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. 2025 May 15;8:100402. doi: 10.1016/j.crmicr.2025.100402

Secretion of antifungal metabolites contributes to the antagonistic activity of Talaromyces oaxaquensis

Aneliz de Ita Zárate-Ortiz a, José Luis Villarruel-Ordaz a, Ana Claudia Sánchez-Espinosa a, Rommel A Carballo-Castañeda b, Aldo Moreno-Ulloa b, Luis David Maldonado-Bonilla c,⁎
PMCID: PMC12149641  PMID: 40496374

Highlights

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    Talaromyces oaxaquensis produces diffusible molecules that repress the in vitro growth of Fusarium oxysporum f. sp. cubense M5 and its own growth.

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    The penicillide Vermixocin A and the polyester 15G256α are known antimicrobial compounds produced and secreted by Talaromyces oaxaquensis.

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    An ethyl acetate extract of supernatants of Talaromyces oaxaquensis cultures cause hyphal swellings in Fusarium oxysporum f. sp. cubense M5 possibly by inhibiting the chitin synthesis.

Keywords: Antifungal metabolites, Chitin synthase, Endophyte, Metabolic profiling

Abstract

Controlling fusarium wilt is critical to guarantee the supply of bananas. In this study, three strains of the endophyte Talaromyces oaxaquensis obtained from pseudostems of Musa sp. AAB cv. Manzano were found to inhibit the in vitro growth of the banana pathogen Fusarium oxysporum f. sp. cubense M5. Constitutive production and secretion of antifungal factors by T. oaxaquensis is a feature of its inhibition effect, as there was no physical contact between the two fungi. An ethyl acetate extract prepared from supernatants of liquid cultures of the three T. oaxaquensis strains displayed inhibitory activity and hyphal swellings. Both the supernatants and mycelia were subjected to metabolic profiling. Penicillides and macrolide polyesters were detected in the supernatants. A molecular docking approach revealed the binding of the polyester 15G256α to chitin synthase 1 of Fusarium oxysporum f. sp. cubense. This is the first study to report the potential of the endophyte Talaromyces from Musa sp. to generate biological control products to protect plants against phytopathogens.

Graphical abstract

Image, graphical abstract

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1. Introduction

The production of bananas and plantains is an important economic activity in developing countries with tropical climates, and the export of the fruits represent a significant income for farmers in Latin America, the Caribbean, Asia, and Africa. Worldwide banana exports have been declining since 2021 and this trend is expected to persist during the next years (FAO, 2024). The fusarium wilt also known as Panama disease, is one of the key factors in the decline of banana production. Fusarium oxysporum f. sp. cubense (Foc) is the causal agent of fusarium wilt (Ploetz 2015). Bananas of the Cavendish group (Musa sp. AAA) have been extensively cultivated, as they are resistant to Foc Race 1, but the production of such bananas has been severely affected by the emergence of F. odoratissimum, a pathogen of the Cavendish group that also affects banana plants from other groups (Ordonez et al., 2015). F. odoratissimum is currently distributed in Australia, Southern Asia, the Middle East, Mozambique, Colombia, and Peru (Bragard et al., 2022).

Exploring endophytic microbes isolated from banana plants might be helpful in identifying natural antagonists of Foc, and, due to these microbes’ adaptation to banana plants and the tropical climate, they might be reliable candidates for implementing novel strategies of biological control. Talaromyces is a versatile genus of ascomycetes that can be adapted to several habitats, including plants (Yilmaz et al. 2014). The diversity of secondary metabolites of Talaromyces spp. is remarkable. Many Talaromyces metabolites display antibacterial or antifungal activity (Lan and Wu, 2020). Penicillides, a novel class of fungal metabolites, are frequently found in endophyte species of Talaromyces and Penicillium (Salvatore et al. 2024). Polyesters, either linear or macrocyclic, are metabolites heterogeneously distributed in fungi, but they are considered one of the main groups of secondary metabolites of Talaromyces (Zhai et al. 2016). Polyesters and a subset of polyesters known as talapolyesters have cytotoxic activity, which reveals their potential biological role in the selection and persistence of Talaromyces spp. in their natural habitat, which could eventually have biotechnological impact (Lan and Wu, 2020).

Three strains of the novel species Talaromyces oaxaquensis have been recovered from pseudostems of Musa sp. AAB cv. Manzano (Zárate Ortíz et al. 2024). An initial screening revealed that these strains can inhibit the in vitro growth of the causal agent of fusarium wilt, Fusarium oxysporum f. sp. cubense M5 (FocM5). Here, we demonstrate that T. oaxaquensis can repress the growth of FocM5 by secreting diffusible molecules and also cause hyphal swellings possibly by interfering with might cell wall biosynthesis.

2. Materials and methods

2.1. In vitro confrontation assays

Direct confrontations were performed by co-cultivating 0.5 cm2-mycelium blocks of the T. oaxaquensis strains N10, N11, and N12 (Zárate Ortiz et al. 2024) together with FocM5 (Maldonado-Bonilla et al. 2019) on opposite sides of PDA plates. FocM5, like strains of Fusarium oxysporum f. sp. cubense race1, belongs to the lineage 2 of Fusarium oxysporum species complex, it is virulent towards Musa sp. AAB cv. Manzano, although it cannot be assigned as race 1 since there is no evidence of infection of Musa sp. AAA Gros Michel. The plates were incubated for 14 days at 25 °C in darkness. Three replicates were included, plus controls of the sole inoculation of the strains of T. oaxaquensis and FocM5. The growth of FocM5 was estimated in each condition by measuring the mycelial growth from the site of inoculation to the furthest point of growth. The percentage of inhibition ( %I) by co-inoculation of each isolate was later calculated with the equation %I = C−TCx100, where C represents the mycelial growth of M5 alone, and T the mycelial growth of FocM5 in the presence of N10, N11, and N12. This experiment was repeated three times. Indirect confrontation assays were performed by preparing PDA plates fully covered with sterile cellophane discs. A 0.5 cm2-block of mycelium from the strains N10, N11, and N12 were placed at the center of the plate, and PDA plates covered with cellophane discs without inoculation were used as the negative control. All these plates were incubated at 25 °C in darkness, and the strains grew by diffusion of the nutrients through the pores of the cellophane. After 7 days of incubation, the cellophane discs were removed along with the mycelia, leaving the plate free of fungus. FocM5 was inoculated at the center of the plate and incubated at 25 °C. After one-week, mycelial growth was measured and the %I was calculated as described above. To validate the potential self-inhibition, indirect confrontations between T. oaxaquensis strains were also conducted. In this case, N10, N11, and N12 were inoculated by triplicates into PDA plates and incubated under the above-mentioned conditions of indirect confrontation assay. Three uninoculated PDA plates were included as the control. The cellophane was removed after 7 days of incubation. Then, 0.5 cm2-blocks of N10 were inoculated in the center of the 12 Petri plates (three uninoculated, three pre-inoculated with N10, three pre-inoculated with N11, and three pre-inoculated with N12). Plates were incubated at 25 °C for 7 days, after which the radial growth was measured. This experiment was performed three times. A similar set of experiments was performed by inoculating N11 and N12 after the removal of the cellophane disc to obtain the rest of the combinations. For each isolate, Tukey’s test was used to assess the difference between pairwise comparisons (control vs. pre-inoculation of N10, N11, or N12).

2.2. Liquid cultures

Previous assays have revealed that a potato broth supplemented with 1 % sucrose (PS) allows the growth of T. oaxaquensis and its production of antifungal factors (data not shown). PS was prepared by boiling 200 g of sliced potato tuber in 1 L of distilled water for 30 min. The sucrose was added after the boiling liquid was filtered with a cheesecloth. Once the medium was prepared, it was autoclaved for 15 min at 121 °C. A 1-cm2 PDA block with mycelium of each isolate was sown into 50 mL Falcon tubes with 15 mL of PS and incubated at 25 °C and 100 rpm for 7 days in darkness. The spherical pellet that grew during this period was broken up by shaking thoroughly. An aliquot of 1 mL of starter culture was inoculated in flasks containing 100 mL of fresh PS. The flasks were incubated at 25 °C and 100 rpm for 14 days.

2.3. Extraction from liquid cultures and inhibitory test

After the incubation period, the liquid cultures described above were filtered with filter paper to separate the mycelia. Out of the initial 100 mL of inoculated PS, roughly 80 % of the liquid was recovered after filtration. One volume of ethyl acetate was added to the filtered media and mixed by shaking. The upper organic phase was collected and dried up. The dried extract was weighted and resuspended with DMSO to a final concentration of 10 mg/mL. To confirm that metabolites with antifungal activity were present in the extract, a PDA block with mycelium of the M5 strain was inoculated by triplicates at the center of a Petri plate with solid minimal M9 medium with 1 % glucose as carbon source (M9G) and supplemented with 50 μg/mL of the extract. Similar plates but supplemented with DMSO were used as negative controls. After inoculation, the plates were incubated in darkness at 25 °C. The diameter of the grown mycelium was measured after 7 days of incubation, and the %I was calculated as described above. This experiment was repeated three times. The statistically significance between the treatments was assessed with one way ANOVA with Tukey's Honestly Significant Difference Test. Furthermore, autoclaved glass slides were covered with 50 % PDA supplemented with 50 μg/mL of the ethyl acetate extracts of the three T. oaxaquensis strains. Glass slides with 50 % PDA plus the corresponding volume of DMSO were used as negative controls. One hundred total conidia of FocM5 were inoculated in the center of the glass slides. The glass slide was placed into a Petri dish and incubated 24 h at 25 °C in darkness. Slides were observed by using a Primo Star microscope equipped with a Canon PowerShot G16 digital camera.

2.4. Untargeted liquid chromatography-tandem mass spectrometry

Once we confirmed that the ethyl acetate extracts contain inhibitors of the fungal growth, extraction was repeated for metabolome mining. The extracts were processed according to the procedure of Contreras Angulo et al. (2022) with slight modifications. Extracts from 14-day-old liquid cultures and PS medium were resuspended in 1 mL of H2O:Acetonitrile (ACN) 80:20 with 0.1 % formic acid (FA). Samples were vortexed for 1 min and sonicated at 40 kHz for 30 min at 4 °C using a Sonicator model M1800H-E (Branson). The concentration was then adjusted to 300 ng/mL. Metabolites were recovered by centrifugation at 14,000 rpm for 10 min at 4 °C. After centrifugation, the particle-free supernatants were collected, and 20 μL were transferred to chromatography vials, and 2 μL were injected into an Agilent 1260 Infinity LC (Agilent Technologies) instrument to separate metabolites by reverse phase by using a ProtID-Chip-43 II column (C18, 43 mm, 300 Å, 5 µm particle size, equipped with a 40-nL enrichment column). The mobile phase, solution B, running conditions, and data acquisition were the same as those reported before (Contreras Angulo et al. 2022). The eluate was delivered to a 6530 Accurate-Mass Q-TOF mass spectrometer (Agilent Technologies) via an HPLC—Chip Cube MS interface. In parallel, mycelia of N10, N11, and N12 grown on PDA for 2 weeks were lyophilized to determine the metabolic profiles of the biomass. A fresh PDA sample without inoculation was included as a negative control. For this purpose, 500 μL of ethyl acetate was added to 5 mg of lyophilized mycelium of each isolate and resuspended by vortex for 1 min and sonicated for 30 min as described above. Resuspended samples were later centrifugated at 14,000 rpm for 10 min at 4 °C, and 400 μL were transferred to 1.5-mL tubes to be vacuum-dried by using a SpeedVac concentrator (Thermo Fisher Scientific) at room temperature for 2 h. Dried samples were resuspended in 50 μL of H2O:ACN 80:20 with 0.1 % FA. These resuspended samples were mixed by vortex and sonication, and then centrifugated as described above. Then, 40 μL were recovered to be injected using the same conditions as those described above to analyze extracts from liquid cultures.

2.5. Data processing

The raw data (.d files) were converted to the free format . mzXML by using the ProteoWizard MsConvert program version 3.0.23089 (Chambers et al. 2012). Online automatic annotation was performed online by transferring the .mzXML data to the Global Natural Products Social Molecular Networking site (GNPS, https://gnps.ucsd.edu) (Wang et al. 2016) and by using the application WinSCP, and the molecular networks for every isolate and negative controls were created by METABOLOMICS-SNETS-V2 with the following parameters: 0.02 Da precursor ion mass tolerance; 0.02 Da fragment ion mass tolerance, and a cosine score of 0.6. The prediction in silico tools DEREPLICATOR+ (Mohimani et al. 2018) and MolDiscovery (Cao et al. 2021) were used to enrich the annotation of metabolites. List of molecules above 600 Da was generated by combining the results of GNPS and MolDiscovery, and the list of predicted metabolites from 400 to 600 Da was generated with DEREPLICATOR+. The Network Annotation Propagation (NAP) tool in the GNPS platform was used to visualize the predominant chemical classes through the MetFrag algorithm a cosine score of 0.6 (da Silva et al. 2018; Kang et al. 2018). MS2LDA was used to annotate substructures based on the neutral losses of spectra (van Der Hooft et al. 2016). The mass error of each compound was calculated according to the equation MassError(ppm)=Experimentalm/z−Theoreticalm/zTheoreticalm/z×106). Metabolites with a mass error above 10 were discarded. Chemical classes were assigned with Classyfire (Djoumbou-Feunang et al. 2016). Molecular network of chemical classes derived from NAO and MS2LDA was built with MolNetEnhancer (Ernst et al. 2019) and visualized and edited in Cytoscape version 3.10.0. (Shannon et al. 2003). The parameters and raw data of LC-MS2 analysis are available in the data availability statement included as supplementary material.

2.6. Molecular docking

The polypeptide sequences of the chitin synthase (Chs) family of Colletotrichum graminicola (Werner et al. 2007) and Chs2 from Candida albicans (Ren et al. 2022) were used as queries to retrieve the homolog sequences of Foc160527 (Asai et al. 2019) available in Ensembl Fungi (https://fungi.ensembl.org/index.html). The complete set of Chss were aligned to carry out a maximum likelihood phylogeny with 1000 bootstrap replicates. The phylogeny enabled the identification of the homolog FocChs1 from the class I of Chss, whose tertiary structure predicted by AlphaFold (Jumper et al. 2021) is available at https://www.uniprot.org/, under entry number A0A559L2L1. The structure of 15G256α was retrieved from PubChem (https://pubchem.ncbi.nlm.nih.gov/) as an .sdf file and used as the ligand to test its binding to FocChs1 by using the cavity-focused method CB-dock (Liu et al. 2020). The protein-ligand models with the lowest Vina score were visualized and edited in UCSF Chimera 1.13.1 (Pettersen et al., 2004), and the 2D plot of this model was visualized using the ezLigPlot tool (Tao et al. 2018).

3. Result

3.1. Talaromyces oaxaquensis strains inhibit the mycelial growth of FocM5

Since the strains N10, N11, and N12 were recovered from pseudostems of Musa sp. AAB, we performed co-inoculations in PDA to determine whether they could antagonize the in vitro growth of the FocM5 strain, which has been previously confirmed as a causal agent of fusarium wilt (Maldonado Bonilla et al. 2019). The T. oaxaquensis strains grew slower than FocM5, but they were able to impede the progression of the mycelial growth of FocM5 (Fig. 1a, upper panel). The M5 aerial whitish hyphae decreased as the growth approached any of the T. oaxaquensis strains. As the inhibition of M5 growth does not require physical contact between the fungi, indirect confrontation assays were performed to confirm that the strains secrete molecules to repress the mycelial growth of M5. The indirect confrontation assays revealed that previous growth of T. oaxquensis in PDA compromised the subsequent growth of M5 (Fig. 1a, lower panel). In addition to the reduction of radial growth, the emergence of aerial hyphae was barely evident in these treatment groups. The estimation of %I revealed a similar effect of repression driven by the three strains, both in direct and indirect confrontations (Fig. 1b), suggesting that T. oaxaquensis deposits antifungal factors when growing in PDA.

Fig. 1.

Fig 1

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The strains N10, N11, and N12 of T. oaxaquensis repress the growth of M5. a) Direct confrontations (upper panel) and indirect confrontation (lower panel); the combination of each assay is indicated at the top. b) Estimation of percentage of inhibition of M5 mycelial growth in direct and indirect confrontations. See text for details.

3.2. Talaromyces oaxaquensis secretes metabolites detrimental to its own growth

Indirect confrontations among the three T. oaxaquensis strains were performed since the findings mentioned above could imply an intrinsic response towards its own potential antifungal factors. All possible combinations plus controls were examined and the mycelial growth was measured. The growth of the N10 strain was not inhibited by its own pre-inoculation or pre-inoculation of N11 and N12 (Fig. 2). However, N11 and N12 did show inhibition in response to the all three pre-inoculations (Fig. 2).

Fig. 2.

Fig 2

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Sensitivity of T. oaxaquensis strains to their own secreted molecules. a) Mycelial growth of N10, N11, and N12 into pre-inoculated PDA plates. Pre-inoculation treatment is indicated at the top of the photograph. b) Diameter of N10, N11, and N12 mycelia in control and pre-inoculated PDA plates. Asterisks denote statistically significant differences with respect to control (one-way ANOVA and Tukey’s test, P < 0.05.

3.3. Assessment of antifungal activity of secreted metabolites from Talaromyces oaxaquensis

Extracts from liquid cultures of N10, N11 and N12 were obtained to demonstrate the secretion of antifungal metabolites. Ethyl acetate was selected as a solvent since it has been used before to profiling antifungal metabolites in T. pinophilus (Vinale et al. 2017). The effect of the extract of the N10 and N12 extracts in inhibiting the mycelial growth of M5 was evident at 1week of incubation (Fig. 3a). The inhibitory effect of each extract was assessed by measuring the %I as described previously for indirect confrontations. While the extracts of N10 and N12 showed similar inhibition of the mycelial growth of M5, the inhibitory effect of the N11 was minor (Fig. 3b). To determine whether the extract also alters the shape of the hyphae, we visualized the hyphae that emerged in the presence of 50 μg/mL of the extract from the three strains and the corresponding volume of DMSO as control. Hyphae that emerged 24 h after inoculation in the control treatment were hyaline, elongated, poorly septate, and without branching. In the presence of the extracts of N11 and N12, the hyphae were thicker and displayed abnormal hyphal branching that formed a bump-like shape (Fig. 3c). Swellings were also detected, whether isolated or in tandem, which presumably emerged after septum formation (Fig. 3c). Although the N10 extract did inhibit the hyphal growth of FocM5 (Fig. 3a), hyphal deformation was not detected (Fig. 3c).

Fig. 3.

Fig 3

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Effect of the ethyl acetate extract of supernatants on the growth of M5. a) Percentage of Inhibition ( %I) of M5 mycelial growth in M9G supplemented with ethyl acetate extracts from the strains. M9G supplemented with DMSO was used as the negative control to estimate the %I. The letter ‘a’ above the bar indicates that there is no difference among the treatments while ‘b’ indicates that the % Inhibition of N11 is statistically different respect to N10 and N11 according to the one-way ANOVA and Tukey’s test (P < 0.05). b) Representative photographs of hyphae of M5 after 24 h of microconidia inoculation of the control condition (50 % PDA supplemented with DMSO) and the same medium supplemented with 50 μg/mL of extract form the supernatant of N12. See texts for experimental setup. Bar = 10 μm.

3.4. Exploratory analysis of the extrolite diversity of Talaromyces strains

As the confrontation assays illustrate how the secretion of molecules restrict the growth of FocM5, the ethyl acetate extracts were subject to LC-MS2. A total of 81 mass spectra were obtained by combining the results of the results of the three supernatants, and 36 were annotated. The annotated compounds together with non-annotated compounds are visualized as a molecular network wherein every node represents a metabolite and is colored according to its chemical class (Fig. 4). In parallel, LC-MS2 of the biomass was carried out to confirm the production of metabolites detected in the supernatants (Supplementary material, Fig. S1). Table S1 (Supplementary material) shows the list of annotated compounds, as well as the biomass or supernatant where it was detected. Prenol lipids are the most abundant chemical class. Orbuticin and its 32‑hydroxy derivative 15G256α were identified. Vermixocin A was identified in all three supernatants, but the structurally related Purpactin A was only identified in the supernatants of N11 (Fig. 4).

Fig. 4.

Fig 4

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Molecular network of metabolites from supernatants of liquid cultures of N10, N11, and N12. Each node is colored according to its chemical class. The thickness of the edges linking the nodes represents the connectivity according to cosine value. Nodes with a black border are the annotated ones (see Supplementary material, Table 1 for details). The selected compounds Purpactin A (Vermixocin B), Vermixocin A, Orbuticin, and 15G256α are shown in the insets around the molecular network. The numbers in the nodes represent the precursor mass (m/z), including the adduct.

3.5. A molecular docking model predicts that the polyester 15G256α couples to the cavity of the Chs1 of F. oxysporum f. sp. cubense

15G256α has been proposed as a means of targeting fungal cell wall biosynthesis (Schlingmann et al. 2002). A phylogeny of Chss from Foc, Saccharomyces cerevisiae, Colletotrichum graminicola, and CaChs2 revealed that the protein TVY66963 of Foc belongs to the class I of the Chs family and is the homolog of Chs1; therefore, it was named FocChs1 (Supplementary material, Fig. S2, upper panel). The residues that have been previously reported to be involved in enzymatic activity in the class I Chs CaChs2 are conserved in FocChs1 (Ren et al. 2022) (Supplementary material, Fig. S2, lower panel). The predicted tridimensional model of FocChs1 presented a remarkable structural similarity to CaChs2, both in the transmembrane and in the catalytic domain (Supplementary material, Fig. S3). FocChs1 and 15G256α were subject to a protein-ligand docking approach to determine a potential FocChs1–15G256α interaction that might interfere with the chitin biosynthesis. The model showed that 15G256α is placed into the cavity of the catalytic domain (Fig. 5a) and interacts with N250 and E251 (Fig. 5b), both of which are required in the recognition of the substrate UDP-GlucNAc in CaChs2 (Ren et al. 2022).

Fig. 5.

Fig 5

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Molecular docking reveals a potential -FocChs1 interaction. a) Model of the lowest Vina score between 15G256α and FocChs1. The first 174 residues of FocChs1 were removed to facilitate the visualization of the docking. b) Close view of the binding of 15G256α to the catalytic pocket of FocChs1 illustrates the proximity of conserved residues critical to chitin synthase activity. See text and the Supplementary material for details regarding the identification and selection of FocChs1.

4. Discussion

Talaromyces spp have been isolated in different niches and in association with other organisms (Yilmaz et al. 2014). These fungi are endowed with adaptations to abiotic factors as well as factors that increase efficiency when competing and interacting with other microbes and hosts. There are no phytopathogens reported in the Talaromyces genus, and even the soil-borne and endophyte T. flavus strains may be used as biological control agents (Kakvan et al. 2013; Yuan et al. 2017). The relatively low growth rate of the T. oaxaquensis in synthetic rich media suggests a disadvantage when competing for nutrients with other microbes in the soil or in the rhizosphere (Zárate Ortíz et al. 2024). Therefore, the association with plants and endophytic growth might contribute to its persistence in the environment. Moreover, production of antimicrobial molecules might restrict the growth of microbial competitors in its proximity that require nutrients, water, or surfaces to colonize. In this study, direct confrontation assays revealed that although FocM5 is extended in a wider area than N10, N11 and N12, its growth is interrupted in proximity of the mycelia of N10, N11 and N12 (Fig. 1a, upper panel). This gradual inhibition of the growth of FocM5 suggests that T. oaxaquensis secretes antifungal molecules whose effect is visualized as FocM5 approaches to the section of the Petri dish occupied by T. oaxaquensis.

The lower panel of Fig. 1a shows the decreased growth of FocM5 as it nears the previous growth of the three strains, which indicates the constitutive production of antifungal factors. Among the three strains, no statistical differences in inhibition were noted (Fig. 1b). Since these indirect confrontations were performed in rich medium, we ruled out the possibility that the T. oaxaquensis strains consume most of the nutrients of the PDA. Such antifungal factors could have a generalist effect towards fungi, as indirect confrontations among the T. oaxaquensis strains illustrated that the mycelial growth of N11 and N12 decreased due to secreted factors from the three strains (Fig. 2). Activity of efflux pumps, chemical modification of toxins, or the duplication of target genes are known self-protection mechanisms that have emerged in fungi to counteract the effect of their own antifungal factors (Keller et al., 2005). The protective mechanisms may be more effective in N10, as the growth of this strain was similar in the control and the pre-inoculated plates (Fig. 2). The antifungal effect might be the result of the synergy between antimicrobial metabolites plus hydrolytic enzymes. The hydrolysis of two purified chitinases of T. flavus has been reported to inhibit both the spore germination and germ tube elongation of phytopathogenic fungi (Duo-Chuan et al. 2005). Additionally, an analysis of the genomes of T. pinophilus and T. rugulosus revealed 81 and 107 genes encoding fungal cell wall-degrading enzymes, respectively (Wang et al. 2020). Like T. oaxaquenis, both species belong to the section Talaromyces, which could indicate that cell wall-degrading enzymes might be a factor that participates in the antagonism of N10, N11, and N12.

The endophyte strains T. pinophilus F36CF and Talaromyces sp. ZH-154 produce the antifungal metabolites secalonic acid and 3-O-methylfunicone, respectively (Vinale et al. 2017; Liu et al. 2010). The ethyl acetate extracts obtained from the supernatants of N10 and N12 were able to inhibit the mycelial growth of FocM5. Regardless of the inhibitory effect of N11 detected in direct or indirect confrontations, the N11 extract showed weak repression of the mycelial growth (Fig. 3a and b). The composition of secondary metabolites relies on clusters of genes encoding biosynthetic enzymes together with their respective transporters and transcriptional regulators (Keller et al. 2005). Polymorphisms in biosynthetic gene clusters and alterations in the chromatin structure might drive changes in the expression of genes encoding biosynthetic enzymes, and the subsequent production of antifungal compounds might explain the weaker inhibitory effect of the N11 extract. The secretion cell wall-degrading enzymes or the insolubility of metabolites in ethyl acetate might confer N11 with its inhibitory effect, as illustrated in Fig. 1.

The altered hyphal morphology of FocM5 and swellings were observed along the hyphae growing in the presence of the N11 and N12 extracts (Fig. 3b). Hyphal swellings might be caused by a decrease in the chitin of the cell wall, either by the deletion of Chs genes or by the addition of chemical inhibitors of Chss (Werner et al. 2007; Sánchez León et al. 2011). Although the N10 extract inhibited the mycelial growth of FocM5, swellings were not microscopically detected, which implies that the potential inhibition of cell wall deposition in altering hyphal morphology was not the only event that caused the overall mycelial growth inhibition of FocM5.

LC-MS2 revealed 36 annotated compounds (Supplementary material, Table 1), either specific to the supernatants, specific to the biomass, or identified in both. Only metabolites with potential activity are discussed in this report. The penicillide Vermixocin A and the macrocyclic polyester 15G256α (32‑hydroxy Orbuticin) were the metabolites identified in the supernatants of all three strains (Fig. 4). Purpactin A, which is an acetylated derivative of Vermixocin A, was another penicillide present in the biomass of the three strains, but it was exclusively detected in the supernatant of N11 (Fig. 4; Supplementary material, Table S1). Vermixocin A inhibits the incorporation of 14C-labeled uridine into P388 mouse cells (Proksa et al., 1992). It is not clear whether this potential inhibition of RNA synthesis might impact the growth of FocM5. Neither Vermixocin A nor Purpactin A inhibits the growth of Aspergillus fumigatus and C. albicans, but additional penicillide derivatives have been shown to inhibit fungal growth (Komai et al. 2006). However, Vermixocin A purified from Penicillium aculeatum PSU-RSPG105 is active against Crytopcoccus neoformans (Daengrot et al. 2016). These findings indicate that the structure of the target and the mechanisms of detoxification are also factors that influence the inhibitory activity of Vermixocin A. Vermixocin A has also been identified in an ethyl acetate extract of the endophyte Alternaria sp. KTDL7, which is toxic to gliobastoma cells (Tapfuma et al. 2019). Purpactin A has been reported as an inhibitor of human acyl-CoA cholesterol acyltransferase, as well as an inhibitor of the TMEM16A chloride channel (Ohshiro et al. 2007; Yimnual et al. 2021), but it is unclear whether such activities can be extrapolated to fungal growth inhibition.

Orbuticin and 15G256α are macrocyclic polyesters identified in Hypoxylon oceanicum, Penicillium verruculosum, and Acremonium butyri (Schlingmann et al. 2002; Breinholt et al. 1993; Roy et al. 1996). The 32-hydrolylation of Orbuticin to produce 15G256α has been proposed as the final step of the cyclic polyester biosynthetic pathway in T. stipitatus CBS 349.72, a strain isolated from flowers of Tagetes patula (Al Fahad 2022). Orbuticin and 15G256α inhibit cell wall formation, and 15G256α presents higher activity, especially against phytopathogens such as Botrytis cinerea, Sclerotinia sclerotium, and Monilinia fructigena (Breinholt et al. 1993). In the present study, the activity of 15G256α might be reflected in the direct and indirect confrontations (Fig. 1) and in the hyphal swellings presented upon treatment with the extracts (Fig. 3). 15G256α was selected to investigate whether it can interfere with Chs activity, as it is more active compared to Orbuticin and is considered the final product of cyclic polyester metabolism (Breinholt et al. 1993; Al Fahad 2022). A phylogeny of the members of the Chs family of Foc and selected Chs proteins revealed that an enzyme from class I Chs (FocChs1) is closely related to CaChs2. Residues of the catalytic domain and interface involved in the recognition of UDP-GucNAc were conserved (Supplementary material, Fig. S2), as was the overall tertiary structure predicted by AlphaFold (Supplementary material, Fig. S3). The ligand-receptor model 15G256α-FocChs1 illustrates the potential binding of 15G256α to a cavity that corresponds to the catalytic pocket (Fig. 5a). The catalytic pocket is also targeted by the known class I Chs inhibitors Nikkomycin Z and Polyoxin D (Ren et al. 2022). Potential electrostatic interactions with residues involved in the recognition of UDP-GlucNAc strengthened the binding of 15G256α to the catalytic pocket (Fig 5b). For example, E321 is critical to the activity of CaChs2 and interacts with the above-mentioned inhibitors (Ren et al. 2022). The residue of FocChs1 that aligns with E321 was E251, which interacts with 15G256α (Supplementary material, Figs. S2 and 5b). Other residues of FocChs1 positioned near 15G256α were D393, Q554, and R557, which might be required for the catalysis (Supplementary material, Figs. S2 and 5b). Therefore, the Talaromyces strains might repress the growth of FocM5 and possibly the growth of other fungal species by targeting the class I Chs with 15G256α, which acts as a competitive inhibitor as it occupies the catalytic pocket and interacts with residues involved in the recognition of UDP-GlucNAc.

The biosynthesis of 2IG256α is likely dependent on two polyketide synthases whose genes are encoded into a biosynthetic gene cluster in T. stipitatus (Al Fahad 2022). 6-Hydroxymellein has been proposed as a derailment product of one of those synthases, as its dihydroxylated aromatic ring is part of the final structure of polyesters (Schlingmann et al. 2002). 6- Hydroxymellein was not identified in the metabolite profiling presented here, but related metabolites such as 5,6-Dihydroxymellein were present in the supernatants of N11 and N12, and MLS002706482 was detected in the supernatants of all three strains (Supplementary material, Table 1). 5,6-Dihydroxymellein and MLS002706482 could hint at a mechanism of self-protection by degradation of 2IG256α. However, further experiments are necessary to determine the link between polyesters and their related metabolites, as well as their biological activity towards fungi. In this context, 5,6-Dihydroxymellein produced by Penicillium chrysogenum has antibacterial activity, and its affinity to b-lactamases has been demonstrated by molecular docking (Orfali et al. 2022). These findings suggest that the strains can also influence bacterial growth via 5,6-Dihydroxymellein. There were not b-lactam rings identified in this study, but the identification of 5,6-Dihydroxymellein suggests that T. oaxaquensis might benefit other plant-associated or soil-borne fungi that produce b-lactam antibiotics such as Penicillium spp. Therefore, the strains characterized here are suitable models to perform biochemical and molecular studies regarding the biosynthesis of polyesters and their biological role towards different organisms.

Although quantitative metabolomics is necessary to know the ratio of each metabolite, either antifungal or not, here we reported that T. oaxaquensis constitutively secretes metabolites that limit the growth and causes malformation of the hyphae of FocM5 and possibly other fungi that concur in the same niche, whether soil, rhizosphere or plant tissue. In this way, T. oaxaquensis ensure a competitors-free space in its proximity that allows for the acquisition of nutrients, their settlement in the environment and access into the plant. This set of metabolites and the natural adaptation of T. oaxquenesis to banana plants and to tropical climate conditions are a suitable combination that might lead to the implementation of novel strategies to control the fusarium wilt.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The presented research was funded by the Universidad del Mar (grant no 2IG2102). LDMB is supported by the program ‘Investigadoras e Investigadores por México’, Project 538. We thank Isabel Zárate Hernández for the technical assistance.

Footnotes

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.crmicr.2025.100402.

Contributor Information

Aneliz de Ita Zárate-Ortiz, Email: anelizortiz98@gmail.com.

José Luis Villarruel-Ordaz, Email: jvillarruel@aulavirtual.umar.mx.

Ana Claudia Sánchez-Espinosa, Email: anaclaudia@aulavirtual.umar.mx.

Rommel A. Carballo-Castañeda, Email: rommelomics@gmail.com.

Aldo Moreno-Ulloa, Email: amoreno@cicese.mx.

Luis David Maldonado-Bonilla, Email: maldonado@zicatela.umar.mx, maldonado@aulavirtual.umar.mx.

Appendix. Supplementary materials

mmc1.docx (14.7KB, docx)
mmc2.docx (12.5KB, docx)
mmc3.jpg (557.5KB, jpg)
mmc4.jpg (1.1MB, jpg)
mmc5.jpg (1.4MB, jpg)
mmc6.xlsx (16.5KB, xlsx)

Data availability

Data will be made available on request.

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Associated Data

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Supplementary Materials

mmc1.docx (14.7KB, docx)
mmc2.docx (12.5KB, docx)
mmc3.jpg (557.5KB, jpg)
mmc4.jpg (1.1MB, jpg)
mmc5.jpg (1.4MB, jpg)
mmc6.xlsx (16.5KB, xlsx)

Data Availability Statement

Data will be made available on request.

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