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Title: Decoding the chemical language of Suillus fungi: genome mining and untargeted metabolomics uncover terpene chemical diversity

Journal Article · · mSystems
ORCiD logo [1];  [2];  [1];  [2];  [3]; ORCiD logo [3]; ; ;
  1. UT-ORNL Graduate School of Genome Science and Technology, University of Tennessee, Knoxville, Tennessee, USA, Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA
  2. Biology Department, Duke University, Durham, North Carolina, USA
  3. Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA

ABSTRACT Ectomycorrhizal fungi establish mutually beneficial relationships with trees, trading nutrients for carbon. Suillus are ectomycorrhizal fungi that are critical to the health of boreal and temperate forest ecosystems. Comparative genomics has identified a high number of non-ribosomal peptide synthetase and terpene biosynthetic gene clusters (BGC) potentially involved in fungal competition and communication. However, the functionality of these BGCs is not known. This study employed co-culture techniques to activate BGC expression and then used metabolomics to investigate the diversity of metabolic products produced by three Suillus species ( Suillus hirtellus EM16, Suillus decipiens EM49, and Suillus cothurnatus VC1858), core members of the pine microbiome. After 28 days of growth on solid media, liquid chromatography–tandem mass spectrometry identified a diverse range of extracellular metabolites (exometabolites) along the interaction zone between Suillus co-cultures. Prenol lipids were among the most abundant chemical classes. Out of the 62 unique terpene BGCs predicted by genome mining, 41 putative prenol lipids (includes 37 putative terpenes) were identified across the three Suillus species using metabolomics. Notably, some terpenes were significantly more abundant in co-culture conditions. For example, we identified a metabolite matching to isomers isopimaric acid, sandaracopimaric acid, and abietic acid, which can be found in pine resin and play important roles in host defense mechanisms and Suillus spore germination. This research highlights the importance of combining genomics and metabolomics to advance our understanding of the chemical diversity underpinning fungal signaling and communication. IMPORTANCE Using a combination of genomics and metabolomics, this study’s findings offer new insights into the chemical diversity of Suillus fungi, which serve a critical role in forest ecosystems.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
National Institutes of Health (NIH); USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
AC05-00OR22725; SC0020403
OSTI ID:
2323377
Journal Information:
mSystems, Journal Name: mSystems Journal Issue: 4 Vol. 9; ISSN 2379-5077
Publisher:
American Society for MicrobiologyCopyright Statement
Country of Publication:
United States
Language:
English

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