Morpho-Molecular and Genomic Characterization of Penicillium mexicanum Isolates Retrieved from a Forsaken Gold Mine
Source abstract
Abstract
During the ongoing studies designed to examine the fungal diversity present within the abandoned and flooded Escádia Grande gold mine (Góis, Portugal), we repeatedly isolated several specimens belonging to a Penicillium species. Molecular phylogenetic analysis, coupled with morphological observations, positioned this fungus within subgen. Penicillium sect. Paradoxa, series Atramentosa, pinpointing its identity as Penicillium mexicanum (the first record for mining soils and the country). Given the limited research conducted on Penicillia isolated from similar environments, the species genome was sequenced utilizing the Oxford Nanopore® MinION™ methodology and studied through bioinformatic analysis. The obtained genome has a size of 29.62 Mb, containing a 47.72% GC content, 10,156 genes, with 44 rRNAs and 178 tRNAs/tmRNAs, providing the first genomic resource for this microorganism. Bioinformatic analysis allowed us to identify multiple genomic traits that can contribute towards this species survival in these extreme environments, including the presence of high levels of major facilitator transporters (MFS), Zn (2)-C6 fungal-type DNA-binding domains, P-loop containing nucleoside triphosphate hydrolases, specific fungal transcription factors and sugar transporters. Furthermore, putative advantageous metabolic traits, such as methylotrophy, assimilatory nitrate and sulfate reduction abilities, were also detected. In addition, the results also highlighted a strong genomic and metabolic organization and investment towards arsenic detoxification (transport and oxidation). Lastly, thirty-two putative biosynthetic gene clusters were predicted, including some with high similarity values to monascorubrin, nidulanin A, histidyltryptophanyldiketopiperazine/dehydrohistidyltryptophanyldiketopiperazine/roquefortine D/roquefortine C/glandicoline A/glandicoline B/meleagrine, YWA1 and choline. Overall, this study expands the current Penicillia knowledge from mining environments while also enhancing our understanding regarding fungal arsenic resistance.
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Research context
OpenAlex topics: Plant Pathogens and Fungal Diseases · Fungal Biology and Applications · Microbial Natural Products and Biosynthesis
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
Centre for Functional Ecology (CFE)—Science for People & the Planet, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal
TERRA—Associate Laboratory for Sustainable Land Use and Ecosystem Services, Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal
FitoLab—Laboratory for Phytopathology, Instituto Pedro Nunes (IPN), Rua Pedro Nunes, 3030-199 Coimbra, Portugal
Funding
FCT—Fundação para a Ciência e Tecnologia, I.P. · PRR—Recovery and Resilience Plan—and the NextGeneration EU European Funds · Centre for Functional Ecology—Science for People and the Planet (CFE) · Ministério da Ciência, Tecnologia e Ensino Superior (MCTES)
References (90)
Show source-provided references
1. Hazard Assessment on Arsenic and Lead in Soils of Castromil Gold Mining Area, Portugal10.1016/j.apgeochem.2003.10.010 ↗
2. A Critical Review of the Effects of Gold Cyanide-Bearing Tailings Solutions on Wildlife10.1016/j.envint.2007.04.007 ↗
3. Ngole-Jeme, V.M., and Fantke, P. (2017). Ecological and Human Health Risks Associated with Abandoned Gold Mine Tailings Contaminated Soil. PLoS ONE, 12.10.1371/journal.pone.0172517 ↗
4. Crognale, S., D’Annibale, A., Pesciaroli, L., Stazi, S.R., and Petruccioli, M. (2017). Fungal Community Structure and As-Resistant Fungi in a Decommissioned Gold Mine Site. Front. Microbiol., 8.10.3389/fmicb.2017.02202 ↗
5. The Amazing Potential of Fungi: 50 Ways We Can Exploit Fungi Industrially10.1007/s13225-019-00430-9 ↗
6. Fungal Taxonomy and Sequence-Based Nomenclature10.1038/s41564-021-00888-x ↗
7. Corbu, V.M., Gheorghe-Barbu, I., Dumbravă, A.Ș., Vrâncianu, C.O., and Șesan, T.E. (2023). Current Insights in Fungal Importance—A Comprehensive Review. Microorganisms, 11.10.3390/microorganisms11061384 ↗
8. The Contribution of Fungi to the Global Economy10.1007/s13225-023-00520-9 ↗
9. Classification of Aspergillus, Penicillium, Talaromyces and Related Genera (Eurotiales): An Overview of Families, Genera, Subgenera, Sections, Series and Species10.1016/j.simyco.2020.05.002 ↗
10. What Are the 100 Most Cited Fungal Genera?
11. A Review of Recently Introduced Aspergillus, Penicillium, Talaromyces and Other Eurotiales Species10.3114/sim.2024.107.01 ↗
12. Heavy Metal Tolerance of Fungi10.1016/S0892-6875(01)00037-1 ↗
13. Gupta, V.K., and Rodriguez-Couto, S. (2018). Role of Penicillium Species in Bioremediation Processes. New and Future Developments in Microbial Biotechnology and Bioengineering, Elsevier.
14. Biosynthesis of Gold Nanoparticles by Penicillium rubens and Catalytic Detoxification of Ochratoxin A and Organic Dye Pollutants10.1007/s10123-023-00341-5 ↗
15. Coelho, E., Reis, T.A., Cotrim, M., Rizzutto, M., and Corrêa, B. (2020). Bioremediation of Water Contaminated with Uranium Using Penicillium piscarium. Biotechnol. Prog., 36.10.1002/btpr.3032 ↗
16. Isolation, Characterization, and Metal Response of Novel, Acid-Tolerant Penicillium spp. from Extremely Metal-Rich Waters at a Mining Site in Transbaikal (Siberia, Russia)10.1007/s00248-018-1186-0 ↗
17. Sánchez-Castellón, J., Urango-Cárdenas, I., Enamorado-Montes, G., Burgos-Nuñez, S., Marrugo-Negrete, J., and Díez, S. (2022). Removal of Mercury, Cadmium, and Lead Ions by Penicillium sp.. Front. Environ. Chem., 2.10.3389/fenvc.2021.795632 ↗
18. Intracellular Biosynthesis of Gold Nanoparticles by the Fungus Penicillium chrysogenum
19. Extracellular Biosynthesis and Characterization of Gold Nanoparticles Using the Fungus Penicillium chrysogenum10.1007/s00542-015-2666-5 ↗
20. Trovão, J., Soares, F., Paiva, D.S., Pratas, J., and Portugal, A. (2024). A Snapshot of the Microbiome of a Portuguese Abandoned Gold Mining Area. Appl. Sci., 14.10.3390/app14010226 ↗
21. Fungal Diversity and Distribution across Distinct Biodeterioration Phenomena in Limestone Walls of the Old Cathedral of Coimbra, UNESCO World Heritage Site10.1016/j.ibiod.2019.05.008 ↗
22. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics
23. ITS Primers with Enhanced Specificity for Basidiomycetes—Application to the Identification of Mycorrhizae and Rusts10.1111/j.1365-294X.1993.tb00005.x ↗
24. Phylogenetic Relationships among Ascomycetes: Evidence from an RNA Polymerse II Subunit10.1093/oxfordjournals.molbev.a026092 ↗
25. Novel Neosartorya Species Isolated from Soil in Korea10.1099/ijs.0.63980-0 ↗
26. Development of Primer Sets Designed for Use with the PCR to Amplify Conserved Genes from Filamentous Ascomycetes10.1128/aem.61.4.1323-1330.1995 ↗
27. Trovão, J., Soares, F., Tiago, I., and Portugal, A. (2021). Talaromyces Saxoxalicus sp. Nov., Isolated from the Limestone Walls of the Old Cathedral of Coimbra, Portugal. Int. J. Syst. Evol. Microbiol., 71.10.1099/ijsem.0.005175 ↗
28. Gapped BLAST and PSI-BLAST: A New Generation of Protein Database Search Programs10.1093/nar/25.17.3389 ↗
29. New and Interesting Species of Penicillium (Eurotiomycetes, Aspergillaceae) in Freshwater Sediments from Spain10.3897/mycokeys.86.73861 ↗
30. Penicillium mexicanum: An Unrecorded Fungal Species Isolated from Air Samples Collected in Korea
31. MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability10.1093/molbev/mst010 ↗
32. UGENE team Unipro UGENE: A Unified Bioinformatics Toolkit10.1093/bioinformatics/bts091 ↗
33. SeaView Version 4: A Multiplatform Graphical User Interface for Sequence Alignment and Phylogenetic Tree Building10.1093/molbev/msp259 ↗
34. ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates10.1038/nmeth.4285 ↗
35. W-IQ-TREE: A Fast Online Phylogenetic Tool for Maximum Likelihood Analysis10.1093/nar/gkw256 ↗
36. New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.010.1093/sysbio/syq010 ↗
37. Survey of Branch Support Methods Demonstrates Accuracy, Power, and Robustness of Fast Likelihood-Based Approximation Schemes10.1093/sysbio/syr041 ↗
38. The Galaxy Platform for Accessible, Reproducible and Collaborative Biomedical Analyses: 2020 Update10.1093/nar/gkaa434 ↗
39. NanoPack: Visualizing and Processing Long-Read Sequencing Data10.1093/bioinformatics/bty149 ↗
40. Assembly of Long, Error-Prone Reads Using Repeat Graphs10.1038/s41587-019-0072-8 ↗
41. QUAST: Quality Assessment Tool for Genome Assemblies10.1093/bioinformatics/btt086 ↗
42. BUSCO: Assessing Genome Assembly and Annotation Completeness with Single-Copy Orthologs10.1093/bioinformatics/btv351 ↗
43. OrthoDB V10: Sampling the Diversity of Animal, Plant, Fungal, Protist, Bacterial and Viral Genomes for Evolutionary and Functional Annotations of Orthologs10.1093/nar/gky1053 ↗
44. Seemann, T. (2024, October 08). Barrnap 0.7: Rapid Ribosomal RNA Prediction. Available online: https://github.com/tseemann/barrnap.
45. ARAGORN, a Program to Detect tRNA Genes and tmRNA Genes in Nucleotide Sequences10.1093/nar/gkh152 ↗
46. RepeatModeler2 for Automated Genomic Discovery of Transposable Element Families10.1073/pnas.1921046117 ↗
47. Smit, A., Hubley, R., and Green, P. (2024, October 08). RepeatMasker Open-4.0. (2013–2015). Available online: http://www.repeatmasker.org.
48. eggNOG-Mapper v2: Functional Annotation, Orthology Assignments, and Domain Prediction at the Metagenomic Scale10.1093/molbev/msab293 ↗
49. InterProScan 5: Genome-Scale Protein Function Classification10.1093/bioinformatics/btu031 ↗
50. The InterPro Protein Families and Domains Database: 20 Years On10.1093/nar/gkaa977 ↗
51. Blast2GO: A Universal Tool for Annotation, Visualization and Analysis in Functional Genomics Research10.1093/bioinformatics/bti610 ↗
52. High-Throughput Functional Annotation and Data Mining with the Blast2GO Suite10.1093/nar/gkn176 ↗
53. dbCAN3: Automated Carbohydrate-Active Enzyme and Substrate Annotation10.1093/nar/gkad328 ↗
54. antiSMASH 7.0: New and Improved Predictions for Detection, Regulation, Chemical Structures and Visualisation10.1093/nar/gkad344 ↗
55. BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences10.1016/j.jmb.2015.11.006 ↗
56. Song, X., Li, Y., Stirling, E., Zhao, K., Wang, B., Zhu, Y., Luo, Y., Xu, J., and Ma, B. (2022). AsgeneDB: A Curated Orthology Arsenic Metabolism Gene Database and Computational Tool for Metagenome Annotation. NAR Genom. Bioinform., 4.10.1093/nargab/lqac080 ↗
57. Fast and Sensitive Protein Alignment Using DIAMOND10.1038/nmeth.3176 ↗
58. Tang, D., Chen, M., Huang, X., Zhang, G., Zeng, L., Zhang, G., Wu, S., and Wang, Y. (2023). SRplot: A Free Online Platform for Data Visualization and Graphing. PLoS ONE, 18.10.1371/journal.pone.0294236 ↗
59. Aspergillus, Penicillium and Talaromyces Isolated from House Dust Samples Collected Around the World10.1016/j.simyco.2014.07.002 ↗
60. Park, M.S., Oh, S.-Y., Fong, J.J., Houbraken, J., and Lim, Y.W. (2019). The Diversity and Ecological Roles of Penicillium in Intertidal Zones. Sci. Rep., 9.10.1038/s41598-019-49966-5 ↗
61. Looking for the Undiscovered Asexual Taxa: Case Studies from Lesser Studied Life Modes and Habitats10.5943/mycosphere/12/1/17 ↗
62. Fungi Are Key Players in Extreme Ecosystems10.1016/j.tree.2022.02.002 ↗
63. Comparative Genomic Study of the Penicillium Genus Elucidates a Diverse Pangenome and 15 Lateral Gene Transfer Events10.1186/s43008-023-00108-7 ↗
64. IMA Genome-F1810.1186/s43008-023-00121-w ↗
65. Roxo, I., Amaral, A., Portugal, A., and Trovão, J. (2024). Draft Genome Sequence and Comparative Genomic Analysis of Penicillium pancosmium MUM 23.27 Isolated from Raw Honey. Arch. Microbiol., 206.10.1007/s00203-023-03766-8 ↗
66. Peculiar Genomic Traits in the Stress-Adapted Cryptoendolithic Antarctic Fungus Friedmanniomyces endolithicus10.1016/j.funbio.2020.01.005 ↗
67. Paiva, D.S., Fernandes, L., Portugal, A., and Trovão, J. (2024). First Genome Sequence of the Microcolonial Black Fungus Saxispiralis lemnorum MUM 23.14: Insights into the Unique Genomic Traits of the Aeminiaceae Family. Microorganisms, 12.10.3390/microorganisms12010104 ↗
68. Major Facilitator Superfamily10.1128/MMBR.62.1.1-34.1998 ↗
69. The Role of Nucleoside Triphosphate Hydrolase Metallochaperones in Making Metalloenzymes10.1093/mtomcs/mfac030 ↗
70. Zhang, S., Shi, G., Xu, X., Guo, X., Li, S., Li, Z., Wu, Q., and Yin, W.-B. (2024). Global Analysis of Natural Products Biosynthetic Diversity Encoded in Fungal Genomes. J. Fungi, 10.10.3390/jof10090653 ↗
71. Morales-Oyervides, L., Ruiz-Sánchez, J.P., Oliveira, J.C., Sousa-Gallagher, M.J., Méndez-Zavala, A., Giuffrida, D., Dufossé, L., and Montañez, J. (2020). Biotechnological Approaches for the Production of Natural Colorants by Talaromyces/Penicillium: A Review. Biotechnol. Adv., 43.10.1016/j.biotechadv.2020.107601 ↗
72. Afroz Toma, M., Rahman, M.H., Rahman, M.S., Arif, M., Nazir, K.H.M.N.H., and Dufossé, L. (2023). Fungal Pigments: Carotenoids, Riboflavin, and Polyketides with Diverse Applications. J. Fungi, 9.10.3390/jof9040454 ↗
73. Bignell, E., Cairns, T.C., Throckmorton, K., Nierman, W.C., and Keller, N.P. (2016). Secondary Metabolite Arsenal of an Opportunistic Pathogenic Fungus. Philos. Trans. R. Soc. Lond. B Biol. Sci., 371.10.1098/rstb.2016.0023 ↗
74. Novel Key Metabolites Reveal Further Branching of the Roquefortine/Meleagrin Biosynthetic Pathway10.1074/jbc.M113.512665 ↗
75. Banani, H., Marcet-Houben, M., Ballester, A.-R., Abbruscato, P., González-Candelas, L., Gabaldón, T., and Spadaro, D. (2016). Genome Sequencing and Secondary Metabolism of the Postharvest Pathogen Penicillium griseofulvum. BMC Genom., 17.10.1186/s12864-015-2347-x ↗
76. Garello, M., Piombo, E., Buonsenso, F., Prencipe, S., Valente, S., Meloni, G.R., Marcet-Houben, M., Gabaldón, T., and Spadaro, D. (2024). Several Secondary Metabolite Gene Clusters in the Genomes of Ten Penicillium spp. Raise the Risk of Multiple Mycotoxin Occurrence in Chestnuts. Food Microbiol., 122.10.1016/j.fm.2024.104532 ↗
77. Hydrolytic Polyketide Shortening by Ayg1p, a Novel Enzyme Involved in Fungal Melanin Biosynthesis10.1074/jbc.M406758200 ↗
78. Pohl, C., Polli, F., Schütze, T., Viggiano, A., Mózsik, L., Jung, S., de Vries, M., Bovenberg, R.A.L., Meyer, V., and Driessen, A.J.M. (2020). A Penicillium rubens Platform Strain for Secondary Metabolite Production. Sci. Rep., 10.10.1038/s41598-020-64893-6 ↗
79. Synthesis of the Fungal Metabolite YWA1 and Related Constructs as Tools to Study MelLec-Mediated Immune Response to Aspergillus Infections10.1021/acs.joc.0c02324 ↗
80. Choline Derivatives Involved in Osmotolerance of Penicillium fellutanum10.1128/AEM.64.1.273-278.1998 ↗
81. Choline: Its Role in the Growth of Filamentous Fungi and the Regulation of Mycelial Morphology10.1111/j.1574-6968.1993.tb05872.x ↗
82. Microbial Melanins for Radioprotection and Bioremediation10.1111/1751-7915.12807 ↗
83. Gostinčar, C., Muggia, L., and Grube, M. (2012). Polyextremotolerant Black Fungi: Oligotrophism, Adaptive Potential, and a Link to Lichen Symbioses. Front. Microbiol., 3.10.3389/fmicb.2012.00390 ↗
84. Morawe, M., Hoeke, H., Wissenbach, D.K., Lentendu, G., Wubet, T., Kröber, E., and Kolb, S. (2017). Acidotolerant Bacteria and Fungi as a Sink of Methanol-Derived Carbon in a Deciduous Forest Soil. Front. Microbiol., 8.10.3389/fmicb.2017.01361 ↗
85. A Novel Sulfidogenic Process via Sulfur Reduction to Remove Arsenate in Acid Mine Drainage: Insights into the Performance and Microbial Mechanisms10.1016/j.watres.2024.121423 ↗
86. Iron and Siderophores in Fungal-Host Interactions10.1016/j.mycres.2007.11.012 ↗
87. Xie, B., Wei, X., Wan, C., Zhao, W., Song, R., Xin, S., and Song, K. (2024). Exploring the Biological Pathways of Siderophores and Their Multidisciplinary Applications: A Comprehensive Review. Molecules, 29.10.3390/molecules29102318 ↗
88. Biosorption: Current Perspectives on Concept, Definition and Application10.1016/j.biortech.2013.12.102 ↗
89. Geomycology: Biogeochemical Transformations of Rocks, Minerals, Metals and Radionuclides by Fungi, Bioweathering and Bioremediation10.1016/j.mycres.2006.12.001 ↗
90. Metals, Minerals and Microbes: Geomicrobiology and Bioremediation10.1099/mic.0.037143-0 ↗