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1. Fungal elemental profiling unleashed through rapid laser-induced breakdown spectroscopy (LIBS)

Author

Tomás A. Rush, Ann M. Wymore, Miguel Rodríguez, Jr, Sara Jawdy, Rytas J. Vilgalys, Madhavi Z. Martin, and Hunter B. Andrews

Subjects
fungal behavior, elemental profiling, ionomics, endophytes, poplar, LIBS, Microbiology, QR1-502
Abstract

ABSTRACT Elemental profiling of fungal species as a phenotyping tool is an understudied topic and is typically performed to examine plant tissue or non-biological materials. Traditional analytical techniques such as inductively coupled plasma–optical emission spectroscopy (ICP-OES) and inductively coupled plasma–mass spectrometry (ICP-MS) have been used to identify elemental profiles of fungi; however, these techniques can be cumbersome due to the difficulty of preparing samples. Additionally, the instruments used for these techniques can be expensive to procure and operate. Laser-induced breakdown spectroscopy (LIBS) is an alternative elemental analytical technique—one that is sensitive across the periodic table, easy to use on various sample types, and is cost-effective in both procurement and operation. LIBS has not been used on axenic filamentous fungal isolates grown in substrate media. In this work, as a proof of concept, we used LIBS on two genetically distinct fungal species grown on a nutrient-rich and nutrient-poor substrate media to determine whether robust elemental profiles can be detected and whether differences between the fungal isolates can be identified. Our results demonstrate a distinct correlation between fungal species and their elemental profile, regardless of the substrate media, as the same strains shared a similar uptake of carbon, zinc, phosphorus, manganese, and magnesium, which could play a vital role in their survival and propagation. Independently, each fungal species exhibited a unique elemental profile. This work demonstrates a unique and valuable approach to rapidly phenotype fungi through optical spectroscopy, and this approach can be critical in understanding these fungi's behavior and interactions with the environment.IMPORTANCEHistorically, ionomics, the elemental profiling of an organism or materials, has been used to understand the elemental composition in waste materials to identify and recycle heavy metals or rare earth elements, identify the soil composition in space exploration on the moon or Mars, or understand human disorders or disease. To our knowledge, ionomic profiling of microbes, particularly fungi, has not been investigated to answer applied and fundamental biological questions. The reason is that current ionomic analytical techniques can be laborious in sample preparation, fail to measure all potential elements accurately, are cost-prohibitive, or provide inconsistent results across replications. In our previous efforts, we explored whether laser-induced breakdown spectroscopy (LIBS) could be used in determining the elemental profiles of poplar tissue, which was successful. In this proof-of-concept endeavor, we undertook a transdisciplinary effort between applied and fundamental mycology and elemental analytical techniques to address the biological question of how LIBS can used for fungi grown axenically in a nutrient-rich and nutrient-poor environment.

Published
2024
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2. LaeA-Regulated Fungal Traits Mediate Bacterial Community Assembly

Author

Joanna Tannous, Casey M. Cosetta, Milton T. Drott, Tomás A. Rush, Paul E. Abraham, Richard J. Giannone, Nancy P. Keller, and Benjamin E. Wolfe

Subjects
Penicillium, fungal metabolites, microbiome, Microbiology, QR1-502
Abstract

ABSTRACT Potent antimicrobial metabolites are produced by filamentous fungi in pure culture, but their ecological functions in nature are often unknown. Using an antibacterial Penicillium isolate and a cheese rind microbial community, we demonstrate that a fungal specialized metabolite can regulate the diversity of bacterial communities. Inactivation of the global regulator, LaeA, resulted in the loss of antibacterial activity in the Penicillium isolate. Cheese rind bacterial communities assembled with the laeA deletion strain had significantly higher bacterial abundances than the wild-type strain. RNA-sequencing and metabolite profiling demonstrated a striking reduction in the expression and production of the natural product pseurotin in the laeA deletion strain. Inactivation of a core gene in the pseurotin biosynthetic cluster restored bacterial community composition, confirming the role of pseurotins in mediating bacterial community assembly. Our discovery demonstrates how global regulators of fungal transcription can control the assembly of bacterial communities and highlights an ecological role for a widespread class of fungal specialized metabolites. IMPORTANCE Cheese rinds are economically important microbial communities where fungi can impact food quality and aesthetics. The specific mechanisms by which fungi can regulate bacterial community assembly in cheeses, other fermented foods, and microbiomes in general are largely unknown. Our study highlights how specialized metabolites secreted by a Penicillium species can mediate cheese rind development via differential inhibition of bacterial community members. Because LaeA regulates specialized metabolites and other ecologically relevant traits in a wide range of filamentous fungi, this global regulator may have similar impacts in other fungus-dominated microbiomes.

Published
2023
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3. Lipo-Chitooligosaccharides Induce Specialized Fungal Metabolite Profiles That Modulate Bacterial Growth

Author

Tomás A. Rush, Joanna Tannous, Matthew J. Lane, Muralikrishnan Gopalakrishnan Meena, Alyssa A. Carrell, Jacob J. Golan, Milton T. Drott, Sylvain Cottaz, Sébastien Fort, Jean-Michel Ané, Nancy P. Keller, Dale A. Pelletier, Daniel A. Jacobson, David Kainer, Paul E. Abraham, Richard J. Giannone, and Jesse L. Labbé

Subjects
lipo-chitooligosaccharides, secondary metabolites, synergism, biosynthetic gene clusters, bacteria, Aspergillus, Microbiology, QR1-502
Abstract

ABSTRACT Lipo-chitooligosaccharides (LCOs) are historically known for their role as microbial-derived signaling molecules that shape plant symbiosis with beneficial rhizobia or mycorrhizal fungi. Recent studies showing that LCOs are widespread across the fungal kingdom have raised questions about the ecological function of these compounds in organisms that do not form symbiotic relationships with plants. To elucidate the ecological function of these compounds, we investigate the metabolomic response of the ubiquitous human pathogen Aspergillus fumigatus to LCOs. Our metabolomics data revealed that exogenous application of various types of LCOs to A. fumigatus resulted in significant shifts in the fungal metabolic profile, with marked changes in the production of specialized metabolites known to mediate ecological interactions. Using network analyses, we identify specific types of LCOs with the most significant effect on the abundance of known metabolites. Extracts of several LCO-induced metabolic profiles significantly impact the growth rates of diverse bacterial species. These findings suggest that LCOs may play an important role in the competitive dynamics of non-plant-symbiotic fungi and bacteria. This study identifies specific metabolomic profiles induced by these ubiquitously produced chemicals and creates a foundation for future studies into the potential roles of LCOs as modulators of interkingdom competition. IMPORTANCE The activation of silent biosynthetic gene clusters (BGC) for the identification and characterization of novel fungal secondary metabolites is a perpetual motion in natural product discoveries. Here, we demonstrated that one of the best-studied symbiosis signaling compounds, lipo-chitooligosaccharides (LCOs), play a role in activating some of these BGCs, resulting in the production of known, putative, and unknown metabolites with biological activities. This collection of metabolites induced by LCOs differentially modulate bacterial growth, while the LCO standards do not convey the same effect. These findings create a paradigm shift showing that LCOs have a more prominent role outside of host recognition of symbiotic microbes. Importantly, our work demonstrates that fungi use LCOs to produce a variety of metabolites with biological activity, which can be a potential source of bio-stimulants, pesticides, or pharmaceuticals.

Published
2022
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4. Lipo-chitooligosaccharides as regulatory signals of fungal growth and development

Author

Candice L. Swift, Arthur QuyManh Maes, Nancy P. Keller, Cristobal Carrera Carriel, Kevin Garcia, Guillaume Bécard, Joanna Tannous, Quanita J. Choudhury, Jean-Michel Ané, Michelle A. O’Malley, Junko Maeda, Jin Woo Bok, Michelle Keller-Pearson, Tomás Allen Rush, Patricia Jargeat, Virginie Puech-Pagès, Sylvain Cottaz, Michael R. Sussman, Fabienne Maillet, Jeniel E. Nett, Adeline Bascaules, Jessy Labbé, Kevin R. Cope, Alexandra Haouy, Bailey Kleven, Véréna Poinsot, Chad J. Johnson, Sébastien Fort, Corinne Lefort, Devanshi Khokhani, Fort, Sébastien, University of Wisconsin-Madison, Oak Ridge National Laboratory [Oak Ridge] (ORNL), UT-Battelle, LLC, Evolution des Interactions Plantes-Microorganismes, Laboratoire de Recherche en Sciences Végétales (LRSV), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Metatoul - Agromix, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Interactions moléculaires et réactivité chimique et photochimique (IMRCP), Institut de Chimie de Toulouse (ICT-FR 2599), Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Evolution et Diversité Biologique (EDB), Laboratoire des Interactions Plantes Microbes Environnement (LIPME), Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), South Dakota State University (SDSTATE), North Carolina State University [Raleigh] (NC State), University of North Carolina System (UNC), The University of Tennessee [Knoxville], University of Georgia [USA], University of California [Santa Barbara] (UC Santa Barbara), University of California (UC), Centre de Recherches sur les Macromolécules Végétales (CERMAV), Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA), Université Fédérale Toulouse Midi-Pyrénées, Interactions Microbiennes dans la Rhizosphère et les Racines, Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-MetaToul-MetaboHUB, Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie du CNRS (INC)-Institut de Chimie de Toulouse (ICT-FR 2599), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut de Chimie du CNRS (INC)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, University of California [Santa Barbara] (UCSB), University of California, Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS), MetaToul Agromix, Université de Toulouse (UT)-Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-MetaboHUB-MetaToul, MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Université de Toulouse (UT)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-MetaboHUB-Génopole Toulouse Midi-Pyrénées [Auzeville] (GENOTOUL), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université de Toulouse (UT)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Institut de Chimie de Toulouse (ICT), Université de Toulouse (UT)-Université de Toulouse (UT)-Institut de Chimie du CNRS (INC)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Institut Ecologie et Environnement (INEE), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Fédération de Recherche Fluides, Energie, Réacteurs, Matériaux et Transferts (FERMAT), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Université Toulouse III - Paul Sabatier (UT3), Université de Toulouse (UT)-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université de Toulouse (UT)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), BIBAC - Chimie analytique et interactions biomolécules - matière molle biomimétique (BIBAC), Institut National des Sciences Appliquées (INSA)-Université de Toulouse (UT)-Institut National des Sciences Appliquées (INSA)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Institut de Chimie de Toulouse (ICT), Université de Toulouse (UT), and ANR-17-EURE-0003,CBH-EUR-GS,CBH-EUR-GS(2017)

Subjects
0301 basic medicine, Hypha, Science, General Physics and Astronomy, Oligosaccharides, Chitin, 02 engineering and technology, Biology, General Biochemistry, Genetics and Molecular Biology, Article, Microbiology, Microbial ecology, 03 medical and health sciences, Fungal biology, Pseudohyphal growth, Symbiosis, Ascomycota, Mycorrhizae, Spore germination, [SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biochemistry [q-bio.BM], Cellular microbiology, Fungal ecology, lcsh:Science, [SDV.BBM.BC] Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biochemistry [q-bio.BM], [SDV.MP.MYC]Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, Chitosan, Multidisciplinary, Ecology, Phylum, Basidiomycota, Fatty Acids, fungi, Fungi, General Chemistry, Spores, Fungal, 021001 nanoscience & nanotechnology, biology.organism_classification, [SDV.MP.MYC] Life Sciences [q-bio]/Microbiology and Parasitology/Mycology, Spore, 030104 developmental biology, lcsh:Q, 0210 nano-technology, Bacteria, Rhizobium, Signal Transduction
Abstract

Lipo-chitooligosaccharides (LCOs) are signaling molecules produced by rhizobial bacteria that trigger the nodulation process in legumes, and by some fungi that also establish symbiotic relationships with plants, notably the arbuscular and ecto mycorrhizal fungi. Here, we show that many other fungi also produce LCOs. We tested 59 species representing most fungal phyla, and found that 53 species produce LCOs that can be detected by functional assays and/or by mass spectroscopy. LCO treatment affects spore germination, branching of hyphae, pseudohyphal growth, and transcription in non-symbiotic fungi from the Ascomycete and Basidiomycete phyla. Our findings suggest that LCO production is common among fungi, and LCOs may function as signals regulating fungal growth and development., Lipo-chitooligosaccharides (LCOs) are signaling molecules produced by certain bacteria and fungi that establish symbiotic relationships with plants. Here, the authors show that LCOs are produced also by many other, non-symbiotic fungi, and regulate fungal growth and development.

Published
2020
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5. The genus Meira: phylogenetic placement and description of a new species

Author

Tomás Allen Rush and M. Catherine Aime

Subjects
Molecular Sequence Data, DNA, Ribosomal, Microbiology, Exobasidiales, Phylogenetics, Genus, DNA, Ribosomal Spacer, Botany, RNA, Ribosomal, 18S, Cluster Analysis, DNA, Fungal, Mycological Typing Techniques, Molecular Biology, Phylogeny, Ustilaginomycotina, biology, Phylogenetic tree, Basidiomycota, Fungal genetics, Genes, rRNA, RNA, Fungal, Exobasidiomycetes, Sequence Analysis, DNA, General Medicine, biology.organism_classification, Incertae sedis, United States, Plant Leaves, Magnolia, RNA, Ribosomal, Evolutionary biology
Abstract

The genus Meira currently contains three recently described species of mite-associated basidiomycete yeasts from Israel and Japan and is placed in the Exobasidiomycetes (Ustilaginomycotina) Incertae sedis. A previously undescribed species of Meira was isolated from the phylloplane of a magnolia leaf in Louisiana, USA. Herein, we describe Meira miltonrushii sp. nov. and include phylogenetic analyses from three rDNA loci to resolve the placement of Meira. This study provides evidence that Meira belongs to the family Brachybasidiaceae in the Exobasidiales and supports the placement of another mite-associated yeast genus, Acaromyces, within Cryptobasidiaceae (Exobasidiales). We also examine sequences produced by numerous environmental studies that suggest Meira species can be found as endophytes of many plant species. To our knowledge, this is the first record of a member of the genus Meira in North America.

Published
2013
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