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 Fungal diversity from Fildes Peninsula (Antarctica) and their antibiosis bioactivity against two plant pathogens
Ji Seon Kim1, Enzo Romero2, Yoonhee Cho1, Ramón Ahumada-Rudolph2, Christian Núñez2, Jonhatan Gómez-Espinoza3, Ernesto Moya-Elizondo4, Sigisfredo Garnica5, Young Woon Lim1,*, Jaime R. Cabrera-Pardo2,6,*

DOI: https://doi.org/10.71150/jm.2411029
Published online: April 14, 2025

1School of Biological Sciences and Institute of Biodiversity, Seoul National University, Seoul 08826, Republic of Korea

2Applied and Sustainable Chemistry Laboratory (LabQAS), Department of Chemistry, Universidad del Bío-Bío, Concepción 4051381, Chile

3Technical Professional High School Diego Portales, Department of Science, Linares, Chile

4Department of Plant Production, Faculty of Agronomy, Universidad de Concepción, Concepción 3812120, Chile

5Institute of Biochemistry and Microbiology, Faculty of Sciences, Universidad Austral de Chile, Teja Island, Valdivia 5090000, Chile

6College of Dental Medicine, Roseman University of Health Sciences, South Jordan, UT 84095, USA

*Correspondence Young Woon Lim E-mail: 'ywlim@snu.ac.kr'
Jaime R. Cabrera-Pardo E-mail: 'jacabrera@ubiobio.cl'
• Received: November 26, 2024   • Revised: February 4, 2025   • Accepted: February 13, 2025

© The Microbiological Society of Korea

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Antarctic fungi can effectively adapt to extreme environments, which leads to the production of unique bioactive compounds. Studies on the discovery of fungi in the diverse environments of Antarctica and their potential applications are increasing, yet remain limited. In this study, fungi were isolated from various substrates on the Fildes Peninsula in Antarctica and screened for their antibiosis activity against two significant plant pathogenic fungi, Botrytis cinerea and Fusarium culmorum. Phylogenetic analysis using multiple genetic markers revealed that the isolated Antarctic fungal strains are diverse, some of which are novel, emphasizing the underexplored biodiversity of Antarctic fungi. These findings suggest that these fungi have potential for the development of new antifungal agents that can be applied in agriculture to manage fungal plant pathogens. Furthermore, the antibiosis activities of the isolated Antarctic fungi were evaluated using a dual-culture assay. The results indicated that several strains from the genera Cyathicula, Penicillium, and Pseudeurotium significantly inhibited pathogen growth, with Penicillium pancosmium showing the highest inhibitory activity against Botrytis cinerea. Similarly, Aspergillus and Tolypocladium strains exhibited strong antagonistic effects against Fusarium culmorum. This study enhances our understanding of Antarctic fungal diversity and highlights its potential for biotechnological applications.
  • Keywords: Antarctic fungi, antibiosis, Botrytis cinerea, Fusarium culmorum
Fungi are among the largest groups of organisms and thrive in diverse environments, where they occupy multiple ecological niches and play several roles, including saprotrophic, pathogenic, and symbiotic roles, making them essential ecosystem components (Kendrick, 2011; Naranjo-Ortiz and Gabaldón, 2019). Globally, their biomass accounts for approximately 12 gigatons of carbon (Bar‐On et al., 2018). Consequently, they exhibited a distinctive metabolic plasticity that enables rapid adaptation and survival through the biosynthesis of various natural products (Bhattarai et al., 2021; Gholami-Shabani et al., 2019). Fungi-derived natural products are pharmaceutically prolific and have been developed for several important biological applications, ranging from highly potent toxins to approved drugs (Aly et al., 2011; Rastegari et al., 2020; Schueffler and Anke, 2014; Vicente et al., 2003).
Antarctica represents one of the most extreme environments on Earth for the existence of life. This ecosystem exhibits high-stress conditions, including low temperatures, sporadic and limited nutrient availability, high aridity, and elevated ultraviolet radiation levels. Antarctic fungi must adapt to survive under these highly demanding conditions (Hassan et al., 2016). These adaptations result from modifications in gene expression and secondary metabolite biosynthesis, forming biologically relevant chemical spaces that allow them to survive efficiently in Antarctica (Varrella et al., 2021; Zucconi et al., 2020).
Studies on fungi in Antarctic ecosystems are limited. However, many studies on Antarctic fungi have explored the diversity and potential applications of culturable fungi from various Antarctic environments (González et al., 2020; Varrella et al., 2021). Despite these efforts, many studies on fungal diversity in Antarctica rely primarily on the internal transcribed spacer (ITS) region, a universal fungal genetic marker (Schoch et al., 2012), which often leads to inaccurate identification (Dupuis et al., 2012; Kiss, 2012). This difficulty in species identification limits our understanding of fungal biology and its potential applications.
Most studies on Antarctic fungi have focused primarily on the characteristics of secondary metabolites, including novel metabolite production and antibacterial properties (Ordóñez-Enireb et al., 2022; Shi et al., 2022; Vieira et al., 2018). However, their potential use, particularly in combating plant pathogens, remains undetermined. Recent findings regarding natural compounds that capable of inhibiting plant diseases have generated renewed interest (Kim and Hwang, 2007; Vinale et al., 2014; Wang et al., 2023). Therefore, Antarctic fungi may be promising candidates with hidden and remarkable capabilities.
Botrytis cinerea and Fusarium culmorum are representative plant pathogenic fungi that cause significant economic losses to agriculture. Botrytis cinerea, responsible for grey mold, is a highly destructive pathogen and is estimated to cause nearly $100 billion in annual agricultural losses (Dwivedi et al., 2024; Roca-Couso et al., 2021). The destructive nature of this fungus ranks second among scientifically and economically relevant pathogenic fungi (Dean et al., 2012). In Chile, B. cinerea affects grapes by reducing both yield and quality during ripening. Integrated management practices, including cultural, chemical, and biological methods, are crucial for controlling this pathogen in Chilean vineyards under temperate and humid conditions (Herrera-Défaz et al., 2023; Latorre et al., 2015).
Fusarium culmorum, on the other hand, affects cereals, such as wheat and barley, causing Fusarium head blight, which reduces grain yield and quality. The presence of this pathogen in Chile is significant, especially in humid areas where it can produce mycotoxins such as deoxynivalenol, posing additional food safety concerns (Scherm et al., 2013). Chemical strategies through fungicides are currently the most widely used methods for controlling infections. Both B. cinerea and F. culmorum have developed resistance to several conventional fungicides (Yin et al., 2023), causing substantial agricultural damage worldwide (Hahn, 2014). Therefore, discovering new natural molecules with high efficiency in controlling plant pathogenic fungal growth is of vital importance to the agricultural sector.
During the Antarctic expedition (ECA59) funded by the Chilean Antarctic Institute, we collected several environmental samples, including soil, lichens, plants, and snow, from the Fildes Peninsula, Antarctica. We isolated 97 fungal strains and examined their diversity and antibiosis ability against two plant pathogens. Through phylogenetic analysis using multi-genetic markers (ITS, LSU, ACT, RPB2, TEF1, and TUB) specific to each taxonomic group, we elucidated species diversity with considerable accuracy. Using a dual-culture assay approach, we evaluated the antibiosis potential of all Antarctic fungal strains against B. cinerea and F. culmorum. Several strains from the genera Aspergillus, Cyathicula, Penicillium, Pseudeurotium, Pseudogymnoascus, and Tolypocladium showed a remarkable capacity to control the growth of these phytopathogens. Thus, our study offers comprehensive insights into the diversity of culturable fungi in Antarctica and their potential for antibiosis. This study will broaden the understanding of Antarctic fungi and establish groundwork for future research.
Sample collection and processing
Antarctic samples for fungal isolation were collected from the Fildes Peninsula, Antarctica in March 2023 (Fig. 1). The exact locations and sample types are listed in Table 1. Samples were collected in sterilized falcon tubes (28×120 mm²) using a metal spatula sterilized with 70% alcohol, transported to Julio Escudero Base Laboratories, and stored at 4°C. They were then transported to the Laboratory of Applied and Sustainable Chemistry (LabQAS; Universidad del Bío-Bío, Chile).
A measured amount (5 g) of each collected sample (sediment, soil, moss, and fruiting body) was resuspended in 10 ml of sterile Type I ultrapure water. From the resulting suspension, 500 µl was plated on Potato Dextrose Agar (PDA; Difco, USA) supplemented with 100 mg/ml tetracycline and 100 mg/ml streptomycin to prevent bacterial contamination and incubated at 13–17°C for one week. Endophytic fungi were isolated from Deschampsia antarctica followed the method outlined by Ismail et al. (2021), with some modifications. Briefly, approximately 5 g of root was washed under running tap water to remove any residual soil. Roots that died or showed signs of lesions or discoloration were excluded from the study. The remaining healthy roots were surface sterilized by immersion in 70% ethanol for 3 min, followed by a 2.5 min soak in sodium hypochlorite solution (approximately 5% active chlorine). The roots were then rinsed three times with sterile Type I ultrapure water for 3 min. After surface sterilization, the roots were dried on sterile filter paper and cut into small segments. Seventy root segments per plot were placed on PDA media supplemented with 100 µg/ml tetracycline and 100 mg/ml streptomycin to inhibit bacterial growth. The plates were incubated at 15°C for 4 weeks. The cultures were carefully monitored for fungal mycelia emergence. Once the mycelia were observed, they were immediately transferred to fresh PDA plates to encourage further growth.
Distinct fungal colonies were selected based on their morphological characteristics, including colony color, texture, border type, and radial growth rate. These distinct colonies were then sub-cultured on fresh PDA plates to obtain pure fungal strains. All fungal strains were deposited in the LabQAS Fungal Collection at the Universidad del Bío-Bío, Chile.
Molecular identification
Genomic DNA was extracted from lyophilized tissues of each fungal strain grown on PDA (using 5 mm diameter blocks) using an AccuPrep Genomic DNA extraction kit (Bioneer Co., Korea), following the manufacturer’s instructions, with a modification of the CTAB buffer instead of the TL buffer. Polymerase chain reaction (PCR) was performed on a C1000 thermal cycler (Bio-Rad, USA) using the AccuPower PCR premix (Bioneer Co., Korea). The primer sets ITS1 and ITS4 (White et al., 1990) were used to amplify the ITS region for all fungal strains under the following conditions: 95°C for 5 min; 35 cycles of 95°C for 40 s, 55°C for 40 s, and 72°C for 1 min; and 72°C for 5 min. All PCR products were verified by gel electrophoresis on a 1% agarose gel and Gel Doc™ XR (Bio-Rad, USA). The PCR products were purified using the Expin™ PCR Purification Kit (GeneAll Biotechnology Co., Korea). DNA sequencing was performed with the same primers used for PCR by Macrogen (Korea), using an ABI PRISM 3700 Genetic Analyzer (Life Technologies, USA). The resulting sequences were proofread and manually edited using Geneious Prime software ver. 2024.0.7 (Biomatters Ltd., USA; Kearse et al., 2012). The forward and reverse sequences obtained were assembled using the de novo assembly function in Geneious Prime software ver. 2024.0.7 (Biomatters Ltd., USA; Kearse et al., 2012).
Preliminary identification at a higher taxonomic level (mostly at the genus level; if not possible, then at the family level) was performed using NCBI BLAST with the ITS region sequences. Based on the preliminary identification via NCBI BLAST, appropriate additional genetic markers for each genus were selected through a reference search to allow for species-level identification (Table S1). The PCR conditions for each primer set are summarized in Table S1. The generated sequences were sequenced and edited according to the same protocol used to generate the ITS sequences. All newly generated sequences were deposited in GenBank (Table 1).
For phylogeny-based identification, reference sequences (mostly holotype sequences) were retrieved from GenBank. When holotype sequences were unavailable, verified strain sequences from the published literature were used (Table S2). Using both reference sequences and the newly generated sequences, phylogenetic analyses were performed using FunVIP 0.3.19 with the ‘--preset fast’ setting, employing FastTree for tree construction (https://github.com/Changwanseo/FunVIP; Seo et al., under Review). The set of genetic markers used for the final identification varied depending on the genus. The final species assignment was validated based on phylogenetic evidence, specifically the branch length and local support values of the phylogenetic tree generated using FastTree v.2.1.11 (Price et al., 2010).
To construct the phylogenetic tree shown in Fig. 2, RAxML phylogenetic analysis was conducted using the GTR+GAMMA model with 1,000 replicates using RAxML ver. 8 (Stamatakis, 2014). The analysis incorporated the ITS and LSU sequences of the strains obtained in this study, along with two outgroup sequences, Conidiobolus coronatus AFTOL-ID 137 and Entomophaga maimaiga ARSEF 1400 (Gryganskyi et al., 2012).
Antibiosis assay employing dual-culture method against B. cinerea and F. culmorum
Antarctic fungal strains were evaluated against two pathogenic fungi, B. cinerea and F. culmorum. For in vitro assays, the strain of B. cinerea F003 was obtained in 2006 from the blueberry fruit cv. O’Neal, infected with this fungus, in Chillán, Ñuble Region, Chile. The strain was identified based on its microscopic morphological characteristics (presence of conidia and conidiophores) and confirmed by PCR using specific primers Bc3F/R, which amplify the intergenic spacer (IGS) region of the ribosomal DNA of B. cinerea (Suarez et al., 2005). The pathogenic isolate of F. culmorum strain F066 was isolated from European hazelnut cv. Barcelona in Camarico, Maule Region, Chile. Identification was based on the microscopic morphological characteristics and phylogenetic analysis of the ITS (MT640271), RPB2 (MT997139), TEF1 (MT661593), and CAL (MT997140) regions (Mishra et al., 2000; O'Donnell et al., 2000, 2008).
Mycelial disks (5 mm in diameter) of Antarctic fungal strains and pathogens were obtained from the margin of an actively growing culture using a cork borer. Both mycelial disks were placed on a Petri dish with 15 ml of PDA and positioned 6 cm apart. The negative controls consisted of mycelial disks from the pathogen alone. The plates were incubated in dark in a culture chamber at 25°C. The percentage of inhibition of radial growth (PIRG) was calculated using the following equation:
PIRG%=Dc−DtDc×100
where PIRG is the percentage of growth inhibition,
Dc is the growth (mm) of the pathogenic fungus in the control group.
Dt is the pathogen growth (mm) in the presence of an Antarctic fungus.
Three replicates were performed for each treatment group. Antagonistic activity was evaluated by measuring the growth radius of the pathogenic fungal mycelia. Once the pathogenic fungus grew free of competition (negative control) and occupied the entire plate, the experiment was terminated. Fusarium culmorum and B. cinerea occupied the entire plate in 15 and 10 days, respectively.
Identification of Antarctic fungi
A total of 97 Antarctic fungal strains were isolated from biotic (moss, lichen, fruit body, macroalgae, and root) and abiotic substrates (soil, sediment, ice, and styrofoam) in similar proportions (Fig. 2), with 48% and 40% of each substrate type, respectively. The substrate type with the highest number of fungal strains was soil (20 strains), followed by moss (18 strains), and roots (16 strains; Table 1).
The ITS region sequences were successfully obtained from 95 of the 97 strains. NCBI BLAST analysis was performed using the ITS region of these 95 strains, whereas the LSU region was used for the remaining two strains. This preliminary analysis identified 97 strains representing 58 taxa. Among these, 54 taxa were assigned to 19 known genera, whereas the remaining four taxa could not be assigned to any known genera. These four taxa matched annotated fungal sequences in the NCBI BLAST database: “Dothideomycetes sp.” (strain numbers: 1808, 1816), “Fungal sp.” (1818, 1824), “Helotiales sp.” (1812, 1813, 1830, 1855, 1859, 1884), and “Uncultured endophytic fungi” (1822, 1842).
Based on previous studies, additional genetic markers suitable for each taxonomic classification were selected, and 132 additional genetic marker sequences were acquired (Table 1): 44 sequences in the LSU region, 34 in the TUB region, 7 in the CMD region, 10 in the ACT region, 34 in the TEF1 region, and 3 in the RPB2 region. Phylogenetic analysis using multiple genetic markers was conducted, along with the appropriate reference sequences for each genus. The analysis confirmed that the 58 taxa belonged to three phyla: 6 classes (2 isolates in Agaricomycetes, 8 in Dothideomycetes, 22 in Eurotiomycetes, 47 in Leotiomycetes, 3 in Mortierellomycetes, and 15 in Sordariomycetes), 12 orders (1 isolate in Agaricales, 1 in Amphisphaeriales, 1 in Atheliales, 5 in Cladosporiales, 21 in Eurotiales, 21 in Helotiales, 14 in Hypocreales, 3 in Mortierellales, 1 in Onygenales, 3 in Pleosporales, and 26 in Thelebolales), 21 families, and 23 genera (Fig. S1). Approximately 30% of the 97 strains (29 strains) were identified at the species-level, whereas the remaining 70% were confirmed as new species candidates, particularly those concentrated in Leotiomycetes. The complete strain phylogeny is presented in Fig. 2, based on ITS and LSU sequences, and the final identification results are reflected in the strain annotations.
Antibiosis evaluation of Antarctic fungi against B. cinerea and F. culmorum
Using a dual-culture assay approach and PIRG as a quantifiable variable, we evaluated the antibiosis potential of all isolated fungal strains against B. cinerea and F. culmorum (Tables S3 and S4). Overall, remarkable antibiosis bioactivities were observed in the isolated fungal strains, with the best examples shown in Fig. 3.
The isolated Antarctic fungi exhibited antibiosis activity against B. cinerea and F. culmorum, with PIRG values ranging from 0 to 72.95% and from 0 to 53.45%, respectively (Tables S3 and S4). Based on the PIRG values, antibiosis activity was categorized into four levels: +++ (PIRG: >40%), ++ (PIRG: 20–40%), + (PIRG: 0–20%), and 0 (no inhibition). The strains showing the highest level of inhibition (+++) included 36 and 8 strains against B. cinerea and F. culmorum, respectively (Tables S3 and S4). The antibiosis activity of the isolated Antarctic fungi was, on average, higher against B. cinerea than against F. culmorum (Fig. 4). However, the antibiosis activity of each fungal strain against the two plant pathogenic fungi did not always align consistently.
Three Penicillium pancosmium strains, 1878, 1887, and 1892, showed elevated levels of antibiosis against B. cinerea, with PIRG values of 71.1, 71.1, and 66, respectively. Additionally, new species candidates of the genera Cyathicula (1830) and Pseudeurotium (1874) showed remarkable levels of antibiosis activity, with PIRG values of 66.9 and 65.1, respectively (Fig. 4A, Table S3). Against F. culmorum, the new species candidates of Aspergillus (1877) and Tolypocladium (1860) most actively controlled pathogen growth, with PIRG values of 31.8 and 30.8, respectively. In addition, two Pseudogymnoascus species (1815 and 1807) and one Pseudeurotium strain (1872) controlled F. culmorum growth (PIRG = 30.8, 27.6, and 29.5, respectively; Fig. 4B, Table S4).
We successfully isolated 58 diverse fungal taxa at the species level from various regions and substrates in Antarctica, representing the first report of culturable fungi associated with Antarctic fruiting bodies. Additionally, we evaluated the antibiosis potential of all fungal strains isolated during the Antarctic expedition (ECA 59) against B. cinerea and F. culmorum. This study revealed several Antarctic strains that substantially inhibited the growth of agriculturally relevant fungal pathogens, thereby emphasizing their ecological and biotechnological significance.
A significant number of these isolated fungal strains were identified as new species candidates because they showed no match at the species-level in the existing species databases. This highlights the lack of comprehensive taxonomic studies on Antarctic fungi and their underrepresentation in global databases. Furthermore, discrepancies between the final phylogenetic identification and ITS-based BLAST results were observed, particularly within the orders Pleosporales and Helotiales. For instance, strains preliminarily identified as “Fungal sp.” (1818 and 1824) and “Helotiales sp.” (1812, 1830, and 1859), based on ITS-based BLAST, were later classified as Cyathicula through phylogenetic analysis. A detailed taxonomic study revealed that the closest known species, Cyathicula microspora, shared only 86.1% to 92.3% ITS sequence identity with these Antarctic fungal strains, indicating a substantial genetic divergence. These findings further highlight the limitations of fungal sequence curation in the NCBI database, particularly for the identification of Antarctic fungi, due to the lack of taxonomic studies on these organisms.
Furthermore, the limitations of ITS as the sole marker and the necessity of multi-genetic approaches for accurate fungal taxonomy were also pointed out, when studying for Antarctic fungi. To overcome the taxonomic ambiguities of Antarctic fungi, we applied a multigene marker-based approach to discover new species candidates. This approach is particularly effective for genera such as Penicillium and Cladosporium, which require additional markers, such as TUB and RPB2, for reliable species-level classification (Bensch et al., 2012; Visagie et al., 2014). By applying this approach, we resolved taxonomic ambiguities and demonstrated its utility in revealing previously uncharacterized fungal diversity. By providing accurate information on these poorly studied Antarctic fungi, this study contributes to the understanding of their potential impact on the changing Antarctic ecosystem and their hidden capabilities for various future applications.
Taxonomic ambiguities in identifying Antarctic fungi were particularly pronounced in the class Leotiomycetes, a group frequently reported in polar environments, including soil, moss, and marine habitats, such as algae, seawater, and sponges (Kochkina et al., 2014, 2019; Ordóñez-Enireb et al., 2022; Rämä et al., 2017; Rosa et al., 2019, 2020). Despite their ecological significance (Bates et al., 2012; Câmara et al., 2021; Kochkina et al., 2014; Park et al., 2015; Yu et al., 2018), Leotiomycetes remain understudied, with many unresolved taxonomic issues (Johnston et al., 2019; Quandt and Haelewaters, 2021). This makes the species-level identification particularly difficult for Antarctic Leotiomycetes (Henríquez et al., 2014; Hirose et al., 2016, 2017; Kochkina et al., 2014; Ordóñez-Enireb et al., 2022). Recent studies have reported an increasing association between Antarctic mosses and Antarctic Leotiomycetes species (De Carvalho et al., 2019; Hirose et al., 2016, 2017), with some Leotiomycetes species identified as pathogenic (Rosa et al., 2020, 2021). These findings underscore the need for accurate identification within this class.
Our findings highlight the antifungal potential of Antarctic fungi, many of which are poorly understood. A dual-culture assay revealed significant antifungal activity against two major phytopathogens, B. cinerea and F. culmorum. On average, B. cinerea was more susceptible to the antibiosis effects of the Antarctic fungal isolates than F. culmorum (Fig. 4). Fungi belonging to Eurotiales, including Penicillium pancosmium, exhibit particularly strong antibiosis activity, suggesting their potential as natural fungicides. Although Penicillium species are well-documented for their biocontrol activities (Roca-Couso et al., 2021; Thambugala et al., 2020), studies on P. pancosmium remain limited, making this a notable discovery.
Among the new species candidates, strains from Cyathicula and Pseudeurotium showed the highest levels of antibiosis activity against both plant pathogens. To the best of our knowledge, this is the first report of the antifungal activity of Cyathicula. Although other species of the family Helotiaceae, to which Cyathicula belongs, also produce various secondary metabolites with antifungal properties (Chen et al., 2013; Elhamouly et al., 2022), the discovery of such activity in Cyathicula expands our understanding of the functional diversity within Helotiaceae, highlighting its potential as a source of novel antifungal compounds. Moreover, Antarctic strains of Aspergillus, Penicillium, Pseudeurotium, and Tolypocladium exhibited antibiosis activity. These fungal groups were well-known for synthesizing antifungal secondary metabolites (Bladt et al., 2013; Brown et al., 1976; Bushley et al., 2013; Heo et al., 2019; Khokhar et al., 2011; Quandt et al., 2015; Wang et al., 2023).
Notably, Pseudogymnoascus, the most taxonomically diverse genus identified in this study (6 taxa, 18 isolates), demonstrated significant antifungal activity, with most showing above-average activity against at least one plant pathogen. This aligns with the results of previous studies indicating the capacity of Pseudogymnoascus to synthesize diverse antifungal compounds, such as amphiols, geomycins A–C, and various sesquiterpenes (Antipova et al., 2023; Shi et al., 2021). These findings emphasize their potential as key sources of bioactive compounds and their ecological role in Antarctic environments, where antifungal properties may confer adaptive advantages. This study highlights the immense microbial diversity within Antarctic ecosystems and their potential to be broadly applicable in biotechnology, agriculture, and medicine. The extreme conditions in Antarctica likely drive unique selective pressures, fostering the evolution of microorganisms producing distinctive secondary metabolites (Marx et al., 2007; Núñez-Montero and Barrientos, 2018; Ramasamy et al., 2023).
Therefore, this study improves our understanding of Antarctic fungi by elucidating their diversity across various Antarctic habitats and their antibiosis activity against plant pathogenic fungi. Furthermore, this study highlights the importance of applying multi-genetic approaches for the accurate identification and taxonomic classification of fungi in underexplored regions, such as Antarctica. By identifying new species candidates and characterizing their antibiosis activity against B. cinerea and F. culmorum, we demonstrate the immense potential of Antarctic fungi as a source of novel bioactive compounds with profound biotechnological applications. As the Antarctic ecosystem continues to undergo changes, this study establishes a foundation for future ecological and biotechnological research by providing critical insights into fungal taxonomy and physiology.
The online version contains supplementary material available at https://doi.org/10.71150/jm.2411029.
Table S1.
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jm-2411029-Supplementary-Table-S1.xlsx
Table S2.
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Table S3.
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jm-2411029-Supplementary-Table-S3.xlsx
Table S4.
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jm-2411029-Supplementary-Table-S4.xlsx
Fig. S1.
Phylogenetic trees of the 97 fungal strains classified by each genus. Each tree, from A to W, is organized by genus, with the genus name, type of tree constructed, and the genetic markers used for the phylogenetic analysis indicated. Our strains are highlighted in bold, and the final identification results are marked with boxes.
jm-2411029-Supplementary-Fig-S1.pdf
Fig. 1.
Sampling sites in Antarctica (ECA59 Expedition) with photographs of each sample type. (A) Map indicating the sampling sites with the location of research stations from Chile and South Korea. Representative photographs of (B) fruit body, (C) ice, (D) lichen, (E) moss, (F) sediment, and (G) soil samples.
jm-2411029f1.jpg
Fig. 2.
Phylogenetic tree of 97 fungal strains isolated in this study. The phylogenetic tree was constructed using RAxML analysis with internal transcribed spacer (ITS) and LSU sequences. The final identification results for each strain are shown along with the strain numbers in bold. Bootstrap values greater than 70% are indicated at each branch node, and branches with a bootstrap value of 100 are represented by thick lines. The substrate type from which each strain was isolated is indicated next to the strain, with the corresponding type highlighted by a colored box. For clarity, the substrate types are listed at the top of each column.
jm-2411029f2.jpg
Fig. 3.
Images showing the top five strains with the highest antibiosis activity against two plant pathogens. The leftmost image in each row represents the control for B. cinerea and F. culmorum. Strain numbers and identification results are indicated below each plate.
jm-2411029f3.jpg
Fig. 4.
Antibiosis activity of Antarctic fungal strains against two plant pathogens. The graphs show the antibiosis activity results, ranked from highest to lowest, for (A) B. cinerea and (B) F. culmorum. The average percentage of inhibition of radial growth (PIRG) is indicated by the dashed line in each graph. Antibiosis activity is categorized into four levels, represented by distinct colors: (+++) in green, (++) in yellow, (+) in light gray, and below-average in gray.
jm-2411029f4.jpg
Table 1.
Collection information and accession numbers of the 97 fungal strains isolated in this study
Order Family Species identification Strain NUM Substrate Latitude (S) Longitude (W) ITS LSU TUB CMD ACT TEF1 RPB2
Agaricales Strophariaceae Pholiota baeosperma 1839 - - - PQ427716 PQ427669
Amphisphaeriales Amphisphaeriaceae Microdochium lycopodinum 1844 Moss 62°10'11.4168" 58°51'10.2096" PQ427765 PQ427672
Atheliales Atheliaceae Athelia arachnoidea 1831 Lichen 62°10'32.9340" 58°55'28.6860" PQ427721
Cladosporiales Cladosporiaceae Cladosporium inversicolor 1898 Root 62°09'56.8980" 58°55'35.2488" PQ427783 PQ433547
Cladosporium sp.1 1819 - - - PQ427699
Cladosporium sp.2 1868 Fruit body 62°10'10.8408" 58°51'02.6460" PQ427748 PQ433531 PQ433545
Cladosporium sp.3 1869 - - - PQ427747
Cladosporium sp.4 1886 Root 62°09'56.8980" 58°55'35.2488" PQ427692 PQ433530 PQ433546
Eurotiales Aspergillaceae Aspergillus sp. 1877 Root 62°09'56.8980" 58°55'35.2488" PQ427757 PQ456765
1888 Root 62°09'56.8980" 58°55'35.2488" PQ427709
1889 Root 62°09'56.8980" 58°55'35.2488" PQ427694 PQ456764
1893 Root 62°09'56.8980" 58°55'35.2488" PQ427710
Penicillium angulare 1806 Soil 62°10'11.4168" 58°51'10.2096" PQ427704 PQ456772
Penicillium crustosum 1804 Soil 62°13'48.2520" 58°57'19.5336" PQ427740 PQ456773
Penicillium jamesonlandense 1805 Moss 62°10'11.4168" 58°51'10.2096" PQ427738 PQ456774
1809 Soil 62°10'11.4168" 58°51'10.2096" PQ427739 PQ456775
Penicillium pancosmium 1878 Root 62°10'11.4168" 58°51'10.2096" PQ427742 PQ456783
1880 Soil 62°10'12.7" 58°55'35.8" PQ427717 PQ456780 PQ433532
1881 Root 62°10'12.7" 58°55'35.8" PQ427707 PQ456778 PQ433533
1882 Soil 62°10'12.7" 58°55'35.8" PQ427697 PQ456777
1883 Root 62°09'56.8980" 58°55'35.2488" PQ427689 PQ456776 PQ433534
1887 Root 62°09'56.8980" 58°55'35.2488" PQ427737 PQ456782 PQ433535
1892 Root 62°09'56.8980" 58°55'35.2488" PQ427708 PQ456779 PQ433536
1895 Soil 62°10'12.7" 58°55'35.8" PQ427743 PQ456784
1897 Root 62°09'56.8980" 58°55'35.2488" PQ427736 PQ456781 PQ433537
Penicillium rubens 1903 - - - PQ427741 PQ456785 PQ433538
Penicillium sp.1 1900 - - - PQ427696 PQ456786
Penicillium sp.2 1825 Soil 62°12'16.3656" 58°58'09.4368" PQ427735 PQ456787
Penicillium sp.3 1901 - - - PQ427773 PQ456788
Helotiales Discinellaceae Varicosporium sp. 1879 Root 62°10'11.4168" 58°51'10.2096" PQ427701 PQ427685
1885 Root 62°10'11.4168" 58°51'10.2096" PQ427763 PQ427686
Helotiaceae Cyathicula sp.1 1812 Fruit body 62°13'47.4816" 58°57'13.3560" PQ427754
1824 Moss 62°11'51.3420" 58°59'18.3408" PQ427753
1827 Fruit body 62°13'47.4816" 58°57'13.3560" PQ427732
1859 Fruit body 62°10'10.8408" 58°51'02.6460" PQ427777
Cyathicula sp.2 1822 Fruit body 62°12'12.69" 58°57'36.59" PQ427760
Cyathicula sp.3 1818 Moss 62°12'12.9708" 58°57'35.2908" PQ427713
1830 Soil 62°12'12.9708" 58°57'35.2908" PQ427734
Cyathicula sp.4 1842 Moss 62°09'26.6148" 58°55'57.0360" PQ427755
Lachnaceae Lachnum sp. 1884 Root 62°09'56.8980" 58°55'35.2488" PQ427781
1894 Root 62°10'11.4168" 58°51'10.2096" PQ427782
Ploettnerulaceae Cadophora melinii 1821 Sediment 62°11'51.3420" 58°59'18.3408" PQ427691 PQ427659 PQ433548
1870 Sediment 62°11'51.3420" 58°59'18.3408" PQ427759 PQ433549
Cadophora ramosa 1845 Styrofoam - - PQ427705 PQ427673 PQ433550
Cadophora sp.1 1810 Styrofoam - - PQ427756
Cadophora sp.2 1863 Soil 62°13'38.8308" 58°56'59.0640" PQ427690 PQ427679
Tricladiaceae Tricladium sp.1 1813 Soil 62°11'56.83" 58°59'33.12" PQ427714
Tricladium sp.1 1855 Soil 62°11'56.83" 58°59'33.12" PQ427719
Tricladium sp.2 1840 - - - PQ427670
Tricladium sp.3 1854 Soil 62°12'12.9708" 58°57'35.2908" PQ427776 PQ427675
Hypocreales Cordycipitaceae Lecanicillium sp. 1829 - - - PQ427751 PQ427663
Hypocreaceae Hypomyces albidus 1843 Fruit body 62°10'10.8408" 58°51'02.6460" PQ427770 PQ433543 PQ433539
1847 Fruit body 62°10'10.8408" 58°51'02.6460" PQ427766 PQ433544 PQ433540
Nectriaceae Cosmospora viridescens 1802 Moss 62°13'47.4816" 58°57'13.3560" PQ427764 PQ456771
Cosmospora sp. 1834 Moss 62°11'47.6700" 58°58'56.0928" PQ427768 PQ456770 PQ433542
1837 Ice 62°13'30.5256" 58°57'31.5036" PQ427767 PQ456769
1846 Moss 62°13'47.4816" 58°57'13.3560" PQ427695 PQ456766
1852 Moss 62°10'10.8408" 58°51'02.6460" PQ427726 PQ456768
1853 Moss 62°11'51.3420" 58°59'18.3408" PQ427712 PQ456767
Tilachlidiaceae Psychronectria sp. 1820 Moss 62°09'26.6148" 58°55'57.0360" PQ427700
Ophiocordycipitaceae Purpureocillium lilacinum 1902 - - - PQ427702 PQ427687
1904 - - - PQ427693 PQ427688
Tolypocladium sp. 1857 Macroalga 62°10'10.8408" 58°51'02.6460" PQ427703 PQ427676
1860 Moss 62°13'47.4816" 58°57'13.3560" PQ427728
Mortierellales Mortierellaceae Mortierella sp. 1803 Fruit body 62°13'47.4816" 58°57'13.3560" PQ427746
1875 Lagoon sediment 62°12'16.3656" 58°58'09.4368" PQ427722
1876 Styrofoam - - PQ427769 PQ427684
Onygenales Onygenaceae Chrysosporium sp. 1841 Fruit body 62°13'47.4816" 58°57'13.3560" PQ427698 PQ427671
Pleosporales Melanommataceae Herpotrichia sp.1 1808 Moss 62°13'47.4816" 58°57'13.3560" PQ427761 PQ427653 PQ433541
Herpotrichia sp.2 1816 Fruit body 62°13'47.4816" 58°57'13.3560" PQ427774 PQ427657
Phaeosphaeriaceae Phaeosphaeria sp. 1833 - - - PQ427665
Thelebolales Pseudeurotiaceae Pseudeurotium sp. 1850 Styrofoam - - PQ427745 PQ427674
1856 Moss 62°12'12.69" 58°57'36.59" PQ427706
1861 Ice 62°13'30.5256" 58°57'31.5036" PQ427771
1865 Sediment 62°12'12.69" 58°57'36.59" PQ427779
1866 Moss 62°15'34.8" 58°59'11.16" PQ427778 PQ427681
1872 Styrofoam 62°12'16.3656" 58°58'09.4368" PQ427780
1873 Sediment 62°09'38.0520" 58°55'31.8540" PQ427772
1874 Sediment 62°15'34.62" 58°59'10.56" PQ427744
Pseudogymnoascus appendiculatus 1828 Moss 62°11'51.3420" 58°59'18.3408" PQ427731 PQ427662
Pseudogymnoascus australis 1811 Moss 62°13'47.4816" 58°57'13.3560" PQ427729 PQ427654
1815 Soil 62°10'11.4168" 58°51'10.2096" PQ427727 PQ427656
Pseudogymnoascus verrucosus 1801 Sediment 62°11'53.5776" 58°59'38.1156" PQ427752 PQ427651
1807 Soil 62°12'16.3656" 58°58'09.4368" PQ427730 PQ427652
1826 Soil 62°12'12.9708" 58°57'35.2908" PQ427723 PQ427661
1832 River sediment 62°13'30.2916" 58°57'14.0508" PQ427725 PQ427664
1836 Soil 62°09'26.4996" 58°56'08.3868" PQ427758 PQ427667
1864 Green alga 62°11'53.8908" 58°58'16.4640" PQ427750 PQ427680
Pseudogymnoascus sp.1 1814 Soil 62°13'48.2520" 58°57'19.5336" PQ427711 PQ427655
1817 Soil 62°12'12.9708" 58°57'35.2908" PQ427720 PQ427658
1823 Sediment 62°11'53.5776" 58°59'38.1156" PQ427724 PQ427660
1835 River sediment 62°13'29.1360" 58°57'09.7236" PQ427733 PQ427666
1862 Sediment 62°09'38.7468" 58°55'26.8320" PQ427749 PQ427678
1867 Soil 62°12'12.9708" 58°57'35.2908" PQ427715 PQ427682
1871 River sediment 62°13'30.2916" 58°57'14.0508" PQ427718 PQ427683
Pseudogymnoascus sp.2 1858 Soil 62°12'12.9708" 58°57'35.2908" PQ427762 PQ427677
Pseudogymnoascus sp.3 1838 Moss 62°11'51.3420" 58°59'18.3408" PQ427775 PQ427668
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      Fungal diversity from Fildes Peninsula (Antarctica) and their antibiosis bioactivity against two plant pathogens
      Image Image Image Image
      Fig. 1. Sampling sites in Antarctica (ECA59 Expedition) with photographs of each sample type. (A) Map indicating the sampling sites with the location of research stations from Chile and South Korea. Representative photographs of (B) fruit body, (C) ice, (D) lichen, (E) moss, (F) sediment, and (G) soil samples.
      Fig. 2. Phylogenetic tree of 97 fungal strains isolated in this study. The phylogenetic tree was constructed using RAxML analysis with internal transcribed spacer (ITS) and LSU sequences. The final identification results for each strain are shown along with the strain numbers in bold. Bootstrap values greater than 70% are indicated at each branch node, and branches with a bootstrap value of 100 are represented by thick lines. The substrate type from which each strain was isolated is indicated next to the strain, with the corresponding type highlighted by a colored box. For clarity, the substrate types are listed at the top of each column.
      Fig. 3. Images showing the top five strains with the highest antibiosis activity against two plant pathogens. The leftmost image in each row represents the control for B. cinerea and F. culmorum. Strain numbers and identification results are indicated below each plate.
      Fig. 4. Antibiosis activity of Antarctic fungal strains against two plant pathogens. The graphs show the antibiosis activity results, ranked from highest to lowest, for (A) B. cinerea and (B) F. culmorum. The average percentage of inhibition of radial growth (PIRG) is indicated by the dashed line in each graph. Antibiosis activity is categorized into four levels, represented by distinct colors: (+++) in green, (++) in yellow, (+) in light gray, and below-average in gray.

      Fig. 1.

      Fig. 2.

      Fig. 3.

      Fig. 4.

      Fungal diversity from Fildes Peninsula (Antarctica) and their antibiosis bioactivity against two plant pathogens
      Order Family Species identification Strain NUM Substrate Latitude (S) Longitude (W) ITS LSU TUB CMD ACT TEF1 RPB2
      Agaricales Strophariaceae Pholiota baeosperma 1839 - - - PQ427716 PQ427669
      Amphisphaeriales Amphisphaeriaceae Microdochium lycopodinum 1844 Moss 62°10'11.4168" 58°51'10.2096" PQ427765 PQ427672
      Atheliales Atheliaceae Athelia arachnoidea 1831 Lichen 62°10'32.9340" 58°55'28.6860" PQ427721
      Cladosporiales Cladosporiaceae Cladosporium inversicolor 1898 Root 62°09'56.8980" 58°55'35.2488" PQ427783 PQ433547
      Cladosporium sp.1 1819 - - - PQ427699
      Cladosporium sp.2 1868 Fruit body 62°10'10.8408" 58°51'02.6460" PQ427748 PQ433531 PQ433545
      Cladosporium sp.3 1869 - - - PQ427747
      Cladosporium sp.4 1886 Root 62°09'56.8980" 58°55'35.2488" PQ427692 PQ433530 PQ433546
      Eurotiales Aspergillaceae Aspergillus sp. 1877 Root 62°09'56.8980" 58°55'35.2488" PQ427757 PQ456765
      1888 Root 62°09'56.8980" 58°55'35.2488" PQ427709
      1889 Root 62°09'56.8980" 58°55'35.2488" PQ427694 PQ456764
      1893 Root 62°09'56.8980" 58°55'35.2488" PQ427710
      Penicillium angulare 1806 Soil 62°10'11.4168" 58°51'10.2096" PQ427704 PQ456772
      Penicillium crustosum 1804 Soil 62°13'48.2520" 58°57'19.5336" PQ427740 PQ456773
      Penicillium jamesonlandense 1805 Moss 62°10'11.4168" 58°51'10.2096" PQ427738 PQ456774
      1809 Soil 62°10'11.4168" 58°51'10.2096" PQ427739 PQ456775
      Penicillium pancosmium 1878 Root 62°10'11.4168" 58°51'10.2096" PQ427742 PQ456783
      1880 Soil 62°10'12.7" 58°55'35.8" PQ427717 PQ456780 PQ433532
      1881 Root 62°10'12.7" 58°55'35.8" PQ427707 PQ456778 PQ433533
      1882 Soil 62°10'12.7" 58°55'35.8" PQ427697 PQ456777
      1883 Root 62°09'56.8980" 58°55'35.2488" PQ427689 PQ456776 PQ433534
      1887 Root 62°09'56.8980" 58°55'35.2488" PQ427737 PQ456782 PQ433535
      1892 Root 62°09'56.8980" 58°55'35.2488" PQ427708 PQ456779 PQ433536
      1895 Soil 62°10'12.7" 58°55'35.8" PQ427743 PQ456784
      1897 Root 62°09'56.8980" 58°55'35.2488" PQ427736 PQ456781 PQ433537
      Penicillium rubens 1903 - - - PQ427741 PQ456785 PQ433538
      Penicillium sp.1 1900 - - - PQ427696 PQ456786
      Penicillium sp.2 1825 Soil 62°12'16.3656" 58°58'09.4368" PQ427735 PQ456787
      Penicillium sp.3 1901 - - - PQ427773 PQ456788
      Helotiales Discinellaceae Varicosporium sp. 1879 Root 62°10'11.4168" 58°51'10.2096" PQ427701 PQ427685
      1885 Root 62°10'11.4168" 58°51'10.2096" PQ427763 PQ427686
      Helotiaceae Cyathicula sp.1 1812 Fruit body 62°13'47.4816" 58°57'13.3560" PQ427754
      1824 Moss 62°11'51.3420" 58°59'18.3408" PQ427753
      1827 Fruit body 62°13'47.4816" 58°57'13.3560" PQ427732
      1859 Fruit body 62°10'10.8408" 58°51'02.6460" PQ427777
      Cyathicula sp.2 1822 Fruit body 62°12'12.69" 58°57'36.59" PQ427760
      Cyathicula sp.3 1818 Moss 62°12'12.9708" 58°57'35.2908" PQ427713
      1830 Soil 62°12'12.9708" 58°57'35.2908" PQ427734
      Cyathicula sp.4 1842 Moss 62°09'26.6148" 58°55'57.0360" PQ427755
      Lachnaceae Lachnum sp. 1884 Root 62°09'56.8980" 58°55'35.2488" PQ427781
      1894 Root 62°10'11.4168" 58°51'10.2096" PQ427782
      Ploettnerulaceae Cadophora melinii 1821 Sediment 62°11'51.3420" 58°59'18.3408" PQ427691 PQ427659 PQ433548
      1870 Sediment 62°11'51.3420" 58°59'18.3408" PQ427759 PQ433549
      Cadophora ramosa 1845 Styrofoam - - PQ427705 PQ427673 PQ433550
      Cadophora sp.1 1810 Styrofoam - - PQ427756
      Cadophora sp.2 1863 Soil 62°13'38.8308" 58°56'59.0640" PQ427690 PQ427679
      Tricladiaceae Tricladium sp.1 1813 Soil 62°11'56.83" 58°59'33.12" PQ427714
      Tricladium sp.1 1855 Soil 62°11'56.83" 58°59'33.12" PQ427719
      Tricladium sp.2 1840 - - - PQ427670
      Tricladium sp.3 1854 Soil 62°12'12.9708" 58°57'35.2908" PQ427776 PQ427675
      Hypocreales Cordycipitaceae Lecanicillium sp. 1829 - - - PQ427751 PQ427663
      Hypocreaceae Hypomyces albidus 1843 Fruit body 62°10'10.8408" 58°51'02.6460" PQ427770 PQ433543 PQ433539
      1847 Fruit body 62°10'10.8408" 58°51'02.6460" PQ427766 PQ433544 PQ433540
      Nectriaceae Cosmospora viridescens 1802 Moss 62°13'47.4816" 58°57'13.3560" PQ427764 PQ456771
      Cosmospora sp. 1834 Moss 62°11'47.6700" 58°58'56.0928" PQ427768 PQ456770 PQ433542
      1837 Ice 62°13'30.5256" 58°57'31.5036" PQ427767 PQ456769
      1846 Moss 62°13'47.4816" 58°57'13.3560" PQ427695 PQ456766
      1852 Moss 62°10'10.8408" 58°51'02.6460" PQ427726 PQ456768
      1853 Moss 62°11'51.3420" 58°59'18.3408" PQ427712 PQ456767
      Tilachlidiaceae Psychronectria sp. 1820 Moss 62°09'26.6148" 58°55'57.0360" PQ427700
      Ophiocordycipitaceae Purpureocillium lilacinum 1902 - - - PQ427702 PQ427687
      1904 - - - PQ427693 PQ427688
      Tolypocladium sp. 1857 Macroalga 62°10'10.8408" 58°51'02.6460" PQ427703 PQ427676
      1860 Moss 62°13'47.4816" 58°57'13.3560" PQ427728
      Mortierellales Mortierellaceae Mortierella sp. 1803 Fruit body 62°13'47.4816" 58°57'13.3560" PQ427746
      1875 Lagoon sediment 62°12'16.3656" 58°58'09.4368" PQ427722
      1876 Styrofoam - - PQ427769 PQ427684
      Onygenales Onygenaceae Chrysosporium sp. 1841 Fruit body 62°13'47.4816" 58°57'13.3560" PQ427698 PQ427671
      Pleosporales Melanommataceae Herpotrichia sp.1 1808 Moss 62°13'47.4816" 58°57'13.3560" PQ427761 PQ427653 PQ433541
      Herpotrichia sp.2 1816 Fruit body 62°13'47.4816" 58°57'13.3560" PQ427774 PQ427657
      Phaeosphaeriaceae Phaeosphaeria sp. 1833 - - - PQ427665
      Thelebolales Pseudeurotiaceae Pseudeurotium sp. 1850 Styrofoam - - PQ427745 PQ427674
      1856 Moss 62°12'12.69" 58°57'36.59" PQ427706
      1861 Ice 62°13'30.5256" 58°57'31.5036" PQ427771
      1865 Sediment 62°12'12.69" 58°57'36.59" PQ427779
      1866 Moss 62°15'34.8" 58°59'11.16" PQ427778 PQ427681
      1872 Styrofoam 62°12'16.3656" 58°58'09.4368" PQ427780
      1873 Sediment 62°09'38.0520" 58°55'31.8540" PQ427772
      1874 Sediment 62°15'34.62" 58°59'10.56" PQ427744
      Pseudogymnoascus appendiculatus 1828 Moss 62°11'51.3420" 58°59'18.3408" PQ427731 PQ427662
      Pseudogymnoascus australis 1811 Moss 62°13'47.4816" 58°57'13.3560" PQ427729 PQ427654
      1815 Soil 62°10'11.4168" 58°51'10.2096" PQ427727 PQ427656
      Pseudogymnoascus verrucosus 1801 Sediment 62°11'53.5776" 58°59'38.1156" PQ427752 PQ427651
      1807 Soil 62°12'16.3656" 58°58'09.4368" PQ427730 PQ427652
      1826 Soil 62°12'12.9708" 58°57'35.2908" PQ427723 PQ427661
      1832 River sediment 62°13'30.2916" 58°57'14.0508" PQ427725 PQ427664
      1836 Soil 62°09'26.4996" 58°56'08.3868" PQ427758 PQ427667
      1864 Green alga 62°11'53.8908" 58°58'16.4640" PQ427750 PQ427680
      Pseudogymnoascus sp.1 1814 Soil 62°13'48.2520" 58°57'19.5336" PQ427711 PQ427655
      1817 Soil 62°12'12.9708" 58°57'35.2908" PQ427720 PQ427658
      1823 Sediment 62°11'53.5776" 58°59'38.1156" PQ427724 PQ427660
      1835 River sediment 62°13'29.1360" 58°57'09.7236" PQ427733 PQ427666
      1862 Sediment 62°09'38.7468" 58°55'26.8320" PQ427749 PQ427678
      1867 Soil 62°12'12.9708" 58°57'35.2908" PQ427715 PQ427682
      1871 River sediment 62°13'30.2916" 58°57'14.0508" PQ427718 PQ427683
      Pseudogymnoascus sp.2 1858 Soil 62°12'12.9708" 58°57'35.2908" PQ427762 PQ427677
      Pseudogymnoascus sp.3 1838 Moss 62°11'51.3420" 58°59'18.3408" PQ427775 PQ427668
      Table 1. Collection information and accession numbers of the 97 fungal strains isolated in this study

      Table 1.

      Journal of Microbiology : Journal of Microbiology
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