Award Abstract # 1441604
Collaborative Research: The Zygomycetes Genealogy of Life (ZyGoLife)- the conundrum of Kingdom Fungi

NSF Org: DEB
Division Of Environmental Biology
Recipient: OREGON STATE UNIVERSITY
Initial Amendment Date: August 26, 2014
Latest Amendment Date: September 12, 2016
Award Number: 1441604
Award Instrument: Standard Grant
Program Manager: Amanda Ingram
DEB
 Division Of Environmental Biology
BIO
 Directorate for Biological Sciences
Start Date: January 1, 2015
End Date: December 31, 2019 (Estimated)
Total Intended Award Amount: $625,000.00
Total Awarded Amount to Date: $625,000.00
Funds Obligated to Date: FY 2014 = $625,000.00
History of Investigator:
  • Joseph Spatafora (Principal Investigator)
    spatafoj@science.oregonstate.edu
  • Michael Krings (Co-Principal Investigator)
  • Thomas Taylor (Former Co-Principal Investigator)
Recipient Sponsored Research Office: Oregon State University
1500 SW JEFFERSON AVE
CORVALLIS
OR  US  97331-8655
(541)737-4933
Sponsor Congressional District: 04
Primary Place of Performance: Oregon State University
Corvallis
OR  US  97331-8507
Primary Place of Performance
Congressional District:
04
Unique Entity Identifier (UEI): MZ4DYXE1SL98
Parent UEI:
NSF Program(s): GoLife
Primary Program Source: 01001415DB NSF RESEARCH & RELATED ACTIVIT
Program Reference Code(s): 6133, 9169, EGCH
Program Element Code(s): 613300
Award Agency Code: 4900
Fund Agency Code: 4900
Assistance Listing Number(s): 47.074

ABSTRACT

Fungi comprise one of the most successful groups of life on Earth. They inhabit most of the world's environments, where they perform numerous functions (e.g., nutrient cycling, foundations of food webs, etc.) that are central to healthy ecosystems. Importantly, fungi interact with all other forms of life, including plants, animals and bacteria -- in associations that range from beneficial to antagonistic. Zygomycete fungi, the focus of this research project, are an ancient group in which most of the morphological and ecological traits associated with Kingdom Fungi first arose, but their evolutionary history and ecological associations have not yet been well resolved. This project will reconstruct the genealogical relationships of this earliest branch in fungal evolutionary history, resolve the origins of symbiotic relationships between plants and zygomycetes, reveal how complex body plans evolved in the group, elucidate mechanisms of mating genetics between organisms with complex and differing life cycles, and develop genomic barcodes to facilitate identification of unknown fungi. The results of this research will contribute to many scientific disciplines and to society. Expanding and maintaining expertise on these fungi is critical for the field of biology, human health and productivity, and safe food production. This project includes training of the next generation of mycologists, dissemination of information on basic fungal biology, development of teaching resources, expansion of biological database and web resources, development of research materials including strain cultures and genomes for the wider scientific community, and broadening of participation of underrepresented groups in STEM disciplines.

Zygomycetes are filamentous fungi that lack flagella and that produce simple but defined reproductive structures. An initial analysis of zygomycete genomes support the hypothesis that the group is a pivotal transition point between certain flagellated Fungi and their specific life histories, and what became the dominant eukaryotic terrestrial clade of Fungi (the fleshy fungi, e.g., mushrooms). Because the zygomycetes are the first terrestrial fungi that exhibit fruiting bodies, understanding how these structures evolved will provide a basis for understanding the origins of complex morphogenesis (e.g., multicellularity) in the Fungi, as well as the evolution of complex life histories. Zygomycetes also display a diversity of ecological relationships with plants (mycorrhizae), animals (pathogens) and bacteria (endosymbionts). Resolving the phylogenetic origins of these interactions will provide an evolutionary framework for elucidating molecular and biochemical mechanisms that govern these interactions, and in doing so, will have direct impacts on research into natural and managed ecosystems and human welfare. This research will also refine molecular environmental sampling techniques, resulting in a more accurate census of zygomycete biodiversity, especially in soil ecosystems. By gathering orders of magnitude more genome-scale data and integrating it with biochemical, morphological, subcellular, and fossil data layers, this elusive region of the fungal genealogy of life will be illuminated and will provide a foundation for broad scale biological research.

PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH

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(Showing: 1 - 10 of 14)
Chang Y, Desiro A, Na H, Sandor L, Lipzen A, Clum A, Barry K, Grigoriev I, Martin F, Stajich J, Smith M, Bonito G, Spatafora JW "Phylogenomics of Endogonaceae and evolution of mycorrhizae within Mucoromycota" New Phytologist , 2019 10.1111/nph.15613
Davis WJ, Chang Y, Amses K, Stajich JE, Benny G, Smith M, Spatafora JW, Grigoriev I, Carter-House D, James TY. "Genome-scale phylogenetics analyses reveals a monophyletic Zoopagales (Zoopagomycota, Fungi) with predacious taxa evolving from mycoparasite ancestors" Molecular Phylogenetic and Evolution , v.133 , 2019 , p.152
Harper, C.J., Krings, M., Dotzler, N., Taylor, E.L. & Taylor, T.N. "Deciphering interfungal relationships in the 410-million-yr-old Rhynie chert: Morphology and development of vesicle-colonizing microfungi" Geobios , v.50 , 2017 , p.9
Harper, C.J., Taylor, E.L., Walker, C., White, J.F., Serbet, R. & Krings, M "Fungal sporulation in a Permian plant fragment from Antarctica" Bulletin of Geosciences , v.93 , 2018 , p.13
Krings, M. & Harper, C.J. "Additional observations on the fungal reproductive unit Windipila spinifera from the Windyfield chert, and description of a similar form, Windipila pumila nov. sp., from the nearby Rhynie chert (Lower Devonian, Scotland)" Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen , v.288 , 2018 , p.235
Krings, M. & Harper, C.J. "A mantled fungal reproductive unit from the Lower Devonian Windyfield chert, Scotland, with prominent spines and otherwise shaped projections extending out from the mantle" Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen , v.285 , 2017 , p.201
Krings, M. & Harper, C.J. "Deciphering interfungal relationships in the 410-million-yr-old Rhynie chert: Glomoid spores under attack" Geobios , v.51 , 2018 , p.151
Krings, M., Harper, C.J., White, J.F., Barthel, M., Heinrichs, J., Taylor, E.L. & Taylor, T.N. "Fungi in a Psaronius root mantle from the Rotliegend (Asselian, Lower Permian/Cisuralian) of Thuringia, Germany" Review of Palaeobotany and Palynology , v.239 , 2017 , p.14
Mondo SJ, Dannebaum RO, Kuo RC, Louie K, LaButti K, Haridas A, Kuo A, Salamov A, Ahrendt SR, Bewick AJ, Lau R, Bowen B, Lipzen A, Sullivan W, Andreopoulos WB, Clum A, Lindquist E, Daum C, Northen TR, Ramamoorthy G, Schmitz RJ, Gryganskyi A, Culley D, Magn "Widespread Adenine N6-methylation of Active Genes in Fungi" Nature Genetics , v.49 , 2017 , p.964 10.1038/ng.3859
Myers JM, Bonds AE, Clemon RA, Thapa NA, Simmon DR, Carter-House D, Ortanez J, Liu P, Miralles-Durán, Desirò A, Longcore JE, Bonito G, Stajich JE, Spatafora JW, Chang Y, Corrochano LM, Gryganskyi A, Grigoriev IV, James TY. "Survey of Early-Diverging Lineages of Fungi Reveals Abundant and Diverse Mycoviruses." mBIO , v.11 , 2020 , p.e02027-20 10.1128/mBio.02027-20.
Spatafora JW, Aime CA, Grigoriev IV, Martin F, Stajich JE, Blackwell M "The Fungal Tree of Life: from molecular systematics to genome-scale phylogenies" Microbiology Spectrum , v.5 , 2017 , p.FUNK-0053 10.1128/microbiolspec.FUNK-0053-2016
(Showing: 1 - 10 of 14)

PROJECT OUTCOMES REPORT

Disclaimer

This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.

The Kingdom Fungi comprises one of the largest and most ecologically important groups of organisms on Earth. Fungi provide numerous essential functions including serving as beneficial partners and antagonistic pathogens with plants and animals, and central players in nutrient cycling through decomposition of most organic substrates. They are also an old kingdom, dating back to approximately 1 billion years. During their evolution they have undergone numerous biological transformations, which included morphological and biochemical innovations, that allowed them to move from aquatic environments and colonize early land ecosystems. These innovations include the loss of flagellum, the origin of the filamentous growth form that comprises the “body” of most fungi, and the ability to execute an extraordinary diversity of biochemical processes. Central to the evolution of these innovations, and the initial colonization of land, are a group of fungi known as the zygomycetes. Zygomycetes are common, but because they are microscopic and do not produce large fruiting bodies like mushrooms, they are significantly understudied. To advance our understanding of this critical group of organisms, we initiated the ZyGoLife project, which consisted of a large and diverse group of collaborative researchers.  Our goal was to collect large amounts of different types of data and integrate these data in testing hypotheses focused on the evolution and diversity of zygomycetes.  A summary of the major findings from this work include: 1) We clarified the relationships of the major lineages of Kingdom Fungi, and demonstrated that zygomycete fungi comprise two separate lineages, representing the first groups of fungi to lose the flagellum and colonize land. 2) Zygomycete fungi colonized land prior to plants and include some of the first fungi that plants formed symbiotic associations with when they evolved into terrestrial ecosystems. 3) We adopted and modified analytical techniques for sequencing the genomes of fungi that are currently not possible to maintain in pure culture. This will significantly promote the sequencing of fungi that cannot be cultured and participate in complex relationships with other organisms. 4) We sequenced the genomes of over 100 species of zygomycetes, across a phylogenetic diversity spanning over 100s of millions of years.  This depth and breadth of sampling allowed us to uncover previously undescribed metabolic diversity of fungi, and link it in a predictive manner with fungal ecology. 5) We demonstrated that Basidiobolus, a gastrointestinal symbiont of amphibians, represents a system for understanding Horizontal Gene Transfer between fungi and bacteria, and that this process is likely facilitated by the unique environmental conditions of the amphibian gastrointestinal system.  Fungal-bacterial interactions are common in nature but their dynamics are poorly understood. The Basidiobolus-amphibian symbiosis provides a tractable, experimental system for the study of the acquisition of novel metabolism by fungi and fungal-bacterial microbiome interactions. Notably, this research significantly increased the genomic resources available to the global research community.  Prior to ZyGoLife, there existed scant genomic resources for zygomycete fungi; after ZyGoLife there now exists hundreds of zygomycete genomes. This exponential increase in resources strengthens and advances basic and foundational research in genetics, genomics and computational biology of fungi, allowing the transfer of knowledge from model systems to a greater diversity of organisms.  As such, it stands to have broad impact in research related to biodiversity, ecology and conservation, complex interactions between fungi and other organisms, plant and human pathology, and bioprospecting for biologically active compounds with potential industrial and pharmaceutical applications. Importantly, research supported by this grant involved the cross-training of the next generation of young scientists in fungal biology, genomics and computational biology, who must be able to work in large, collaborative groups and approach scientific inquiry through the analysis of complex, heterogeneous data sets.


Last Modified: 12/31/2020
Modified by: Joseph W Spatafora

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