Comparative Genome-Wide Analysis Underscores the Rapid Expansion of Cytochrome P450s for Secondary Metabolism in the Mycoparasite Pezizomycetes
Abstract
:1. Introduction
2. Materials and Methods
2.1. Species and Database
2.2. Genome Mining of Mycoparasites for P450s
2.3. Assigning P450 Family and Subfamily
2.4. Phylogenetic Analysis
Species Name | Genome Version | Phylum | Class | Species Code | Genome Database Link | Reference |
---|---|---|---|---|---|---|
Ampelomyces quisqualis HMLAC05119 | v1.0 | Ascomycota | Pezizomycotina | Ampqui1 | https://mycocosm.jgi.doe.gov/Ampqui1 | [5] |
Clonostachys rosea IK726 | Ascomycota | Pezizomycotina | Cloros1 | https://mycocosm.jgi.doe.gov/Cloros1 | [7] | |
Escovopsis weberi CC031208-10 | Ascomycota | Pezizomycotina | Escweb1 | https://mycocosm.jgi.doe.gov/Escweb1 | [12] | |
Naematelia encephela UCDFST 68-887.2 | v1.0 | Ascomycota | Pezizomycotina | Treen1 | https://mycocosm.jgi.doe.gov/Treen1 | [7] |
Trichoderma arundinaceum IBT 40837 | Ascomycota | Pezizomycotina | Triaru1 | https://mycocosm.jgi.doe.gov/Triaru1 | [16] | |
Trichoderma asperelloides T203 | v1.0 | Ascomycota | Pezizomycotina | Triasper1 | https://mycocosm.jgi.doe.gov/Triasper1 | [17] |
Trichoderma asperellum CBS 433.97 | v1.0 | Ascomycota | Pezizomycotina | Trias1 | https://mycocosm.jgi.doe.gov/Trias1 | [19] |
Trichoderma atroviride | v2.0 | Ascomycota | Pezizomycotina | Triat2 | https://mycocosm.jgi.doe.gov/Triat2 | [17] |
Trichoderma citrinoviride TUCIM 6016 | v4.0 | Ascomycota | Pezizomycotina | Trici4 | https://mycocosm.jgi.doe.gov/Trici4 | [23] |
Trichoderma gamsii T6085 | Ascomycota | Pezizomycotina | Trigam1 | https://mycocosm.jgi.doe.gov/Trigam1 | [17] | |
Trichoderma guizhouense NJAU 4742 | Ascomycota | Pezizomycotina | Trigui1 | https://mycocosm.jgi.doe.gov/Trigui1 | [25] | |
Trichoderma hamatum GD12 | Ascomycota | Pezizomycotina | Triham1 | https://mycocosm.jgi.doe.gov/Triham1 | [17] | |
Trichoderma harzianum CBS 226.95 | v1.0 | Ascomycota | Pezizomycotina | Triha1 | https://mycocosm.jgi.doe.gov/Triha1 | [17] |
Trichoderma longibrachiatum ATCC 18648 | v3.0 | Ascomycota | Pezizomycotina | Trilo3 | https://mycocosm.jgi.doe.gov/Trilo3 | [53] |
Trichoderma pleuroti TPhu1 | Ascomycota | Pezizomycotina | Triple1 | https://mycocosm.jgi.doe.gov/Triple1 | [19] | |
Trichoderma virens Gv29-8 | v2.0 | Ascomycota | Pezizomycotina | TriviGv29_8_2 | https://mycocosm.jgi.doe.gov/TriviGv29_8_2 | [19] |
Tremella mesenterica Fries | v1.0 | Basidiomycota | Agaricomycotina | Treme1 | https://mycocosm.jgi.doe.gov/Treme1 | [15] |
Caulochytrium protostelioides ATCC 52028 single-cell | v1.0 | Caulochytriomycota | Caulochytriomycotina | Caupr_SCcomb | https://mycocosm.jgi.doe.gov/Caupr_Sccomb | [7] |
Caulochytrium protostelioides ATCC 52028 | v1.0 | Caulochytriomycota | Caulochytriomycotina | Caupr1 | https://mycocosm.jgi.doe.gov/Caupr1 | [8] |
Dimargaris cristalligena RSA 468 single-cell | v1.0 | Kickxellomycota | Kickxellomycotina | DimcrSC1 | https://mycocosm.jgi.doe.gov/DimcrSC1 | [10] |
Piptocephalis cylindrospora RSA 2659 single-cell | v3.0 | Zoopagomycota | Zoopagomycotina | Pipcy3_1 | https://mycocosm.jgi.doe.gov/Pipcy3_1 | [54] |
Syncephalis pseudoplumigaleata Benny S71-1 single-cell | v1.0 | Zoopagomycota | Zoopagomycotina | Synps1 | https://mycocosm.jgi.doe.gov/Synps1 | [7] |
Thamnocephalis sphaerospora RSA 1356 single-cell | v1.0 | Zoopagomycota | Zoopagomycotina | Thasp1 | https://mycocosm.jgi.doe.gov/Thasp1 | [7] |
Rozella allomycis CSF55 | Rozellomycota | Rozal1_1 | https://mycocosm.jgi.doe.gov/Rozal1_1 | [7] |
2.5. Identification of P450s That Are Part of Secondary-Metabolite BGCs (SMBGCs)
2.6. Saprophytic and Ectomycorrhizal Pezizomycete P450s and SMBGCs
2.7. Functional Prediction of P450s
3. Results and Discussion
3.1. Pezizomycete Mycoparasites Have More P450s in Their Genomes
3.2. Pezizomycete Mycoparasites Have Highly Diverse P450 Families and Subfamilies
3.3. Mycoparasites Have a Large and Diverse Number of SMBGCs
3.4. Mycoparasites Have a Large Number of P450s as Part of Their SMBGCs
3.5. Mycoparasite P450s Are Indeed Involved in the Synthesis of Secondary Metabolites
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Species Name | Information | Reference |
---|---|---|
Ampelomyces quisqualis HMLAC05119 | Ampelomyces is an ecologically and economically valuable hyperparasite that can parasitize the hypha, conidiophore, conidium, and perithecium of powdery mildew fungi. Ampelomyces species were among the first fungi used as plant parasitic fungi biocontrol agents. Ampelomyces species produce secondary metabolites such as quinones, phenolic compounds, and lytic enzymes inhibiting fungi or bacteria and have potential antibiotic use against human pathogens. | [5,6] |
Caulochytrium protostelioides ATCC 52028 single-cell | This species is a mycoparasite of Sordaria species and the first example of zoosporic true fungi having aerial sporangia, a unique trait within the Chytridiomycota. The hyphae secrete hydrophobin, a small cysteine-rich protein that develops aerial hyphae. This is the only fungus identified to produce hydrophobins outside the Dikarya (Ascomycota and Basidiomycota). | [7] |
Clonostachys rosea IK726 | This species is known for its biocontrol capabilities against a wide variety of plant pathogenic fungi, and various commercial products based on this fungus are available for use in biocontrol applications worldwide. This fungus effectively controls plant diseases caused by fungal and oomycete pathogens such as Alternaria spp., Bipolaris sorokiniana, Botrytis cinerea, Fusarium spp., Helminthosporium solani, Pythium tracheiphilum, and Zymoseptoria tritici. | [8] |
Dimargaris cristalligena RSA 468 single-cell | This fungus is a mycoparasite from the subphylum Kickxellomycotina (formerly of the Zygomycota). It is primarily a haustorial parasite of Mucorales and is known to produce various secondary metabolites. | [7,9] |
Escovopsis weberi CC031208-10 | This fungus is a parasite of Leucoagaricus spp., a garden fungus of leaf-cutting ants. It has adapted to mycoparasitism to the extent that it has lost plant-material-degrading enzymes. This fungus secretes various secondary metabolites that have antifungal and antibacterial activity. | [10,11] |
Naematelia encephela UCDFST 68-887.2 | This fugus is a parasite of Stereum sanguinolentum. This fungus has a worldwide presence. | [12] |
Piptocephalis cylindrospora RSA 2659 single-cell | P. cylindrospora is an obligatory parasite of Mucorales that infects the host with specialized haustoria. Haustoria are branched, walled cells that penetrate host cell walls to absorb energy. Strain RSA2659 is grown on the mucoraceous mould Cokeromyces recurvatus. This fungus is distinguished by the presence of relatively large, brownish sporophores with three-dimensional dichotomous branching. | [7] |
Rozella allomycis CSF55 | R. allomycis is an obligate parasite of the Blastocladiomycotan fungus Allomyces. | [13] |
Syncephalis pseudoplumigaleata Benny S71-1 single-cell | This fungus is an obligate parasite of zygomycetes. | [7] |
Thamnocephalis sphaerospora RSA 1356 single-cell | This fungus is believed to be a weak parasite of other fungi and can be cultivated on Cokeromyces (a Mucoralean). | [7] |
Tremella mesenterica Fries | This species is a parasite of the Peniophora fungus and has a deceptive appearance as if it is growing on wood. However, it grows on the crust of fungal mycelium. | [14] |
Trichoderma arundinaceum IBT 40837 | This species produces the biotechnologically valuable compound harzianum A. Harzianum A is used as a biocontrol agent against plant fungal pathogens and promotes plant defence. | [15] |
Trichoderma asperelloides T203 | This fungus was one of the earliest models for understanding Trichoderma mycoparasitism and rhizosphere interactions. It enhanced plant growth potential and tolerance to abiotic stressors and induced systemic resistance to fungal and bacterial disease-causing pathogens. As a result, T. asperelloides strain T203 was the subject of several laboratory, greenhouse, and large-scale field investigations. It was incorporated into commercial agricultural preparations to improve plant development and as a biocontrol agent for plant diseases. | [16] |
Trichoderma asperellum CBS 433.97 | T. asperellum is a potent antifungal agent because it can parasitize or hinder the growth and development of other fungi. As a result, this species is used as a biological control agent against a wide range of plant-pathogenic fungi and fungi-like protozoa, including Phytophthora megakarya and nematodes. T. asperellum has also exhibited antibacterial activity via the synthesis of trichotoxin peptaibols and produces various secondary metabolites. | [17,18] |
Trichoderma atroviride | This fungus is a biocontrol agent for many economically significant airborne and soilborne plant diseases. Its mycoparasitic activity is due to successful food competition, cell-wall-degrading enzyme synthesis, and antibiosis. This fungus also produces different types of secondary metabolites. | [19,20] |
Trichoderma citrinoviride TUCIM 6016 | T. citrinoviride has antifungal activities and nematode resistance, and its use as a biological control of plant fungal pathogens and nematodes has been elucidated. | [17,21,22] |
Trichoderma gamsii T6085 | One of the most promising agents for controlling Fusarium head blight (FHB) symptoms and mycotoxin accumulations, combined with mycoparasitic, antagonistic, and competitive activity against Fusarium graminearum, one of the primary causal agents of FHB. | [23] |
Trichoderma guizhouense NJAU 4742 | A mycoparasite of F. oxysporum, it has the potential to develop into a novel biofertilizer and biofungicide. | [17,24] |
Trichoderma hamatum GD12 | This fungus is unique because it can promote plant growth, activate biocontrol against pre- and post-emergence soil pathogens, and induce systemic resistance to foliar pathogens. | [25] |
Trichoderma harzianum CBS 226.95 | T. harzianum is extensively researched due to its plant protection properties. It produces secondary metabolites with antibiotic characteristics, including peptaibols, harzianic acid, trichoharzianin, and trichodermin. This fungus is used for foliar application, seed, and soil treatments to suppress diseases caused by pathogens such as Botrytis, Fusarium, and Penicillium sp. | [17,26] |
Trichoderma longibrachiatum ATCC 18648 | T. longibrachiatum’s parasitic and deadly effects on the cysts of the worm Heterodera avenae have led to its proposed use as a biocontrol agent. Because of its mycoparasitism, it has been investigated for reducing crop fungal diseases. | [17,27] |
Trichoderma virens Gv29-8 | This species produces many secondary metabolites with potential biotechnological values, including gliotoxin and gliovirin, which have potential biocontrol activity against Rhizoctonia solani. | [19] |
Species Name | P450 Family and Subfamily | Count |
---|---|---|
Clonostachys rosea IK726 | CYP51F | 2 |
CYP61A | 3 | |
Trichoderma virens Gv29-8 | CYP61A | 2 |
Thamnocephalis sphaerospora RSA 1356 single-cell | CYP51F | 2 |
Trichoderma longibrachiatum ATCC 18648 | CYP61A | 2 |
Trichoderma hamatum GD12 | CYP51F | 2 |
CYP61A | 2 | |
Trichoderma atroviride | CYP51F | 2 |
Trichoderma gamsii T6085 | CYP51F | 2 |
CYP61A | 2 | |
Trichoderma asperellum CBS 433.97 | CYP61A | 2 |
Trichoderma citrinoviride TUCIM 6016 | CYP61A | 2 |
Trichoderma asperelloides T203 | CYP61A | 2 |
Trichoderma pleuroti TPhu1 | CYP61A | 2 |
Trichoderma arundinaceum IBT 40837 | CYP51F | 2 |
CYP61A | 2 | |
Trichoderma guizhouense NJAU 4742 | CYP51F | 2 |
CYP61A | 3 | |
Trichoderma harzianum CBS 226.95 | CYP51F | 2 |
CYP61A | 3 |
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Syed, P.R.; Padayachee, T.; Gamede, P.; Nkosi, B.V.Z.; Nelson, D.R.; Karpoormath, R.; Syed, K. Comparative Genome-Wide Analysis Underscores the Rapid Expansion of Cytochrome P450s for Secondary Metabolism in the Mycoparasite Pezizomycetes. Microbiol. Res. 2024, 15, 1251-1268. https://doi.org/10.3390/microbiolres15030084
Syed PR, Padayachee T, Gamede P, Nkosi BVZ, Nelson DR, Karpoormath R, Syed K. Comparative Genome-Wide Analysis Underscores the Rapid Expansion of Cytochrome P450s for Secondary Metabolism in the Mycoparasite Pezizomycetes. Microbiology Research. 2024; 15(3):1251-1268. https://doi.org/10.3390/microbiolres15030084
Chicago/Turabian StyleSyed, Puleng Rosinah, Tiara Padayachee, Philasande Gamede, Bridget Valeria Zinhle Nkosi, David R. Nelson, Rajshekhar Karpoormath, and Khajamohiddin Syed. 2024. "Comparative Genome-Wide Analysis Underscores the Rapid Expansion of Cytochrome P450s for Secondary Metabolism in the Mycoparasite Pezizomycetes" Microbiology Research 15, no. 3: 1251-1268. https://doi.org/10.3390/microbiolres15030084