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Genomics and Transcriptomics Analyses of the Oil-Accumulating Basidiomycete Yeast Trichosporon oleaginosus: Insights into Substrate Utilization and Alternative Evolutionary Trajectories of Fungal Mating Systems

Journal Article · · mBio (Online)
 [1];  [2];  [2];  [3];  [4];  [4];  [4];  [4];  [4];  [4];  [4];  [5];  [5];  [2];  [3]
  1. Ruhr Univ., Bochum (Germany). Junior Research Group for Microbial Biotechnology; DOE/OSTI
  2. Technische Univ. Munchen, Garching (Germany). Fachgebiet Industrielle Biokatalyse
  3. Ruhr Univ., Bochum (Germany). Junior Research Group for Microbial Biotechnology
  4. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  5. Duke Univ., Durham, NC (United States). Medical Center. Department of Molecular Genetics and Microbiology
Microbial fermentation of agro-industrial waste holds great potential for reducing the environmental impact associated with the production of lipids for industrial purposes from plant biomass. However, the chemical complexity of many residues currently prevents efficient conversion into lipids, creating a high demand for strains with the ability to utilize all energy-rich components of agricultural residues. Here, we present results of genome and transcriptome analyses of Trichosporon oleaginosus. This oil-accumulating yeast is able to grow on a wide variety of substrates, including pentoses and N-acetylglucosamine, making it an interesting candidate for biotechnological applications. Transcriptomics shows specific changes in gene expression patterns under lipid-accumulating conditions. Furthermore, gene content and expression analyses indicate that T. oleaginosus is well-adapted for the utilization of chitin-rich biomass. We also focused on the T. oleaginosus mating type, because this species is a member of the Tremellomycetes, a group that has been intensively analyzed as a model for the evolution of sexual development, the best-studied member being Cryptococcus neoformans. The structure of the T. oleaginosus mating-type regions differs significantly from that of other Tremellomycetes and reveals a new evolutionary trajectory paradigm. Comparative analysis shows that recruitment of developmental genes to the ancestral tetrapolar mating-type loci occurred independently in the Trichosporon and Cryptococcus lineages, supporting the hypothesis of a trend toward larger mating-type regions in fungi. IMPORTANCE: Finite fossil fuel resources pose sustainability challenges to society and industry. Microbial oils are a sustainable feedstock for biofuel and chemical production that does not compete with food production. We describe genome and transcriptome analyses of the oleaginous yeast Trichosporon oleaginosus, which can accumulate up to 70% of its dry weight as lipids. In contrast to conventional yeasts, this organism not only shows an absence of diauxic effect while fermenting hexoses and pentoses but also effectively utilizes xylose and N-acetylglucosamine, which are building blocks of lignocellulose and chitin, respectively. Transcriptome analysis revealed metabolic networks that govern conversion of xylose or N-acetylglucosamine as well as lipid accumulation. These data form the basis for a targeted strain optimization strategy. Furthermore, analysis of the mating type of T. oleaginosus supports the hypothesis of a trend toward larger mating-type regions in fungi, similar to the evolution of sex chromosomes in animals and plants.
Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
Federal Ministry for Education and Research (BMBF); German Research Foundation (DFG); Ministry for Innovation, Science and Investigation of the State of North Rhine-Westphalia; National Institutes of Health (NIH); USDOE Office of Science (SC)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1626122
Journal Information:
mBio (Online), Journal Name: mBio (Online) Journal Issue: 4 Vol. 6; ISSN 2150-7511
Publisher:
American Society for Microbiology (ASM)Copyright Statement
Country of Publication:
United States
Language:
English

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Cocoa butter-like lipid production ability of non-oleaginous and oleaginous yeasts under nitrogen-limited culture conditions journal February 2017
Distribution of methionine sulfoxide reductases in fungi and conservation of the free-methionine-R-sulfoxide reductase in multicellular eukaryotes journal June 2021
Lipid and DHA-production in Aurantiochytrium sp. – Responses to nitrogen starvation and oxygen limitation revealed by analyses of production kinetics and global transcriptomes journal December 2019
Convergent evolution of linked mating-type loci in basidiomycete fungi journal August 2019
Fungal Sex: The Basidiomycota book September 2017
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The pH Signaling Transcription Factor PAC-3 Regulates Metabolic and Developmental Processes in Pathogenic Fungi journal September 2019
Distribution and Diversity of Cytochrome P450 Monooxygenases in the Fungal Class Tremellomycetes journal June 2019
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Biology, dynamics, and applications of transposable elements in basidiomycete fungi journal January 2017
Genetic engineering and production of modified fatty acids by the non-conventional oleaginous yeast Trichosporon oleaginosus ATCC 20509 journal January 2016
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Identification of new signalling peptides through a genome-wide survey of 250 fungal secretomes journal January 2019
The effects of TORC signal interference on lipogenesis in the oleaginous yeast Trichosporon oleaginosus journal March 2017
Opportunities and challenges in the development of Cutaneotrichosporon oleaginosus ATCC 20509 as a new cell factory for custom tailored microbial oils journal October 2017
Metabolism of aromatics by Trichosporon oleaginosus while remaining oleaginous journal November 2017
Convergent evolution of linked mating-type loci in basidiomycete fungi journal September 2019

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