In this SFA, we are developing novel bioinformatic and experimental tools and resources for the identification and characterization of bacterial-fungal interactions that occur within complex natural microbiomes. The theoretical framework of this project is built upon gaining a more comprehensive understanding of how bacteria and fungi sense, respond to, and co-evolve with one another through multi-omics-based interrogations. A more complete understanding of the molecular mechanisms and dialogues underlying interactions between bacteria and fungi allows us to interrogate how the dynamics of these relationships are altered in the context of environmental change (i.e., moisture, nutrient availability, temperature). Through these studies, we hope to gain a predictive understanding of how these interactions impact microbiome function and how they may be altered to steer the function of soil ecosystems and increase resilience to climate change and other environmental perturbations.
Goals and Aims
The primary goal of this SFA is to gain a fundamental understanding of how to identify, characterize, and interrogate interactions between bacteria and fungi that occur within complex microbiomes. Our research approach integrates novel bioinformatic and experimental approaches in a complementary fashion. A systematic approach wherein we examine interactions at various levels of complexity (i.e., organismal, co-cultures, and community) ensures a more complete understanding of how interactions between bacteria and fungi are formed and how they are impacted by the environment. The development of bioinformatic resources such as databases and pipelines by our team also facilitates standardized investigations of BFI and ensure scientific growth within the field.
Our ten-year program vision is to gain insight into the molecular mechanisms underlying interactions between diverse bacterial and fungal taxa and how these interactions are impacted by environmental perturbations such as warming and drought. This knowledge will be fundamental to understanding how complex environmental microbiomes can be steered to accomplish DOE mission goals such as increasing plant productivity and increasing resiliency to climate change. The project aligns with several BSSD science and technology goals including, but not limited to the development of tools and techniques to manipulate microbiomes for beneficial purposes, facilitating novel and innovative approaches to functional gene characterizations, seeking a mechanistic understanding of cell-to-cell interactions and signaling at various scales, and consideration of complex interkingdom biological dependencies among soil microbial community members.
Video 1. Time-lapse of Trichoderma harzianum germination
Video 2. 3D visualization of endobacteria in fungi
Video 3. Panning zoom of the distribution of Endobacteria (cyan) found ubiquitously across the fungal mycelia (magenta).
Morales DP, Robinson AJ, Pawlowski AC, Ark C, Kelliher JM, Junier P, Werner JH, Chain PSG. (2022). Advances and Challenges in Fluorescence in situ Hybridization for Visualizing Fungal Endobacteria. Frontiers in Microbiology 13 (2022). doi: 10.3389/fmicb.2022.892227.
Lupini S, Peña-Bahamonde J, Bonito G, and Rodrigues DF. Effect of Endosymbiotic Bacteria on Fungal Resistance Toward Heavy Metals. Frontiers in Microbiology 13, (2022). doi:10.3389/fmicb.2022.822541.
Estoppey A, Weisskopf L, Di Francesco E, Vallat-Michel A, Bindschedler S, Chain PS, and Junier P. 2022. Improved methods to assess the effect of bacteria on germination of fungal spores. FEMS Microbiology Letters. 369(1): fnac034. doi: 10.1093/femsle/fnac034.
Zheng AO, Sher A, Fridman D, Musante CJ, & Young JD. (2022). Pool size measurements improve precision of flux estimates but increase sensitivity to unmodeled reactions outside the core network in isotopically nonstationary metabolic flux analysis (INST-MFA). Biotechnology Journal, 17, e2000427. doi: 10.1002/biot.202000427.
Robinson AJ, Daligault HE, Kelliher JM, LeBrun ES, Chain PSG. Multiple Cases of Bacterial Sequence Erroneously Incorporated into Publicly Available Chloroplast Genomes. Frontiers in Genetics. 12 (2022). doi: 10.3389/fgene.2021.821715.
Robinson AJ, House GL, Morales DP, Kelliher JM, Gallegos-Graves LV, LeBrun ES, Davenport KW, Palmieri F, Lohberger A, Bregnard D, Estoppey A, Buffi M, Paul C, Junier T, Hervé V, Cailleau G, Lupini S, Nguyen HN, Zheng AO, Gimenes LJ, Bindschedler S, Rodrigues DF, Werner JH, Young JD, Junier P, and Chain PSG. Widespread bacterial diversity within the bacteriome of fungi. Communications Biology 4, 1168 (2021). doi: 10.1038/s42003-021-02693-y.
Hervé V, Simon A, Randevoson F, Cailleau G, Rajoelison G, Razakamanarivo H, Bindschedler S, Verrecchia E, Junier, P. Functional Diversity of the Litter-Associated Fungi from an Oxalate-Carbonate Pathway Ecosystem in Madagascar. Microorganisms 2021, 9, 985. doi: 10.3390/microorganisms9050985. In the Special Issue: Fungal Ecology in Plant Decomposition.
Gimeno A, Stanley CE, Ngamenie Z, Hsung MH, Walder F, Schieder SS, Bindschedler S, Junier P, Keller B, and Vogelgsang S. 2021. A versatile microfluidic platform measures hyphal interactions between Fusarium graminearum and Clonostachysrosea in real-time. Communications Biology. 4:262. doi: 10.1038/s42003-021-01767-1.
Junier P, Cailleau G, Palmieri I, Valloton C, Trautschold O, Junier T, Paul C, Bregnard D, Palmieri F, Estoppey A, Buffi M, Lohbgerger A, Robinson A, Kelliher J, Davenport K, House G, Morales D, Gallegos-Graves L, Dichosa A, Lupini S, Nguyen H, Young JD, Rodriguez D, Parra-Vasquez N, Bindschedler S, and P.S. Chain. 2021. Democratization of fungal highway columns as a tool to investigate bacteria associated with soil fungi. FEMS Microbiology Ecology. 11;97:fiab003. doi: 10.1093/femsec/fiab003. Selected as Editor’s choice.
Allen, D. K., J. D. Young, 2020: Tracing metabolic flux through time and space with isotope labeling experiments. Current Opinion in Biotechnology, 64:92-100. https://www.sciencedirect.com/science/article/pii/S095816691301132
Hashmi, I., C. Paul, A. Al-Dourobi, F. Sandoz, P. Deschamps, T. Junier, P. Junier, and S Bindschedler, 2019: Comparison of the plant growth promotion performance of a consortium of Bacilli inoculated as endospores or as vegetative cells. FEMS Microbiology Ecology, 95. https://doi.org/10.1093/femsec/fiz147
Robinson, A. J., D. O. Natvig, and P. S. G Chain, 2020. Genomic Analysis of Diverse Members of the Fungal Genus Monosporascus Reveals Novel Lineages, Unique Genome Content and a Potential Bacterial Associate. G3: Genes, Genomes, Genetics, 10:2573-2583. https://doi.org/10.1534/g3.120.401489
Paul, C., S. Filippidou, I. Jamil, W. Kooli, G. House, A. Estoppey, M. Hayoz, T. Junier, F. Palmieri, T. Wunderlin, A. Lehmann, S. Bindschedler, T. Vennemann, P. S. G. Chain, and Junier, P. 2019. Chapter Three - Bacterial spores, from ecology to biotechnology, in Advances in Applied Microbiology, G.M. Gadd and S. Sariaslani, Editors. 2019, Academic Press. p. 79-111.
Lohberger, A., J. E. Spangenberg, Y. Ventura, S. Bindschedler, E. P. Verrecchia, R. Bshary, P. Junier, 2019: 46 Effect of Organic Carbon and Nitrogen on the Interactions of Morchella spp. and Bacteria Dispersing on Their Mycelium. Frontiers in Microbiology, 10:124. https://doi.org/10.3389/fmicb.2019.00124
Palmieri, F., A. Estoppey, G. L. House, A. Lohberger, S. Bindschedler, P. S. G. Chain, and P. Junier, 2019: Oxalic acid, a molecule at the crossroads of bacterial-fungal interactions. Advances in Applied Microbiology, 106:49-77. https://doi.org/10.1016/bs.aambs.2018.10.001
Nguyen, H. N., C. Chaves-Lopez, R. C. Oliveira, A. Paparella, and D. F. Rodrigues, 2019: Cellular and metabolic approaches to investigate the effects of graphene and graphene oxide in the fungi Aspergillus flavus and Aspergillus niger. Carbon, 143, 419-429. https://doi.org/10.1016/j.carbon.2018.10.099
Amann, R. I., S. Baichoo, B. J. Blencowe, P. Bork, M. Borodovsky, C. Brooksbank, P. S. G. Chain, R. R. Colwell, D. G. Daffonchio, A. Danchin, V. de Lorenzo, P. C. Dorrestein, R. D. Finn, C. M. Fraser, J. A. Gilbert, S. J. Hallam, P. Hugenholtz, J. P. A. Ioannidis, J. K. Jansson, J. F. Kim, H. P. Klenk, M. G. Klotz, R. Knight, K. T. Konstantinidis, N. C. Kyrpides, C. E. Mason, A. C. McHardy, F. Meyer, C. A. Ouzounis, A. A. N. Patrinos, M. Podar, K. S. Pollard, J. Ravel, A. R. Muñoz, R. J. Roberts, R. Rosselló-Móra, S. A. Sansone, P. D. Schloss, L. M. Schriml, J. C. Setubal, R. Sorek, R. L. Stevens, J. M. Tiedje, A. Turjanski, G. W. Tyson, D. W. Ussery, G. M. Weinstock, O. White, W. B. Whitman, and I. Xenarios, 2019: Toward unrestricted use of public genomic data. Science, 363:350-352. https://doi.org/10.1126/science.aaw1280
Paul C, S. Filippidou, I. Jamil, W. Kooli, G. L. House, A. Estoppey, M. Hayoz, T. Junier, F. Palmieri, T. Wunderlin, A. Lehmann, S. Bindschedler, T. Vennemann, P. S. G. Chain, and P. Junier, 2019: Bacterial spores, from ecology to biotechnology. Advances in Applied Microbiology, 106:79-111. https://doi.org/10.1016/bs.aambs.2018.10.002
Chaves-Lopez, C., H. N. Nguyen, R. C. Oliveira, E. T. Nadres, A. Paparella, and D. F. Rodrigues, 2018: A morphological, enzymatic and metabolic approach to elucidate apoptotic-like cell death in fungi exposed to h-and α-molybdenum trioxide nanoparticles. Nanoscale, 10, 20702-20716. https://doi.org/10.1039/c8nr06470a
Deveau, A., G. Bonito, J. Uehling, M. Paoletti, M. Becker, S. Bindschedler, S. Hacquard, V. Hervé, J. Labbé, O. A. Lastovetsky, S. Mieszkin, L. J. Millet, B. Vajna, P. Junier, P. Bonfante, B. P. Krom, S. Olsson, J. D. van Elsas, and L. Y. Wick, 2018: Bacterial-fungal interactions: ecology, mechanisms and challenges. FEMS Microbiology Reviews, 42(3):335-352. https://doi.org/10.1093/femsre/fuy008