; Hertweck, Christian Nature, Vol. 437, Issue 7060 https://doi.org/10.1038/nature03997	journal	October 2005
Endofungal bacteria as producers of mycotoxins Lackner, Gerald; Partida-Martinez, Laila P.; Hertweck, Christian Trends in Microbiology, Vol. 17, Issue 12 https://doi.org/10.1016/j.tim.2009.09.003	journal	December 2009
SseBCD Proteins Are Secreted by the Type III Secretion System of Salmonella Pathogenicity Island 2 and Function as a Translocon Nikolaus, T.; Deiwick, J.; Rappl, C. Journal of Bacteriology, Vol. 183, Issue 20 https://doi.org/10.1128/JB.183.20.6036-6045.2001	journal	October 2001
Ecological and evolutionary significance of mycorrhizal symbioses in vascular plants (A Review) Malloch, D. W.; Pirozynski, K. A.; Raven, P. H. Proceedings of the National Academy of Sciences, Vol. 77, Issue 4 https://doi.org/10.1073/pnas.77.4.2113	journal	April 1980
Rnnotator: an automated de novo transcriptome assembly pipeline from stranded RNA-Seq reads Martin, Jeffrey; Bruno, Vincent M.; Fang, Zhide BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-663	journal	January 2010
Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants Bonito, Gregory; Reynolds, Hannah; Robeson, Michael S. Molecular Ecology, Vol. 23, Issue 13 https://doi.org/10.1111/mec.12821	journal	June 2014
Mollicutes -related endobacteria thrive inside liverwort-associated arbuscular mycorrhizal fungi : Endobacteria in liverwort-arbuscular mycorrhizal fungi Desirò, Alessandro; Naumann, Maria; Epis, Sara Environmental Microbiology, Vol. 15, Issue 3 https://doi.org/10.1111/j.1462-2920.2012.02833.x	journal	July 2012
MycoCosm portal: gearing up for 1000 fungal genomes Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1183	journal	December 2013
High resolution PTR-TOF: Quantification and formula confirmation of VOC in real time Graus, Martin; Müller, Markus; Hansel, Armin Journal of the American Society for Mass Spectrometry, Vol. 21, Issue 6 https://doi.org/10.1016/j.jasms.2010.02.006	journal	June 2010
Fatty Acid-Derived Biofuels and Chemicals Production in Saccharomyces cerevisiae Zhou, Yongjin J.; Buijs, Nicolaas A.; Siewers, Verena Frontiers in Bioengineering and Biotechnology, Vol. 2 https://doi.org/10.3389/fbioe.2014.00032	journal	September 2014
Functional Characterization of an Evolutionarily Distinct Phosphopantetheinyl Transferase in the Apicomplexan Cryptosporidium parvum Cai, Xiaomin; Herschap, Dustin; Zhu, Guan Eukaryotic Cell, Vol. 4, Issue 7 https://doi.org/10.1128/EC.4.7.1211-1220.2005	journal	July 2005
1-Octen-3-ol inhibits conidia germination of Penicillium paneum despite of mild effects on membrane permeability, respiration, intracellular pH, and changes the protein composition Chitarra, Gilma S.; Abee, Tjakko; Rombouts, Frank M. FEMS Microbiology Ecology, Vol. 54, Issue 1 https://doi.org/10.1016/j.femsec.2005.02.013	journal	September 2005
Diverse Bacteria Inhabit Living Hyphae of Phylogenetically Diverse Fungal Endophytes Hoffman, M. T.; Arnold, A. E. Applied and Environmental Microbiology, Vol. 76, Issue 12 https://doi.org/10.1128/AEM.02928-09	journal	April 2010
Evolution of an endofungal Lifestyle: Deductions from the Burkholderia rhizoxinica Genome Lackner, Gerald; Moebius, Nadine; Partida-Martinez, Laila P. BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-210	journal	May 2011
Diversity Patterns, Ecology and Biological Activities of Fungal Communities Associated with the Endemic Macroalgae Across the Antarctic Peninsula Furbino, Laura E.; Godinho, Valéria M.; Santiago, Iara F. Microbial Ecology, Vol. 67, Issue 4 https://doi.org/10.1007/s00248-014-0374-9	journal	February 2014
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 Deveau, A.; Palin, B.; Delaruelle, C. New Phytologist, Vol. 175, Issue 4 https://doi.org/10.1111/j.1469-8137.2007.02148.x	journal	September 2007
Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants Simon, Luc; Bousquet, Jean; Lévesque, Roger C. Nature, Vol. 363, Issue 6424 https://doi.org/10.1038/363067a0	journal	May 1993
Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential Salvioli, Alessandra; Ghignone, Stefano; Novero, Mara The ISME Journal, Vol. 10, Issue 1 https://doi.org/10.1038/ismej.2015.91	journal	June 2015
Bayesian Phylogenetics with BEAUti and the BEAST 1.7 Drummond, Alexei J.; Suchard, Marc A.; Xie, Dong Molecular Biology and Evolution, Vol. 29, Issue 8 https://doi.org/10.1093/molbev/mss075	journal	February 2012
Reconstructing the early evolution of Fungi using a six-gene phylogeny James, Timothy Y.; Kauff, Frank; Schoch, Conrad L. Nature, Vol. 443, Issue 7113 https://doi.org/10.1038/nature05110	journal	October 2006
Presymbiotic growth and sporal morphology are affected in the arbuscular mycorrhizal fungus Gigaspora margarita cured of its endobacteria Lumini, Erica; Bianciotto, Valeria; Jargeat, Patricia Cellular Microbiology, Vol. 9, Issue 7 https://doi.org/10.1111/j.1462-5822.2007.00907.x	journal	July 2007
Where is the unseen fungal diversity hidden? A study of Mortierella reveals a large contribution of reference collections to the identification of fungal environmental sequences Nagy, László G.; Petkovits, Tamás; Kovács, Gábor M. New Phytologist, Vol. 191, Issue 3 https://doi.org/10.1111/j.1469-8137.2011.03707.x	journal	March 2011
Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi Desirò, Alessandro; Salvioli, Alessandra; Ngonkeu, Eddy L. The ISME Journal, Vol. 8, Issue 2 https://doi.org/10.1038/ismej.2013.151	journal	September 2013
Isolation of Endohyphal Bacteria from Foliar Ascomycota and In Vitro Establishment of Their Symbiotic Associations Arendt, Kayla R.; Hockett, Kevin L.; Araldi-Brondolo, Sarah J. Applied and Environmental Microbiology, Vol. 82, Issue 10 https://doi.org/10.1128/AEM.00452-16	journal	March 2016
OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes Li, L. Genome Research, Vol. 13, Issue 9 https://doi.org/10.1101/gr.1224503	journal	September 2003
A core gut microbiome in obese and lean twins Turnbaugh, Peter J.; Hamady, Micah; Yatsunenko, Tanya Nature, Vol. 457, Issue 7228 https://doi.org/10.1038/nature07540	journal	November 2008
Isolating a functionally relevant guild of fungi from the root microbiome of Populus Bonito, Gregory; Hameed, Khalid; Ventura, Rafael Fungal Ecology, Vol. 22 https://doi.org/10.1016/j.funeco.2016.04.007	journal	August 2016
Investigating the Endobacteria Which Thrive in Arbuscular Mycorrhizal Fungi Desirò, Alessandro; Salvioli, Alessandra; Bonfante, Paola Microbial Environmental Genomics (MEG) https://doi.org/10.1007/978-1-4939-3369-3_2	book	January 2016
Mitochondrial Fatty Acid Synthesis Type II: More than Just Fatty Acids Hiltunen, J. Kalervo; Schonauer, Melissa S.; Autio, Kaija J. Journal of Biological Chemistry, Vol. 284, Issue 14 https://doi.org/10.1074/jbc.R800068200	journal	November 2008
Endobacteria affect the metabolic profile of their host Gigaspora margarita, an arbuscular mycorrhizal fungus: Endobacteria affect proteins and lipids in Gigaspora Salvioli, Alessandra; Chiapello, Marco; Fontaine, Joel Environmental Microbiology https://doi.org/10.1111/j.1462-2920.2010.02246.x	journal	June 2010
The multienzyme architecture of eukaryotic fatty acid synthases Leibundgut, Marc; Maier, Timm; Jenni, Simon Current Opinion in Structural Biology, Vol. 18, Issue 6 https://doi.org/10.1016/j.sbi.2008.09.008	journal	December 2008
Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis Tisserant, E.; Malbreil, M.; Kuo, A. Proceedings of the National Academy of Sciences, Vol. 110, Issue 50 https://doi.org/10.1073/pnas.1313452110	journal	November 2013
The Subsystems Approach to Genome Annotation and its Use in the Project to Annotate 1000 Genomes Overbeek, R. Nucleic Acids Research, Vol. 33, Issue 17 https://doi.org/10.1093/nar/gki866	journal	September 2005
Bacterial Long Chain Fatty Acid Transport: Gateway to a Fatty Acid-responsive Signaling System DiRusso, Concetta C.; Black, Paul N. Journal of Biological Chemistry, Vol. 279, Issue 48 https://doi.org/10.1074/jbc.R400026200	journal	August 2004
A high resolution and high sensitivity proton-transfer-reaction time-of-flight mass spectrometer (PTR-TOF-MS) Jordan, A.; Haidacher, S.; Hanel, G. International Journal of Mass Spectrometry, Vol. 286, Issue 2-3 https://doi.org/10.1016/j.ijms.2009.07.005	journal	September 2009
Glomalean Fungi from the Ordovician Redecker, D. Science, Vol. 289, Issue 5486 https://doi.org/10.1126/science.289.5486.1920	journal	September 2000
PATRIC, the bacterial bioinformatics database and analysis resource Wattam, Alice R.; Abraham, David; Dalay, Oral Nucleic Acids Research, Vol. 42, Issue D1 https://doi.org/10.1093/nar/gkt1099	journal	November 2013
Detection of Betaproteobacteria inside the Mycelium of the Fungus Mortierella elongata Sato, Yoshinori; Narisawa, Kazuhiko; Tsuruta, Kazuto Microbes and Environments, Vol. 25, Issue 4 https://doi.org/10.1264/jsme2.ME10134	journal	January 2010
Fatty acid production in Schizochytrium sp.: Involvement of a polyunsaturated fatty acid synthase and a type I fatty acid synthase Hauvermale, A.; Kuner, J.; Rosenzweig, B. Lipids, Vol. 41, Issue 8 https://doi.org/10.1007/s11745-006-5025-6	journal	August 2006
The rhizosphere microbiome and plant health Berendsen, Roeland L.; Pieterse, Corné M. J.; Bakker, Peter A. H. M. Trends in Plant Science, Vol. 17, Issue 8 https://doi.org/10.1016/j.tplants.2012.04.001	journal	August 2012
RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes Brettin, Thomas; Davis, James J.; Disz, Terry Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep08365	journal	February 2015
Diet Drives Convergence in Gut Microbiome Functions Across Mammalian Phylogeny and Within Humans Muegge, B. D.; Kuczynski, J.; Knights, D. Science, Vol. 332, Issue 6032 https://doi.org/10.1126/science.1198719	journal	May 2011
The genome of the obligate endobacterium of an AM fungus reveals an interphylum network of nutritional interactions Ghignone, Stefano; Salvioli, Alessandra; Anca, Iulia The ISME Journal, Vol. 6, Issue 1 https://doi.org/10.1038/ismej.2011.110	journal	August 2011
Attenuated virulence and protective efficacy of a Burkholderia pseudomallei bsa type III secretion mutant in murine models of melioidosis Stevens, M. P. Microbiology, Vol. 150, Issue 8 https://doi.org/10.1099/mic.0.27146-0	journal	August 2004
Regulation of cell size in response to nutrient availability by fatty acid biosynthesis in Escherichia coli Yao, Z.; Davis, R. M.; Kishony, R. Proceedings of the National Academy of Sciences, Vol. 109, Issue 38 https://doi.org/10.1073/pnas.1209742109	journal	August 2012
In Situ Identification of Intracellular Bacteria Related to Paenibacillus spp. in the Mycelium of the Ectomycorrhizal Fungus Laccaria bicolor S238N Bertaux, J.; Schmid, M.; Prevost-Boure, N. C. Applied and Environmental Microbiology, Vol. 69, Issue 7 https://doi.org/10.1128/AEM.69.7.4243-4248.2003	journal	July 2003
Secretion of YscP from Yersinia enterocolitica is essential to control the length of the injectisome needle but not to change the type III secretion substrate specificity : Secretion of YscP Agrain, Céline; Sorg, Isabel; Paroz, Cécile Molecular Microbiology, Vol. 57, Issue 5 https://doi.org/10.1111/j.1365-2958.2005.04758.x	journal	July 2005
Lipid production by oleaginous Mucorales cultivated on renewable carbon sources Papanikolaou, Seraphim; Galiotou-Panayotou, Maria; Fakas, Stylianos European Journal of Lipid Science and Technology, Vol. 109, Issue 11 https://doi.org/10.1002/ejlt.200700169	journal	November 2007
NORINE: a database of nonribosomal peptides Caboche, S.; Pupin, M.; Leclere, V. Nucleic Acids Research, Vol. 36, Issue Database https://doi.org/10.1093/nar/gkm792	journal	December 2007
An interdomain network: the endobacterium of a mycorrhizal fungus promotes antioxidative responses in both fungal and plant hosts Vannini, Candida; Carpentieri, Andrea; Salvioli, Alessandra New Phytologist, Vol. 211, Issue 1 https://doi.org/10.1111/nph.13895	journal	February 2016
A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data Spatafora, Joseph W.; Chang, Ying; Benny, Gerald L. Mycologia, Vol. 108, Issue 5 https://doi.org/10.3852/16-042	journal	September 2016
Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica Glaeser, Stefanie P.; Imani, Jafargholi; Alabid, Ibrahim The ISME Journal, Vol. 10, Issue 4 https://doi.org/10.1038/ismej.2015.163	journal	October 2015
PartitionFinder: Combined Selection of Partitioning Schemes and Substitution Models for Phylogenetic Analyses Lanfear, R.; Calcott, B.; Ho, S. Y. W. Molecular Biology and Evolution, Vol. 29, Issue 6 https://doi.org/10.1093/molbev/mss020	journal	January 2012
Phylogenomics and evolution of secondary metabolism in plant-associated fungi Spatafora, Joseph W.; Bushley, Kathryn E. Current Opinion in Plant Biology, Vol. 26 https://doi.org/10.1016/j.pbi.2015.05.030	journal	August 2015
Horizontal Gene Transfer in Eukaryotic Plant Pathogens Soanes, Darren; Richards, Thomas A. Annual Review of Phytopathology, Vol. 52, Issue 1 https://doi.org/10.1146/annurev-phyto-102313-050127	journal	August 2014
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