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Fungal Metabolism in Filamentous Fungi

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A special issue of Journal of Fungi (ISSN 2309-608X). This special issue belongs to the section "Fungal Cell Biology, Metabolism and Physiology".

Deadline for manuscript submissions: closed (31 January 2023) | Viewed by 24179

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Dr. Gwenaël Ruprich-Robert

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Laboratoire Interdisciplinaire des Energies de Demain (LIED), UMR 8236, CNRS, Université Paris Cité, F-75013 Paris, France
Interests: filamentous fungi; secondary metabolism; fungal genetics and genomics; fungal network
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Dr. Florence Chapeland-Leclerc

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Dear Colleagues,

The research carried out for many years on fungal secondary metabolites (SMs) has been divided into two branches: fundamental and applied. On the one hand, this research has provided a better understanding of the physiological functions of SMs, which are still largely unknown, even if we know that some of them play a crucial role in the “well-being” of the producing organisms. On the other hand, in terms of benefits to humans, filamentous fungi represent a limitless source of bioactive metabolites which can find applications in therapeutics, as exemplified by the antibiotic drug penicillin.

The recent availability of genome sequences for an increasing number of fungi has led to rapid progress in the identification of dozens of biosynthesis gene clusters potentially involved in SM production. Moreover, metabolomic approaches based on high-resolution mass spectrometry have emerged as a convenient tool to efficiently explore SM production, which could be associated with an efficient molecular networking bioinformatic approach. However, it remains that only a limited number of SM pathways have been elucidated in fungi because most of the fungal BGCs are “silent” under standard culture conditions, and the putative related natural products are then not produced. A variety of interesting strategies have been successfully developed to broaden the spectrum of SM production, such as (i) the one strain–many compounds (OSMAC) and co-culture approaches, (ii) the deletion/overexpression of cluster-specific transcription factors or global regulators, and (iii) the modulation of BGC expression mediated by chromatin regulation. Overall, these different approaches are all the more effective if they can be combined in interdisciplinary and integrated approaches. Here, we aim to present the latest advances in the characterization of new fungal SMs, whether from a fundamental perspective for a better understanding of fungal biology, or from a more applied point of view with the identification of molecules of interest.

Dr. Gwenaël Ruprich-Robert
Dr. Florence Chapeland-Leclerc
Guest Editors

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Keywords

secondary metabolism
filamentous fungi
biosynthesis gene cluster (BGC)
natural products
metabolism regulation
metabolomics
genomics
bioactive compounds
drug discovery

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Fungal Metabolism in Filamentous Fungi: 2nd Edition in Journal of Fungi (4 articles)

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Research

11 pages, 1950 KiB

Open AccessArticle

Melanin Induction Restores the Pathogenicity of Gaeumannomyces graminis var. tritici in Wheat Plants

by Camila Aranda, Isabel Méndez, Patricio Javier Barra, Luis Hernández-Montiel, Ana Fallard, Gonzalo Tortella, Evelyn Briones and Paola Durán

J. Fungi 2023, 9(3), 350; https://doi.org/10.3390/jof9030350 - 14 Mar 2023

Cited by 3 | Viewed by 2087

Abstract

One of the most challenging aspects of long-term research based on microorganisms is the maintenance of isolates under ex situ conditions, particularly the conservation of phytopathological characteristics. Our research group has worked for more than 10 years with Gaumannomyces graminis var. tritici (Ggt), the main biotic factor affecting wheat. In this sense we preserved the microorganisms in oil overlaid. However, several strains preserved for a long time lost their pathogenicity. These strains show white and non-infective mycelia. In this sense, we hypothesized that this is attributable to low melanin content. Melanin is a natural pigment mainly involved in UV protection, desiccation, salinity, oxidation, and fungal pathogenicity. Therefore, understanding the melanin role on Ggt pathogenicity is fundamental to developing melanin activation strategies under laboratory studies. In this study, we induce melanin activation by UV-A light chamber, 320 to 400 nm (T1) and temperature changes of 30 °C, 15 °C, and 20 °C (T2). Fungal pathogenicity was evaluated by determination of blackening roots and Ggt was quantified by real-time PCR in inoculated wheat plants. Results revealed that Ggt grown under UV-A (T1) conditions showed around 40% higher melanin level with a concomitant effect on root infection (98% of blackened roots) and 4-fold more Ggt genome copy number compared with the control (non-infective mycelia) being T1, a more inductor factor compared with T2. These findings would support the role of melanin in pathogenicity in darkly pigmented fungi such as Ggt and could serve as a basis for activating pathogenicity under laboratory conditions. Full article

(This article belongs to the Special Issue Fungal Metabolism in Filamentous Fungi)

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26 pages, 18109 KiB

Open AccessArticle

Mediator Subunit Med15 Regulates Cell Morphology and Mating in Candida lusitaniae

by Ayman Sabra, Nicolas Biteau, Jean-William Dupuy, Christophe Klopp, Thierry Noël and Karine Dementhon

J. Fungi 2023, 9(3), 333; https://doi.org/10.3390/jof9030333 - 8 Mar 2023

Cited by 1 | Viewed by 1882

Abstract

Candida lusitaniae is an emerging opportunistic pathogenic yeast capable of shifting from yeast to pseudohyphae form, and it is one of the few Candida species with the ability to reproduce sexually. In this study, we showed that a dpp3Δ mutant, inactivated for a putative pyrophosphatase, is impaired in cell separation, pseudohyphal growth and mating. The defective phenotypes were not restored after the reconstruction of a wild-type DPP3 locus, reinforcing the hypothesis of the presence of an additional mutation that we suspected in our previous study. Genetic crosses and genome sequencing identified an additional mutation in MED15, encoding a subunit of the mediator complex that functions as a general transcriptional co-activator in Eukaryotes. We confirmed that inactivation of MED15 was responsible for the defective phenotypes by rescuing the dpp3Δ mutant with a wild-type copy of MED15 and constructing a med15Δ knockout mutant that mimics the phenotypes of dpp3Δ in vitro. Proteomic analyses revealed the biological processes under the control of Med15 and involved in hyphal growth, cell separation and mating. This is the first description of the functions of MED15 in the regulation of hyphal growth, cell separation and mating, and the pathways involved in C. lusitaniae. Full article

(This article belongs to the Special Issue Fungal Metabolism in Filamentous Fungi)

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13 pages, 5145 KiB

Open AccessArticle

The Effect of Trichoderma harzianum Hypovirus 1 (ThHV1) and Its Defective RNA ThHV1-S on the Antifungal Activity and Metabolome of Trichoderma koningiopsis T-51

by Jiaqi You, Zheng Hu, Chaohan Li, Hongjuan Yang, Lihua Zhu, Biting Cao, Ronghao Song and Weihong Gu

J. Fungi 2023, 9(2), 175; https://doi.org/10.3390/jof9020175 - 28 Jan 2023

Cited by 2 | Viewed by 2287

Abstract

Mycoviruses widely exist in filamentous fungi and sometimes cause phenotypic changes in hosts. Trichoderma harzianum hypovirus 1 (ThHV1) and its defective RNA ThHV1-S were found in T. harzianum and exhibited high transmissibility. In our previous study, ThHV1 and ThHV1-S were transferred to an excellent biological control agent T. koningiopsis T-51 to form a derivative strain 51-13. In this study, we assessed the metabolic changes in strain 51-13 and antifungal activity of its culture filtrate (CF) and volatile organic compounds (VOCs). The antifungal activity of CF and VOCs of T-51 and 51-13 was different. Compared with the CF of T-51, that of 51-13 exhibited high inhibitory activity against B. cinerea, Sclerotinia sclerotiorum, and Stagonosporopsis cucurbitacearum but low inhibitory activity against Leptosphaeria biglobosa and Villosiclava virens. The VOCs of 51-13 exhibited high inhibitory activity against F. oxysporum but low inhibitory activity against B. cinerea. The transcriptomes of T-51 and 51-13 were compared; 5531 differentially expressed genes (DEGs) were identified in 51-13 with 2904 up- and 2627 downregulated genes. In KEGG enrichment analysis, 1127 DEGs related to metabolic pathways (57.53%) and 396 DEGs related to biosynthesis of secondary metabolites (20.21%) were clearly enriched. From the CF of T-51 and 51-13, 134 differential secondary metabolites (DSMs) were detected between T-51 and 51-13 with 39 up- and 95 downregulated metabolites. From these, 13 upregulated metabolites were selected to test their antifungal activity against B. cinerea. Among them, indole-3-lactic acid and p-coumaric acid methyl ester (MeCA) exhibited strong antifungal activity. The IC₅₀ of MeCA was 657.35 μM and four genes possibly related to the synthesis of MeCA exhibited higher expression in 51-13 than in T-51. This study revealed the mechanism underlying the increase in antifungal activity of T-51 because of the mycovirus and provided novel insights in fungal engineering to obtain bioactive metabolites via mycoviruses. Full article

(This article belongs to the Special Issue Fungal Metabolism in Filamentous Fungi)

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12 pages, 2497 KiB

Open AccessArticle

Nitrogen Enriched Solid-State Cultivation for the Overproduction of Azaphilone Red Pigments by Penicillium sclerotiorum SNB-CN111

by Téo Hebra, Véronique Eparvier and David Touboul

J. Fungi 2023, 9(2), 156; https://doi.org/10.3390/jof9020156 - 24 Jan 2023

Cited by 1 | Viewed by 1926

Abstract

Azaphilones are microbial specialized metabolites employed as yellow, orange, red or purple pigments. In particular, yellow azaphilones react spontaneously with functionalized nitrogen groups, leading to red azaphilones. In this study, a new two-step solid-state cultivation process to produce specific red azaphilones pigments was implemented, and their chemical diversity was explored based on liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS) and a molecular network. This two-step procedure first implies a cellophane membrane allowing accumulating yellow and orange azaphilones from a Penicillium sclerotiorum SNB-CN111 strain, and second involves the incorporation of the desired functionalized nitrogen by shifting the culture medium. The potential of this solid-state cultivation method was finally demonstrated by overproducing an azaphilone with a propargylamine side chain, representing 16% of the metabolic crude extract mass. Full article

(This article belongs to the Special Issue Fungal Metabolism in Filamentous Fungi)

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17 pages, 2254 KiB

Open AccessArticle

Complementary Strategies to Unlock Biosynthesis Gene Clusters Encoding Secondary Metabolites in the Filamentous Fungus Podospora anserina

by Ling Shen, Catherine Roullier, François-Hugues Porée, Thomas Gaslonde, Ludivine Riffault-Valois, Olivier Grovel, Gwenaël Ruprich-Robert and Florence Chapeland-Leclerc

J. Fungi 2023, 9(1), 9; https://doi.org/10.3390/jof9010009 - 21 Dec 2022

Cited by 1 | Viewed by 2123

Abstract

The coprophilous ascomycete Podospora anserina is known to have a high potential to synthesize a wide array of secondary metabolites (SMs). However, to date, the characterization of SMs in this species, as in other filamentous fungal species, is far less than expected by the functional prediction through genome mining, likely due to the inactivity of most SMs biosynthesis gene clusters (BGCs) under standard conditions. In this work, our main objective was to compare the global strategies usually used to deregulate SM gene clusters in P. anserina, including the variation of culture conditions and the modification of the chromatin state either by genetic manipulation or by chemical treatment, and to show the complementarity of the approaches between them. In this way, we showed that the metabolomics-driven comparative analysis unveils the unexpected diversity of metabolic changes in P. anserina and that the integrated strategies have a mutual complementary effect on the expression of the fungal metabolome. Then, our results demonstrate that metabolite production is significantly influenced by varied cultivation states and epigenetic modifications. We believe that the strategy described in this study will facilitate the discovery of fungal metabolites of interest and will improve the ability to prioritize the production of specific fungal SMs with an optimized treatment. Full article

(This article belongs to the Special Issue Fungal Metabolism in Filamentous Fungi)

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14 pages, 2581 KiB

Open AccessArticle

The Mitochondrial Alternative Oxidase in Ustilago maydis Is Not Involved in Response to Oxidative Stress Induced by Paraquat

by Lucero Romero-Aguilar, Héctor Vázquez-Meza, Guadalupe Guerra-Sánchez, Oscar Ivan Luqueño-Bocardo and Juan Pablo Pardo

J. Fungi 2022, 8(11), 1221; https://doi.org/10.3390/jof8111221 - 19 Nov 2022

Cited by 4 | Viewed by 1889

Abstract

It has been shown that the alternative oxidase in mitochondria of fungi and plants has important functions in the response against stress conditions, although their role in some organisms is still unknown. This is the case of Ustilago maydis. There is no evidence of the participation of the U. maydis Aox1 in stressful conditions such as desiccation, high or low temperature, and low pH, among others. Therefore, in this work, we studied the role of the U. maydis Aox1 in cells exposed to oxidative stress induced by methyl viologen (paraquat). To gain insights into the role of this enzyme, we took advantage of four strains: the FB2 wild-type, a strain without the alternative oxidase (FB2aox1Δ), other with the Aox1 fused to the Gfp under the control of the original promoter (FB2aox1-Gfp), and one expressing constitutively de Aox1-Gfp (FB2Potef:aox1-Gfp). Cells were incubated for various times in the presence of 1 mM paraquat and growth, replicative capacities, mitochondrial respiratory activity, Aox1 capacity, and the activities of several antioxidant enzymes (catalase, glutathione peroxidase, glutathione reductase, and superoxide dismutase) were assayed. The results show that (1) the response of U. maydis against oxidative stress was the same in the presence or absence of the Aox1; (2) the activities of the antioxidant enzymes remained constant despite the oxidative stress; and (3) there was a decrease in the GSH/GSSG ratio in U. maydis cells incubated with paraquat. Full article

(This article belongs to the Special Issue Fungal Metabolism in Filamentous Fungi)

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18 pages, 5740 KiB

Open AccessArticle

Disruption of the Chitin Biosynthetic Pathway Results in Significant Changes in the Cell Growth Phenotypes and Biosynthesis of Secondary Metabolites of Monascus purpureus

by Meng Shu, Pengxin Lu, Shuai Liu, Song Zhang, Zihan Gong, Xinru Cai, Bo Zhou, Qinlu Lin and Jun Liu

J. Fungi 2022, 8(9), 910; https://doi.org/10.3390/jof8090910 - 27 Aug 2022

Cited by 10 | Viewed by 2119

Abstract

In this study, the gene monascus-5162 from Monascus purpureus LQ-6, identified as chitin synthase gene VI (chs6), was knocked out to disrupt the chitin biosynthetic pathway and regulate the biosynthesis of Monascus pigments (MPs) and citrinin. The results showed that the aerial hyphae on a solid medium were short and sparse after the deletion of chs6 in M. purpureus LQ-6, significantly reducing the germination percentage of active spores to approximately 22%, but the colony diameter was almost unaffected. Additionally, the deletion of chs6 changed the mycelial morphology of M. purpureus LQ-6 during submerged fermentation and increased its sensitivity to environmental factors. MP and citrinin biosynthesis was dramatically inhibited in the recombinant strain. Furthermore, comparative transcriptome analysis revealed that the pathways related to spore development and growth, including the MAPK signaling pathway, chitin biosynthetic pathway, and regulatory factors LaeA and WetA genes, were significantly downregulated in the early phase of fermentation. The mRNA expression levels of genes in the cluster of secondary metabolites were significantly downregulated, especially those related to citrinin biosynthesis. This is the first detailed study to reveal that chs6 plays a vital role in regulating the cell growth and secondary metabolism of the Monascus genus. Full article

(This article belongs to the Special Issue Fungal Metabolism in Filamentous Fungi)

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11 pages, 2451 KiB

Open AccessArticle

New Insights into Methyl Jasmonate Regulation of Triterpenoid Biosynthesis in Medicinal Fungal Species Sanghuangporusbaumii (Pilát) L.W. Zhou & Y.C. Dai

by Zengcai Liu, Ruipeng Liu, Xinyu Tong and Li Zou

J. Fungi 2022, 8(9), 889; https://doi.org/10.3390/jof8090889 - 23 Aug 2022

Cited by 5 | Viewed by 1971

Abstract

Triterpenoids are secondary metabolites produced by the fungus Sanghuangporus baumii that have important pharmacological activities. However, the yield of triterpenoids is low and cannot meet market demand. Here, we treated S. baumii with several concentrations of MeJA (methyl jasmonate) and found that the total triterpenoid content was highest (23.31 mg/g) when the MeJA concentration was 250 μmol/L. qRT-PCR was used to quantify the transcription of five key genes involved in triterpenoid biosynthesis. The results showed that the relative transcription of most genes increased with increasing MeJA concentration, indicating that MeJA is a potent inducer of triterpenoid biosynthesis in S. baumii. To further explore whether other terpenoid biosynthesis pathways are also involved in the accumulation of triterpenoids induced by MeJA, we measured the contents of cis-Zeatin (cZ), gibberellins (GAs), and the transcript levels of related biosynthesis genes. We found that MeJA significantly inhibited the biosynthesis of cZ, GAs, and the transcription of related genes. The repressive effects of MeJA on cZ and GA accumulation were further confirmed by growth rate and biomass assays. In conclusion, our study provides an effective method to enhance the triterpenoid content of S. baumii, and also provides novel insights into the mechanism of MeJA-induced triterpenoid biosynthesis. Full article

(This article belongs to the Special Issue Fungal Metabolism in Filamentous Fungi)

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13 pages, 4078 KiB

Open AccessArticle

Genomic and AntiSMASH Analyses of Marine-Sponge-Derived Strain Aspergillus niger L14 Unveiling Its Vast Potential of Secondary Metabolites Biosynthesis

by Ping Wang, Shuang Xu, Yuqi Tang, Hong Wang, Xuelian Bai and Huawei Zhang

J. Fungi 2022, 8(6), 591; https://doi.org/10.3390/jof8060591 - 31 May 2022

Cited by 5 | Viewed by 4002

Abstract

Aspergillus niger is one of the most important sources of secondary metabolites (SMs), with a wide array of pharmacological effects, including anti-inflammatory, antitumor, immunomodulatory and antioxidant effects. However, the biosynthetic analysis of these bioactive components has been rarely reported owing to the lack of high-quality genome sequences and comprehensive analysis. In this study, the whole genome of one marine-sponge-derived strain A. niger L14 was sequenced and assembled as well as in-depth bioinformatic analysis. The results indicated that the sequence assembly of strain L14 generated one high-quality genome with a total size of 36.1 Mb, a G + C content of 45.3% and an N50 scaffold of 4.2 Mb. Gene annotation was extensively deployed using various BLAST databases, including non-redudant (Nr) protein sequence, nucleotide (Nt) sequence, Swiss-Prot, Gene ontology (GO), Kyoto Encyclopedia of Genes and Genomes (KEGG) and Clusters of Orthologous Groups (COG) as well as Pathogen Host Interactions (PHI) and Carbohydrate-active enzymes (CAZy) databases. AntiSMASH analysis revealed that this marine strain harbors a total of 69 SMs biosynthesis gene clusters (BGCs), including 17 PKSs, 18 NRPSs, 21 NRPS-likes, 9 terpenes, 2 indoles, 1 betalactone and 1 siderophore, suggesting its biosynthetic potential to produce a wide variety of SMs. These findings will assist in future investigations on the genetic basis of strain L14 and provide insights into its new bioactive SMs for new drug discovery. Full article

(This article belongs to the Special Issue Fungal Metabolism in Filamentous Fungi)

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13 pages, 3027 KiB

Open AccessArticle

Integrated Transcriptomics and Nontargeted Metabolomics Analysis Reveal Key Metabolic Pathways in Ganoderma lucidum in Response to Ethylene

by Li Meng, Ruyue Zhou, Jialong Lin, Qingji Wang, Panmeng Wang, Wei Wang, Li Wang and Zhuang Li

J. Fungi 2022, 8(5), 456; https://doi.org/10.3390/jof8050456 - 28 Apr 2022

Cited by 9 | Viewed by 2375

Abstract

Ganoderic acid (GA) is an important secondary metabolite of Ganoderma lucidum with a diverse array of pharmacological properties. In this study, we found that exogenous ethylene increased the production of endogenous ethylene and ganoderic acid in G. lucidum. However, the mechanism by which ethylene is regulated remains unclear. As a result, we performed a combined transcriptomics and nontargeted metabolomics analysis to evaluate the regulatory mechanism of ethylene. A total of 4070 differentially expressed genes (1835 up-regulated and 2235 down-regulated) and 378 differentially accumulated metabolites (289 up-regulated and 89 down-regulated) were identified in all groups. The transcriptomics and nontargeted metabolomics data revealed that genes involved in the tricarboxylic acid (TCA) cycle, polyamine metabolic pathway, acetyl-CoA carboxylase (ACC) pathway, and triterpenoid metabolism were up-regulated, whereas the metabolic intermediates involved in these metabolic pathways were down-regulated. These findings imply that ethylene potentially accelerates normal glucose metabolism, hence increasing the number of intermediates available for downstream biological processes, including polyamine metabolism, ethylene synthesis pathway, and ganoderic acid biosynthesis. The findings will contribute significantly to our understanding of secondary metabolites biosynthesis in fungi. Full article

(This article belongs to the Special Issue Fungal Metabolism in Filamentous Fungi)

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