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Genomic Analysis of Aspergillus Section Terrei Reveals a High Potential in Secondary Metabolite Production and Plant Biomass Degradation.

ABSTRACT: Aspergillus terreus has attracted interest due to its application in industrial biotechnology, particularly for the production of itaconic acid and bioactive secondary metabolites. As related species also seem to possess a prosperous secondary metabolism, they are of high interest for genome mining and exploitation. Here, we present draft genome sequences for six species from Aspergillus section Terrei and one species from Aspergillus section Nidulantes. Whole-genome phylogeny confirmed that section Terrei is monophyletic. Genome analyses identified between 70 and 108 key secondary metabolism genes in each of the genomes of section Terrei, the highest rate found in the genus Aspergillus so far. The respective enzymes fall into 167 distinct families with most of them corresponding to potentially unique compounds or compound families. Moreover, 53% of the families were only found in a single species, which supports the suitability of species from section Terrei for further genome mining. Intriguingly, this analysis, combined with heterologous gene expression and metabolite identification, suggested that species from section Terrei use a strategy for UV protection different to other species from the genus Aspergillus. Section Terrei contains a complete plant polysaccharide degrading potential and an even higher cellulolytic potential than other Aspergilli, possibly facilitating additional applications for these species in biotechnology.

SUBMITTER: Theobald S

PROVIDER: S-EPMC11278011 | biostudies-literature | 2024 Jul

REPOSITORIES: biostudies-literature

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Genomic Analysis of Aspergillus Section Terrei Reveals a High Potential in Secondary Metabolite Production and Plant Biomass Degradation.

Theobald Sebastian S Vesth Tammi C TC Geib Elena E Nybo Jane L JL Frisvad Jens C JC Larsen Thomas O TO Kuo Alan A LaButti Kurt K Lyhne Ellen K EK Kjærbølling Inge I Ledsgaard Line L Barry Kerrie K Clum Alicia A Chen Cindy C Nolan Matt M Sandor Laura L Lipzen Anna A Mondo Stephen S Pangilinan Jasmyn J Salamov Asaf A Riley Robert R Wiebenga Ad A Müller Astrid A Kun Roland S RS Dos Santos Gomes Ana Carolina AC Henrissat Bernard B Magnuson Jon K JK Simmons Blake A BA Mäkelä Miia R MR Mortensen Uffe H UH Grigoriev Igor V IV Brock Matthias M Baker Scott E SE de Vries Ronald P RP Andersen Mikael R MR

Journal of fungi (Basel, Switzerland) 20240722 7

Aspergillus terreus has attracted interest due to its application in industrial biotechnology, particularly for the production of itaconic acid and bioactive secondary metabolites. As related species also seem to possess a prosperous secondary metabolism, they are of high interest for genome mining and exploitation. Here, we present draft genome sequences for six species from Aspergillus section Terrei and one species from Aspergillus section Nidulantes. Whole- ...[more]

PMID: 39057392

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Project description:Section Terrei of Aspergillus was studied using a polyphasic approach including sequence analysis of parts of the ?-tubulin and calmodulin genes and the ITS region, macro- and micromorphological analyses and examination of extrolite profiles to describe three new species in this section. Based on phylogenetic analysis of calmodulin and ?-tubulin sequences seven lineages were observed among isolates that have previously been treated as A. terreus and its subspecies by Raper & Fennell (1965) and others. Aspergillus alabamensis, A. terreus var. floccosus, A. terreus var. africanus, A. terreus var. aureus, A. hortai and A. terreus NRRL 4017 all represent distinct lineages from the A. terreus clade. Among them, A. terreus var. floccosus, A. terreus NRRL 4017 and A. terreus var. aureus could also be distinguished from A. terreus by using ITS sequence data. New names are proposed for A. terreus var. floccosus, A. terreus var. africanus, A. terreus var. aureus, while Aspergillus hortai is recognised at species level. Aspergillus terreus NRRL 4017 is described as the new species A. pseudoterreus. Also included in section Terrei are some species formerly placed in sections Flavipedes and Versicolores. A. clade including the type isolate of A. niveus (CBS 115.27) constitutes a lineage closely related to A. carneus. Fennellia nivea, the hypothesized teleomorph is not related to this clade. Aspergillus allahabadii, A. niveus var. indicus, and two species originally placed in section Versicolores, A. ambiguus and A. microcysticus, also form well-defined lineages on all trees. Species in Aspergillus section Terrei are producers of a diverse array of secondary metabolites. However, many of the species in the section produce different combinations of the following metabolites: acetylaranotin, asperphenamate, aspochalamins, aspulvinones, asteltoxin, asterric acid, asterriquinones, aszonalenins, atrovenetins, butyrolactones, citreoisocoumarins, citreoviridins, citrinins, decaturins, fulvic acid, geodins, gregatins, mevinolins, serantrypinone, terreic acid (only the precursor 3,6-dihydroxytoluquinone found), terreins, terrequinones, terretonins and territrems. The cholesterol-lowering agent mevinolin was found in A. terreus and A. neoafricanus only. The hepatotoxic extrolite citrinin was found in eight species: A. alabamensis, A. allahabadii, A. carneus, A. floccosus, A. hortai, A. neoindicus, A. niveus and A. pseudoterreus. The neurotoxic extrolite citreoviridin was found in five species: A. neoafricanus, A. aureoterreus, A. pseudoterreus, A. terreus and A. neoniveus. Territrems, tremorgenic extrolites, were found in some strains of A. alabamensis and A. terreus.

Project description:BackgroundFermentation of sugars derived from plant biomass feedstock is crucial for sustainability. Hence, utilizing customized enzymatic cocktails to obtain oligosaccharides instead of monomers is an alternative fermentation strategy to produce prebiotics, cosmetics, and biofuels. This study developed an engineered strain of Aspergillus niger producing a tailored cellulolytic cocktail capable of partially degrading sugarcane straw to yield cellooligosaccharides.ResultsThe A. niger prtT∆ strain created resulted in a reduced extracellular protease production. The prtT∆ background was then used to create strains by deleting exoenzyme encoding genes involved in mono- or disaccharide formation. Consequently, we successfully generated a tailored prtT∆bglA∆ strain by eliminating a beta-glucosidase (bglA) gene and subsequently deleted two cellobiohydrolases and one beta-xylosidase encoding genes using a multiplex strategy, resulting in the Quintuple∆ strain (prtT∆; bglA∆; cbhA∆; cbhB∆; xlnD∆). When applied for sugarcane biomass degradation, the tailored secretomes produced by A. niger resulted in a higher ratio of cellobiose and cellotriose compared with glucose relative to the reference strain. Mass spectrometry revealed that the Quintuple∆ strain secreted alternative cellobiohydrolases and beta-glucosidases to compensate for the absence of major cellulases. Enzymes targeting minor polysaccharides in plant biomass were also upregulated in this tailored strain.ConclusionTailored secretome use increased COS/glucose ratio during sugarcane biomass degradation showing that deleting some enzymatic components is an effective approach for producing customized enzymatic cocktails. Our findings highlight the plasticity of fungal genomes as enzymes that target minor components of plant cell walls, and alternative cellulases were produced by the mutant strain. Despite deletion of important secretome components, fungal growth was maintained in plant biomass.

Dataset Information

Genomic Analysis of Aspergillus Section Terrei Reveals a High Potential in Secondary Metabolite Production and Plant Biomass Degradation.

Publications

Genomic Analysis of <i>Aspergillus</i> Section <i>Terrei</i> Reveals a High Potential in Secondary Metabolite Production and Plant Biomass Degradation.

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