Evolutionary Histories of Type III Polyketide Synthases in Fungi
Open accessAbstract
Type III polyketide synthases (PKSs) produce secondary metabolites with diverse biological activities, including antimicrobials. While they have been extensively studied in plants and bacteria, only a handful of type III PKSs from fungi has been characterized in the last 15 years. The exploitation of fungal type III PKSs to produce novel bioactive compounds requires understanding the diversity of these enzymes, as well as of their biosynthetic pathways. Here, phylogenetic and reconciliation analyses of 522 type III PKSs from 1,193 fungal genomes revealed complex evolutionary histories with massive gene duplications and losses, explaining their discontinuous distribution in the fungal tree of life. In addition, horizontal gene transfer events from bacteria to fungi and, to a lower extent, between fungi, could be inferred. Ancestral gene duplication events have resulted in the divergence of eight phylogenetic clades. Especially, two clades show ancestral linkage and functional co-evolution between a type III PKS and a reducing PKS genes. Investigation of the occurrence of protein domains in fungal type III PKS predicted gene clusters highlighted the diversity of biosynthetic pathways, likely reflecting a large chemical landscape. Type III PKS genes are most often located next to genes encoding cytochrome P450s, MFS transporters and transcription factors, defining ancestral core gene clusters. This analysis also allowed predicting gene clusters for the characterized fungal type III PKSs and provides working hypotheses for the elucidation of the full biosynthetic pathways. Altogether, our analyses provide the fundamental knowledge to motivate further characterization and exploitation of fungal type III PKS biosynthetic pathways.
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Four fundamental regions in the genome of L. plantarum 55A were identified to produce bacteriocins and secondary metabolites including cyclic-lactone autoinducer, RiPP-like molecules, T3PKS, and terpenes.
“Four fundamental regions in the genome of L. plantarum 55A were identified to produce bacteriocins and secondary metabolites including cyclic-lactone autoinducer”
From Genomic Characterization of Lactiplantibacillus plantarum Strains: Potential Probiotics from Ethiopian Traditional Fermented Cottage Cheese (2024) · cites this paper as [49]
The Materials and Methods section describes a survey of fungal genomes for type III PKS gene clusters, not four regions in L. plantarum 55A. Searches for that strain and for cyclic-lactone autoinducer found no passage addressing the claimed regions or products; page numbers were unavailable in our copy. (LLM, conf=0.78)
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Cloning and characterization of a type III polyketide synthase from Aspergillus niger
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“In other fungi, newly identified SMs are predicted to be synthesized by a type III PKS (Rusman et al., 2018), suggesting that these fungi also contain type III PKS genes.”
BackgroundMori, T., Yang, D., Matsui, T., Hashimoto, M., Morita, H., Fujii, I., & Abe, I. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.626416 · Cited by 21 · cited 3× · see citing works
“Comparison of the sequence logos (Supplementary Material S9) between each fungal clade, plant and bacterial clades (Figures 2, 3A) highlights the highly conserved Cys-His-Asn catalytic triad, as well as the Phe residue that was reported to control product specificity (Rubin-Pitel et al., 2008; Mori et al., 2015).”
BackgroundType III polyketide synthases in lichen mycobionts
Muggia, L., & Martin, G. (2010) · Fungal Biology · doi:10.1016/j.funbio.2010.03.001 · Cited by 20 · see citing works
Identification of a type III polyketide synthase involved in the biosynthesis of spirolaxine
Sun, L., Wang, S., Zhang, S., Yu, D., Qin, Y., Huang, H., Wang, W., & Zhan, J. (2016) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-016-7444-5 · Cited by 18 · see citing works
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“oryzae, CsyB appears to be located next to an MFS transporter gene only, suggesting that the csypyrone compounds reported for this PKS might be the final compounds (Seshime et al., 2010a; Hashimoto et al., 2013).”
BackgroundManoharan, G., Sairam, T., Rajesh, T., Ramakrishnan, D., Tiwari, M. K., Lee, J.-K., & Jeya, M. (2019) · Enzyme and Microbial Technology · doi:10.1016/j.enzmictec.2019.109396 · Cited by 14 · see citing works
Diversity and evolution of polyketide biosynthesis gene clusters in the Ceratocystidaceae
Sayari, M., Steenkamp, E. T., van der Nest, M. A., & Wingfield, B. D. (2018) · Fungal Biology · doi:10.1016/j.funbio.2018.04.011 · Cited by 12 · cited 2× · see citing works
“In addition to these characterized enzymes, several type III PKS genes have been reported in fungal genomes (Muggia and Grube, 2010; Lackner et al., 2012; Bertrand et al., 2018; Sayari et al., 2018).”
BackgroundMolecular characterization of two alkylresorcylic acid synthases from Sordariomycetes fungi
Ramakrishnan, D., Tiwari, M. K., Manoharan, G., Sairam, T., Rajesh, T., Lee, J.-K., & Jeya, M. (2018) · Enzyme and Microbial Technology · doi:10.1016/j.enzmictec.2018.04.006 · Cited by 11 · cited 9× · see citing works
“The CtPKS gene is located next to P450 and thiolase genes, as well as a sugar transporter and F-box-like genes, which function in fungal SM remains to be demonstrated (Figure 7).”
BackgroundInfluentialYan, H., Sun, L., Huang, J., Qiu, Y., Xu, F., Yan, R., Zhu, D., Wang, W., & Zhan, J. (2018) · The Journal of Microbiology · doi:10.1007/s12275-018-8278-x · Cited by 11 · see citing works
Lv, Y., Xiao, J., & Pan, L. (2014) · Biotechnology Letters · doi:10.1007/s10529-014-1609-z · Cited by 10 · cited 2× · see citing works
“niger type III PKS yields four products only, of which the major one is protocatechuic acid (Lv et al., 2014).”
BackgroundKirimura, K., Watanabe, S., & Kobayashi, K. (2016) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.04.023 · Cited by 9 · see citing works
The Impact of Natural Selection on the Evolution and Function of Placentally Expressed Galectins
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“It was shown that orthologous genes can experience accelerated evolution in certain organisms only (Ely et al., 2019).”
BackgroundCorrection: The Evolution of Fungal Metabolic Pathways
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Genome-Based Cluster Deletion Reveals an Endocrocin Biosynthetic Pathway in Aspergillus fumigatus
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Flagged first, then by citations
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Fungal secondary metabolites in food and pharmaceuticals in the era of multi-omics
Shankar, A., & Sharma, K. K. (2022) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-022-11945-8 · Cited by 71 · see citing works
“Similar kind of genes has also been reported in the basidiomycete group of fungi (Navarro-Muñoz and Collemare 2020).”
BackgroundProduction, Biosynthesis, and Commercial Applications of Fatty Acids From Oleaginous Fungi
Zhang, X., Li, B. J., Huang, B.-C., Wang, F.-B., Zhang, Y., Zhao, S.-G., Li, M., Wang, H., Yu, X., Liu, X., et al. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.873657 · Cited by 85 · see citing works
“Type III polyketide synthases (PKSs) produce secondary metabolites with diverse biological activities, including antimicrobials (120, 121).”
BackgroundZhgun, A. A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241311184 · Cited by 65 · see citing works
Cox, R. J. (2022) · Natural Product Reports · doi:10.1039/d2np00007e · Cited by 61 · see citing works
Next-generation antifungal drugs: Mechanisms, efficacy, and clinical prospects
Lu, X., Zhou, J., Ming, Y., Wang, Y., He, R., Li, Y., Feng, L., Zeng, B., Du, Y., & Wang, C. (2025) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2025.06.013 · Cited by 48 · see citing works
“Strategies targeting enzymes involved in fungal toxin synthesis (such as polyketide synthases) 255 , cell cycle-dependent kinases (CDKs) 256 , or spindle assembly checkpoint proteins 256 also offer promising avenues for inhibiting fungal proliferation.”
Biosynthesis of fungal polyketides by collaborating and trans -acting enzymes
Skellam, E. (2021) · Natural Product Reports · doi:10.1039/d1np00056j · Cited by 36 · see citing works
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Gilchrist, C. L. M., & Chooi, Y. (2021) · Fungal Biology and Biotechnology · doi:10.1186/s40694-021-00120-9 · Cited by 31 · see citing works
“They are observed mostly in bacteria, though several have been characterised in fungi and have been shown to produce α-pyrones, resorcylic acids and resorcinols [55, 56].”
BackgroundTriumphs and Challenges of Natural Product Discovery in the Postgenomic Era
Cano‐Prieto, C., Undabarrena, A., de Carvalho, A. C., Keasling, J. D., & Cruz‐Morales, P. (2024) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-032620-104731 · Cited by 34 · see citing works
Marks, B. B., Nogueira, M. A., & Hungría, M. (2025) · Agronomy · doi:10.3390/agronomy15061350 · Cited by 30 · see citing works
“Type III: Small aromatic compounds, mostly synthesized by fungal species with especially antimicrobial action [39].”
Botryosphaeriaceae gene machinery: Correlation between diversity and virulence
Belair, M., Restrepo-Leal, J. D., Praz, C. R., Fontaine, F., Rémond, C., Fernández, O., & Besaury, L. (2023) · Fungal Biology · doi:10.1016/j.funbio.2023.03.004 · Cited by 27 · see citing works
Kersey, P. J., Collemare, J., Cockel, C. P., Das, D., Dulloo, E. M., Kelly, L. J., Lettice, E. P., Malécot, V., Maxted, N., Metheringham, C. L., et al. (2020) · Plants People Planet · doi:10.1002/ppp3.10136 · Cited by 28 · see citing works
Self-citationGuzman, J. D., & Vilcinskas, A. (2021) · Antonie van Leeuwenhoek · doi:10.1007/s10482-021-01676-7 · Cited by 25 · see citing works
“The presence of methyltransferases and flavindependent monoxygenases is a common feature of certain type-3 PKS clusters particularly those found in fungi (Navarro-Muñoz and Collemare 2020) and in some myxobacteria (Hug et al.”
BackgroundExpansion and Conservation of Biosynthetic Gene Clusters in Pathogenic Pyrenophora spp.
Moolhuijzen, P., Muria‐Gonzalez, M. J., Syme, R. A., Rawlinson, C., See, P. T., Moffat, C. S., & Ellwood, S. R. (2020) · Toxins · doi:10.3390/toxins12040242 · Cited by 24 · see citing works
Mushroom oils: A review of their production, composition, and potential applications
Tan, R., Ilham, Z., Wan-Mohtar, W. A. A. Q. I., Halim-Lim, S. A., Usuldin, S. R. A., Ahmad, R., & Adlim, M. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e31594 · Cited by 22 · see citing works
Larsen, J. S., Pearson, L. A., & Neilan, B. A. (2021) · Genome Biology and Evolution · doi:10.1093/gbe/evab056 · Cited by 21 · see citing works
Biosynthesis of the Nuclear Factor of Activated T Cells Inhibitor NFAT-133 in Streptomyces pactum
Zhou, W., Posri, P., Abugrain, M. E., Weisberg, A. J., Chang, J. H., & Mahmud, T. (2020) · ACS Chemical Biology · doi:10.1021/acschembio.0c00775 · Cited by 18 · see citing works
Aiswarya, G., Vijayanathan, M., Sreekumar, S., Jasim, B., Menon, T. G., Radhakrishnan, E. K., & Soniya, E. V. (2021) · Current Molecular Pharmacology · doi:10.2174/1874467214666210319145816 · Cited by 18 · see citing works
Gizachew, S., & Engidawork, E. (2024) · Genes · doi:10.3390/genes15111389 · Cited by 15 · see citing works
“…molecules (exhibit antibacterial activity) [48], T3PKS (produce secondary metabolites with diverse biological activities, including antimicrobials) [49], and terpenes (have antimicrobial, antiparasitic, antiallergenic, antispasmodic, antihyperglycemic, anti-inflammatory, and immunomodulatory…”
Microbial polyketides and their roles in insect virulence: from genomics to biological functions
Toopaang, W., Bunnak, W., Srisuksam, C., Wattananukit, W., Tanticharoen, M., Yang, Y., & Amnuaykanjanasin, A. (2022) · Natural Product Reports · doi:10.1039/d1np00058f · Cited by 16 · see citing works
The Influence of Symbiosis on the Proteome of the Exaiptasia Endosymbiont Breviolum minutum
Mashini, A. G., Oakley, C. A., Beepat, S. S., Peng, L., Grossman, A. R., Weis, V. M., & Davy, S. K. (2023) · Microorganisms · doi:10.3390/microorganisms11020292 · Cited by 15 · see citing works
Sedaghatjoo, S., Mishra, B., Forster, M. K., Becker, Y., Keilwagen, J., Killermann, B., Thines, M., Karlovský, P., & Maier, W. (2022) · IMA Fungus · doi:10.1186/s43008-022-00098-y · Cited by 14 · see citing works
“2015; Navarro-Muñoz and Collemare 2020).”
Advances in Fungal Promoter Engineering for Enhancing Secondary Metabolite Biosynthesis
Pu, N., & Zhang, H. (2025) · Biotechnology Journal · doi:10.1002/biot.70075 · Cited by 12 · see citing works
Baeza, M., Zúñiga, S., Peragallo, V., Barahona, S., Alcaı́no, J., & Cifuentes, V. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.623171 · Cited by 12 · see citing works
Emerging diversity in polyketide synthase
Lin, Z., & Qu, X. (2022) · Tetrahedron Letters · doi:10.1016/j.tetlet.2022.154183 · Cited by 11 · see citing works
A genomic approach to analyze the cold adaptation of yeasts isolated from Italian Alps
Turchetti, B., Buzzini, P., & Baeza, M. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1026102 · Cited by 10 · see citing works
“, 2021), and produces a wide array of compounds such as chalcones, pyrones, acridones, phloroglucinols, and stilbenes, with several physiological roles such as pigmentation, salinity and dehydration resistance, stress adaptation, and cell wall remodeling (Yu et al., 2012; Parvez et al., 2018; Navarro-Muñoz and Collema…”
BackgroundEvolutionary relationships of adenylation domains in fungi
Noriler, S. A., Navarro-Muñoz, J. C., Glienke, C., & Collemare, J. (2022) · Genomics · doi:10.1016/j.ygeno.2022.110525 · Cited by 10 · see citing works
Self-citationMycotools: An Automated and Scalable Platform for Comparative GenomicsPreprint
Konkel, Z. M., & Slot, J. C. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.08.556886 · Cited by 9 · see citing works
CLOCI: unveiling cryptic fungal gene clusters with generalized detection
Konkel, Z. M., Kubatko, L. S., & Slot, J. C. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae625 · Cited by 8 · see citing works
“PDS is a proxy for the extent of horizontal cluster transfer and / or coordinated cluster gene loss, which are elevated in some categories of gene clusters ( 25 , 42 , 55 , 58 , 76 , 77 ).”
BackgroundUnveiling potential PET degrading eukaryotes through in silico bioprospecting of PETases
Méndez-Zamora, A., Diaz‐Vidal, T., Robles-Machuca, M., Pereira‐Santana, A., & Casas‐Godoy, L. (2024) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2024.174978 · Cited by 8 · see citing works
Zhang, L., Liu, Y., Chen, K., Yue, Q., Wang, C., Xie, L., Molnár, I., & Xu, Y. (2025) · Metabolic Engineering · doi:10.1016/j.ymben.2025.08.001 · Cited by 8 · see citing works
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“Library screening and product biosynthesis were done in yeast extract M9 media (YM9, containing 1 × M9 salts, 10 g L − 1 yeast extract, 3% glycerol, and 42 g L − 1 MOPS [3-(N-morpholino) propanesul-fonic acid]).”
MethodMartinelli, L., Rédou, V., Cochereau, B., Delage, L., Hymery, N., Poirier, E., Meur, C. L., Floch, G. L., Cladière, L., Mehiri, M., et al. (2020) · Marine Drugs · doi:10.3390/md18120637 · Cited by 8 · see citing works
“Fungal proteins sequences us d for this tree were identified by the study of Navarro-Munoz and Coll mare [43] and NCBI public database (Supplementary Material S1).”
BackgroundMethodResultInfluentialUnravelling the Functional Diversity of Type III Polyketide Synthases in Fungi
Sokolova, N., Denisov, S. S., Hackl, T., & Haslinger, K. (2025) · Angewandte Chemie International Edition · doi:10.1002/anie.202514786 · Cited by 9 · see citing works
Christinaki, A. C., Myridakis, A., & Kouvelis, V. N. (2024) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkae006 · Cited by 7 · see citing works
“This result aligns with a previous study that showed a scattered distribution of T3PKS in fungi due to HGT events (Navarro-Muñoz and Collemare 2020).”
ResultGenome-Based Analysis of Verticillium Polyketide Synthase Gene Clusters
Sayari, M., Dolatabadian, A., El-Shetehy, M., Rehal, P. K., & Daayf, F. (2022) · Biology · doi:10.3390/biology11091252 · Cited by 7 · see citing works
Arishi, A. A., Holland, D. C., Bracegirdle, J., Nedelkos, P. A., Garratt, L. W., Mantjani, L., Moggach, S. A., Lacey, E., Vuong, D., Kalaitzis, J. A., et al. (2026) · Journal of Natural Products · doi:10.1021/acs.jnatprod.5c01541 · Cited by 5 · see citing works
Fungal metabolites as novel plant pathogen antagonists
Singh, J., Mishra, S., & Singh, V. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-23950-2.00012-6 · Cited by 3 · see citing works
Löhr, N. A., Platz, L., Hoffmeister, D., & Müller, M. (2024) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2024.102510 · Cited by 2 · see citing works
Ruiz, V. C., Aleu, J., Garrido, C., & Collado, I. G. (2024) · Agronomy · doi:10.3390/agronomy14112747 · Cited by 2 · see citing works
Mashini, A. G. (2022) · doi:10.26686/wgtn.18739247 · Cited by 2 · see citing works
CLOCI: Unveiling cryptic gene clusters with generalized detectionPreprint
Konkel, Z. M., Kubatko, L. S., & Slot, J. C. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.06.20.545441 · Cited by 2 · see citing works
“However, PDS for the nitrate assimilation cluster is not as high as specialized metabolite clusters with smaller transfer distances (72) because nitrate assimilation is such a broadly distributed accessory function (Figure 2a).”
BackgroundSamaddar, A., Mendonsa, J. M., Siddaiah, N., Rudramurthy, S. M., Pamidimukkala, U., & Kindo, A. J. (2025) · Medical Mycology · doi:10.1093/mmy/myaf108 · Cited by 1 · see citing works
Hidden handshakes and hostilities: the two sides of fungal metabolites in plant-fungal interactions
Gunda, T. J., Jasrotia, N., Eshawu, A. B., Awasthi, N. S., Dhar, H., Ghalsasi, V. V., Thakur, A., & Thakur, K. (2026) · Journal of Plant Biochemistry and Biotechnology · doi:10.1007/s13562-026-01055-1 · Cited by 1 · see citing works
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Shlyk, N. P., Yurchenko, E. A., Leshchenko, E. V., Chingizova, E. A., Chingizov, A. R., Chausova, V. E., Kirichuk, N. N., Khudyakova, Y. V., Викторович, П. М., Antonov, A. S., et al. (2025) · The Journal of Antibiotics · doi:10.1038/s41429-025-00811-0 · Cited by 1 · see citing works
“Up to 2020 only eleven type III PKSs have been characterized in the fungal kingdom, ten from Ascomycota and one from Basidiomycota [50].”
Vijayanathan, M., Abhinav, K. V., Bandyopadhyay, D., Mahendran, K. R., Sharaf, A., Pillai, M. R., & Soniya, E. V. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.08.26.505429
Functional analysis of a putative type III polyketide synthase from deep-sea sediment metagenome
Kulasekaran, N. T., Subramanian, S. H. S., Thilakam, M. L., Dharani, G., Lee, J. K., & Jeya, M. (2024) · Journal of Bioscience and Bioengineering · doi:10.1016/j.jbiosc.2023.12.019
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Unravelling the Functional Diversity of Type III Polyketide Synthases in Fungi
Sokolova, N., Denisov, S. S., Hackl, T., & Haslinger, K. (2025) · Angewandte Chemie · doi:10.1002/ange.202514786
Xiang, L., Zhang, X., Lei, Y., Wu, J., Yan, G., Chen, W., Li, S., Wang, W., Jin, J.-M., Liang, C., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26170557
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“Notably, NAPAA, NI siderophore, and T3PKS BGCs were found exclusively in Cladobotryum species, including C. rhodochroum , reinforcing the species’ unique secondary metabolite potential [80].”
Begum, S., Wu, X., Shah, M. T., Ibrahim, N., Li, Y., Kanwal, A., Chen, S., Jiang, L., Liang, Y., & Liu, X. (2026) · Mycological Progress · doi:10.1007/s11557-026-02139-x
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- Authors
- Navarro-Muñoz, J. C., & Collemare, J.
- Affiliations
- Westerdijk Fungal Biodiversity Institute (NL)
- Corresponding author
- Collemare, Jérôme
- Venue
- Frontiers in Microbiology
- Publisher
- Frontiers Media SA
- Published
- 2020-01-21
- Volume
- 10
- Pages
- 3018-3018
- ISSN
- 1664-302X (ISSN-L)
- PMC
- PMC6985275
- OpenAlex
- W3002174916
- Cited by
- 59
- References
- 80
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 13 · 2023: 7 · 2022: 12 · 2021: 8 · 2020: 5
- FWCI
- 4.79
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Frontiers in Microbiology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (submittedVersion)
- Topics
- Health Sciences › Medicine › Pharmacology › Microbial Natural Products and Biosynthesis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Microbial Metabolism and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- type III polyketide synthase, fungal secondary metabolites, fungal evolution, gene duplication, gene loss, horizontal gene transfer, phylogenetic analysis, coevolution, gene clusters, cytochrome P450, major facilitator superfamily, transcription factors, antimicrobial agents, fungal genome
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