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Title: Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis

Abstract

The dominant fungi in arid grasslands and shrublands are members of the Ascomycota phylum. Ascomycota fungi are important drivers in carbon and nitrogen cycling in arid ecosystems. These fungi play roles in soil stability, plant biomass decomposition, and endophytic interactions with plants. They may also form symbiotic associations with biocrust components or be latent saprotrophs or pathogens that live on plant tissues. However, their functional potential in arid soils, where organic matter, nutrients and water are very low or only periodically available, is poorly characterized. Five Ascomycota fungi were isolated from different soil crust microhabitats and rhizosphere soils around the native bunchgrass Pleuraphis jamesii in an arid grassland near Moab, UT, USA. Putative genera were Coniochaeta, isolated from lichen biocrust, Embellisia from cyanobacteria biocrust, Chaetomium from below lichen biocrust, Phoma from a moss microhabitat, and Aspergillus from the soil. The fungi were grown in replicate cultures on different carbon sources (chitin, native bunchgrass or pine wood) relevant to plant biomass and soil carbon sources. Secretomes produced by the fungi on each substrate were characterized. Results demonstrate that these fungi likely interact with primary producers (biocrust or plants) by secreting a wide range of proteins that facilitate symbiotic associations. Each ofmore » the fungal isolates secreted enzymes that degrade plant biomass, small secreted effector proteins, and proteins involved in either beneficial plant interactions or virulence. Aspergillus and Phoma expressed more plant biomass degrading enzymes when grown in grass- and pine-containing cultures than in chitin. Coniochaeta and Embellisia expressed similar numbers of these enzymes under all conditions, while Chaetomium secreted more of these enzymes in grass-containing cultures. This study of Ascomycota genomes and secretomes provides important insights about the lifestyles and the roles that Ascomycota fungi likely play in arid grassland, ecosystems. However, the exact nature of those interactions, whether any or all of the isolates are true endophytes, latent saprotrophs or opportunistic phytopathogens, will be the topic of future studies.« less

Authors:
ORCiD logo; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL); Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1618577
Alternate Identifier(s):
OSTI ID: 1580512; OSTI ID: 1603981
Report Number(s):
PNNL-SA-140986; LA-UR-16-29573; LA-UR-19-20737; LA-UR-18-25519
Journal ID: ISSN 1471-2164; 976; PII: 6358
Grant/Contract Number:  
AC05-76RL01830; 89233218CNA000001
Resource Type:
Published Article
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Name: BMC Genomics Journal Volume: 20 Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United Kingdom
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Ascomycota; Fungi; Arid; Grassland; Soil; Biocrust; Genome; Secretome; Lifestyle; Plants

Citation Formats

Challacombe, Jean F., Hesse, Cedar N., Bramer, Lisa M., McCue, Lee Ann, Lipton, Mary, Purvine, Samuel, Nicora, Carrie, Gallegos-Graves, La Verne, Porras-Alfaro, Andrea, and Kuske, Cheryl R. Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis. United Kingdom: N. p., 2019. Web. https://doi.org/10.1186/s12864-019-6358-x.
Challacombe, Jean F., Hesse, Cedar N., Bramer, Lisa M., McCue, Lee Ann, Lipton, Mary, Purvine, Samuel, Nicora, Carrie, Gallegos-Graves, La Verne, Porras-Alfaro, Andrea, & Kuske, Cheryl R. Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis. United Kingdom. https://doi.org/10.1186/s12864-019-6358-x
Challacombe, Jean F., Hesse, Cedar N., Bramer, Lisa M., McCue, Lee Ann, Lipton, Mary, Purvine, Samuel, Nicora, Carrie, Gallegos-Graves, La Verne, Porras-Alfaro, Andrea, and Kuske, Cheryl R. Thu . "Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis". United Kingdom. https://doi.org/10.1186/s12864-019-6358-x.
@article{osti_1618577,
title = {Genomes and secretomes of Ascomycota fungi reveal diverse functions in plant biomass decomposition and pathogenesis},
author = {Challacombe, Jean F. and Hesse, Cedar N. and Bramer, Lisa M. and McCue, Lee Ann and Lipton, Mary and Purvine, Samuel and Nicora, Carrie and Gallegos-Graves, La Verne and Porras-Alfaro, Andrea and Kuske, Cheryl R.},
abstractNote = {The dominant fungi in arid grasslands and shrublands are members of the Ascomycota phylum. Ascomycota fungi are important drivers in carbon and nitrogen cycling in arid ecosystems. These fungi play roles in soil stability, plant biomass decomposition, and endophytic interactions with plants. They may also form symbiotic associations with biocrust components or be latent saprotrophs or pathogens that live on plant tissues. However, their functional potential in arid soils, where organic matter, nutrients and water are very low or only periodically available, is poorly characterized. Five Ascomycota fungi were isolated from different soil crust microhabitats and rhizosphere soils around the native bunchgrass Pleuraphis jamesii in an arid grassland near Moab, UT, USA. Putative genera were Coniochaeta, isolated from lichen biocrust, Embellisia from cyanobacteria biocrust, Chaetomium from below lichen biocrust, Phoma from a moss microhabitat, and Aspergillus from the soil. The fungi were grown in replicate cultures on different carbon sources (chitin, native bunchgrass or pine wood) relevant to plant biomass and soil carbon sources. Secretomes produced by the fungi on each substrate were characterized. Results demonstrate that these fungi likely interact with primary producers (biocrust or plants) by secreting a wide range of proteins that facilitate symbiotic associations. Each of the fungal isolates secreted enzymes that degrade plant biomass, small secreted effector proteins, and proteins involved in either beneficial plant interactions or virulence. Aspergillus and Phoma expressed more plant biomass degrading enzymes when grown in grass- and pine-containing cultures than in chitin. Coniochaeta and Embellisia expressed similar numbers of these enzymes under all conditions, while Chaetomium secreted more of these enzymes in grass-containing cultures. This study of Ascomycota genomes and secretomes provides important insights about the lifestyles and the roles that Ascomycota fungi likely play in arid grassland, ecosystems. However, the exact nature of those interactions, whether any or all of the isolates are true endophytes, latent saprotrophs or opportunistic phytopathogens, will be the topic of future studies.},
doi = {10.1186/s12864-019-6358-x},
journal = {BMC Genomics},
number = 1,
volume = 20,
place = {United Kingdom},
year = {2019},
month = {12}
}

Journal Article:
Free Publicly Available Full Text
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https://doi.org/10.1186/s12864-019-6358-x

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  • Applied Microbiology and Biotechnology, Vol. 91, Issue 6, p. 1477-1492
  • DOI: 10.1007/s00253-011-3473-2

Characterization of extracellular lignocellulolytic enzymes of Coniochaeta sp. during corn stover bioconversion
journal, December 2012


<I>Coniochaeta</I> (<I>Lecythophora</I>), <I>Collophora</I> gen. nov. and <I>Phaeomoniella</I> species associated with wood necroses of <I>Prunus</I> trees
journal, June 2010

  • Damm, U.; Fourie, P. H.; Crous, P. W.
  • Persoonia - Molecular Phylogeny and Evolution of Fungi, Vol. 24, Issue 1
  • DOI: 10.3767/003158510X500705

A class-wide phylogenetic assessment of Dothideomycetes
journal, January 2009


A general suite of fungal endophytes dominate the roots of two dominant grasses in a semiarid grassland
journal, January 2010


Effectors of Filamentous Plant Pathogens: Commonalities amid Diversity
journal, March 2017

  • Franceschetti, Marina; Maqbool, Abbas; Jiménez-Dalmaroni, Maximiliano J.
  • Microbiology and Molecular Biology Reviews, Vol. 81, Issue 2
  • DOI: 10.1128/MMBR.00066-16

The toxicology mechanism of endophytic fungus and swainsonine in locoweed
journal, October 2016


Alternaria spp.: from general saprophyte to specific parasite
journal, July 2003


Soil Influences Colonization of Root-Associated Fungal Endophyte Communities of Maize, Wheat, and Their Progenitors
journal, January 2016

  • Bokati, Deepak; Herrera, José; Poudel, Ravin
  • Journal of Mycology, Vol. 2016
  • DOI: 10.1155/2016/8062073

Evolution and genome architecture in fungal plant pathogens
journal, August 2017

  • Möller, Mareike; Stukenbrock, Eva H.
  • Nature Reviews Microbiology, Vol. 15, Issue 12
  • DOI: 10.1038/nrmicro.2017.76

Fusarium verticillioides chitin synthases CHS5 and CHS7 are required for normal growth and pathogenicity
journal, January 2011


Fungal Beta-Glucosidases: A Bottleneck in Industrial Use of Lignocellulosic Materials
journal, September 2013

  • Sørensen, Annette; Lübeck, Mette; Lübeck, Peter
  • Biomolecules, Vol. 3, Issue 4
  • DOI: 10.3390/biom3030612

Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi
journal, April 2018


Arsenal of plant cell wall degrading enzymes reflects host preference among plant pathogenic fungi
journal, January 2011

  • King, Brian C.; Waxman, Katrina D.; Nenni, Nicholas V.
  • Biotechnology for Biofuels, Vol. 4, Issue 1
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Lignin degrading ability of selected aspergillus Spp.
journal, August 1984

  • Milstein, O. A.; Haars, A.; Sharma, A.
  • Applied Biochemistry and Biotechnology, Vol. 9, Issue 4
  • DOI: 10.1007/BF02798992

Chitin synthesis and fungal pathogenesis
journal, August 2010

  • Lenardon, Megan D.; Munro, Carol A.; Gow, Neil AR
  • Current Opinion in Microbiology, Vol. 13, Issue 4
  • DOI: 10.1016/j.mib.2010.05.002

Production of Pyomelanin, a Second Type of Melanin, via the Tyrosine Degradation Pathway in Aspergillus fumigatus
journal, November 2008

  • Schmaler-Ripcke, J.; Sugareva, V.; Gebhardt, P.
  • Applied and Environmental Microbiology, Vol. 75, Issue 2
  • DOI: 10.1128/AEM.02077-08

Analysis of cytochrome b5 reductase-mediated metabolism in the phytopathogenic fungus Zymoseptoria tritici reveals novel functionalities implicated in virulence
journal, September 2015


The Nep1-like proteins-a growing family of microbial elicitors of plant necrosis
journal, July 2004


Fungal Infection of Plants
journal, October 1996


Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi
journal, December 2012


Synthesis and assembly of fungal melanin
journal, December 2011

  • Eisenman, Helene C.; Casadevall, Arturo
  • Applied Microbiology and Biotechnology, Vol. 93, Issue 3
  • DOI: 10.1007/s00253-011-3777-2

The Lignicolous Fungus Coniochaeta pulveracea and Its Interactions with Syntrophic Yeasts from the Woody Phylloplane
journal, May 2011

  • van Heerden, Andrea; van Zyl, Willem H.; Cruywagen, Christiaan W.
  • Microbial Ecology, Vol. 62, Issue 3
  • DOI: 10.1007/s00248-011-9869-9

Plant Cell Wall Deconstruction by Ascomycete Fungi
journal, September 2013


Gibberella zeae chitin synthase genes, GzCHS5 and GzCHS7, are required for hyphal growth, perithecia formation, and pathogenicity
journal, June 2009


Extrolites of Aspergillus fumigatus and Other Pathogenic Species in Aspergillus Section Fumigati
journal, January 2016


New insights on trehalose: a multifunctional molecule
journal, January 2003


BREAKING AND ENTERING: Host Penetration by the Fungal Rice Blast Pathogen Magnaporthe grisea
journal, October 1996


The Magnaporthe oryzae Alt A 1-like protein MoHrip1 binds to the plant plasma membrane
journal, October 2017

  • Zhang, Yi; Liang, Yingbo; Dong, Yijie
  • Biochemical and Biophysical Research Communications, Vol. 492, Issue 1
  • DOI: 10.1016/j.bbrc.2017.08.039

MS-GF+ makes progress towards a universal database search tool for proteomics
journal, October 2014

  • Kim, Sangtae; Pevzner, Pavel A.
  • Nature Communications, Vol. 5, Issue 1
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Lignocellulose deconstruction in the biosphere
journal, December 2017

  • Bomble, Yannick J.; Lin, Chien-Yuan; Amore, Antonella
  • Current Opinion in Chemical Biology, Vol. 41
  • DOI: 10.1016/j.cbpa.2017.10.013

Tools of the crook- infection strategies of fungal plant pathogens
journal, January 2018

  • Rodriguez-Moreno, Luis; Ebert, Malaika K.; Bolton, Melvin D.
  • The Plant Journal, Vol. 93, Issue 4
  • DOI: 10.1111/tpj.13810