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Comparative Transcriptomics Analysis of the Responses of the Filamentous Fungus Glarea lozoyensis to Different Carbon Sources.

ABSTRACT: The natural product pneumocandin B0 is the precursor of the antifungal drug caspofungin. We found that replacing glucose in the initial fermentation medium with 20 g/L fructose is more conducive to pneumocandin B0 production and biomass accumulation. In order to explore the mechanism of the different metabolic responses to fructose and glucose, we used each as the sole carbon source, and the results showed that fructose increased the total pneumocandin B0 yield and biomass by 54.76 and 13.71%, respectively. Furthermore, we analyzed the differences of gene expression and metabolic pathways between the two different carbon sources by transcriptomic analysis. When fructose was used as the carbon source, genes related to the pentose phosphate pathway (PPP), glycolysis and branched-chain amino acid metabolism were significantly upregulated, resulting in increased intracellular pools of NADPH and acetyl-CoA in Glarea lozoyensis for cell growth and pneumocandin B0 product synthesis. Interestingly, the pneumocandin B0 biosynthetic gene cluster and the genes of the TCA cycle were significantly downregulated, while the FAS genes were significantly upregulated, indicating that more acetyl-CoA was used for fatty acid synthesis. In particular, we found that excessive synthesis of fatty acids caused lipid accumulation, and lipid droplets can sequester lipophilic secondary metabolites such as pneumocandin B0 to reduce cell damage, which may also be an important reason for the observed increase of pneumocandin B0 yield. These results provide new insights into the relationship between pneumocandin B0 biosynthesis and carbon sources in G. lozoyensis. At the same time, this study provides important genomic information for improving pneumocandin B0 production through metabolic engineering strategies in the future.

SUBMITTER: Zhang K

PROVIDER: S-EPMC7040073 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Comparative Transcriptomics Analysis of the Responses of the Filamentous Fungus Glarea lozoyensis to Different Carbon Sources.

Zhang Ke K Huang Baoqi B Yuan Kai K Ji Xiaojun X Song Ping P Ding Qingqing Q Wang Yuwen Y

Frontiers in microbiology 20200218

The natural product pneumocandin B0 is the precursor of the antifungal drug caspofungin. We found that replacing glucose in the initial fermentation medium with 20 g/L fructose is more conducive to pneumocandin B0 production and biomass accumulation. In order to explore the mechanism of the different metabolic responses to fructose and glucose, we used each as the sole carbon source, and the results showed that fructose increased the total pneumocandin B0 yield a ...[more]

PMID: 32132986

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Project description:UNLABELLED:Operons are multigene transcriptional units which occur mostly in prokaryotes but rarely in eukaryotes. Protein-coding operons have not been reported in the Fungi even though they represent a very diverse kingdom of organisms. Here, we report a functional operon involved in the secondary metabolism of the fungus Glarea lozoyensis belonging to Leotiomycetes (Ascomycota). Two contiguous genes, glpks3 and glnrps7, encoding polyketide synthase and nonribosomal peptide synthetase, respectively, are cotranscribed into one dicistronic mRNA under the control of the same promoter, and the mRNA is then translated into two individual proteins, GLPKS3 and GLNRPS7. Heterologous expression in Aspergillus nidulans shows that the GLPKS3-GLNRPS7 enzyme complex catalyzes the biosynthesis of a novel pyrrolidinedione-containing compound, xenolozoyenone (compound 1), which indicates the operon is functional. Although it is structurally similar to prokaryotic operons, the glpks3-glnrps7 operon locus has a monophylogenic origin from fungi rather than having been horizontally transferred from prokaryotes. Moreover, two additional operons, glpks28-glnrps8 and glpks29-glnrps9, were verified at the transcriptional level in the same fungus. This is the first report of protein-coding operons in a member of the Fungi. IMPORTANCE:Operons are multigene transcriptional units which occur mostly in prokaryotes but rarely in eukaryotes. Three operon-like gene structures for secondary metabolism that were discovered in the filamentous fungus Glarea lozoyensis are the first examples of protein-coding operons identified in a member of the Fungi. Among them, the glpks3-glnrps7 operon is responsible for the biosynthesis of xenolozoyenone, which is a novel tetramic acid-containing compound. Although structurally similar to prokaryotic operons, the glpks3-glnrps7 operon locus did not result from horizontal gene transfer from prokaryotes. In addition, operonlike structures have been predicted in silico to be common in other fungi. The common occurrence and operonlike structure in fungi provide evolutionary insight and essential data for eukaryotic gene transcription.

Dataset Information

Comparative Transcriptomics Analysis of the Responses of the Filamentous Fungus Glarea lozoyensis to Different Carbon Sources.

Publications

Comparative Transcriptomics Analysis of the Responses of the Filamentous Fungus <i>Glarea lozoyensis</i> to Different Carbon Sources.

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