Fungi associated to pollution sources in Mandinga Lagoon, Veracruz, Mexico and their bioactive potential
DOI:
https://doi.org/10.15517/63n5k423Keywords:
aquatic fungi; , ITS sequencing; , NCI protocol; , fungal extracts; , bioactive fungi;, fungal bioprospectingAbstract
Introduction: The Mandinga Lagoon System, located in the state of Veracruz, Mexico, is under significant demographic pressure due to urban expansion around the municipalities of Boca del Río, Medellín and Alvarado. Aquatic fungi are known to respond to pollution, maintaining and adapting their life cycles to obtain their carbon source by decomposing organic matter. Objectives: To isolate and identify fungi from sampling sites associated with punctual sources of contamination and explore their antiproliferative activity against solid tumor cell lines. Methods: Two liters of water were collected in four sampling sites. The isolation of filamentous fungi was made on Potato Dextrose Agar by plate streaking method. Monosporic isolates were identified using taxonomic keys, and molecular identification was made using the primers ITS1F/ITS4. Fungal extracts were obtained from biomass in culture medium, and their antiproliferative activity was evaluated against two human solid tumor cell lines. Results: Seven fungal strains belonging to five different genera of Ascomycetes were isolated: Neopestalotiopsis, Cladosporium, Fusarium, Purpureocillium and Penicillium. Hexane and chloroform broth-extracts from Purpureocillium lavendulum showed the highest activity against A549 and HeLa cell lines (GI50 = 3 μg/ml and GI50 = 12 μg/ml, respectively). Meanwhile, the chloroform biomass-extract from Penicillium sp. and ethyl acetate broth-extract from Fusarium oxysporum showed GI50 values < 50 μg/ml. Conclusions: The ability of fungi to produce secondary metabolites as response to environmental stress represents an opportunity to perform bioprospecting studies. The results in this study indicate that P. lavendulum is a promising fungus to continue the bioguided separation of bioactive compounds with antiproliferative activity.
Downloads
References
Ameen, F., AlNadhari, S., & Al-Homaidan, A. A. (2022). Marine fungi showing multifunctional activity against human pathogenic microbes and cancer. PLoS ONE, 17(11), e0276926. https://doi.org/10.1371/journal.pone.0276926 DOI: https://doi.org/10.1371/journal.pone.0276926
Bao, Z. X., Liu, R., Li, C. Q., Pan, X. R., & Zhao, P. J. (2022). Pathogenicity and metabolites of Purpureocillium lavendulum YMF1.00683 against Meloidogyne incognita. Pathogens, 11(7), 795. https://doi.org/10.3390/pathogens11070795 DOI: https://doi.org/10.3390/pathogens11070795
Barnett, H. L., & Hunter, B. B. (1998). Illustrated genera of imperfect fungi. The American Phytopathological Society.
Benson, D. A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., & Sayers, E. W. (2013). GenBank. Nucleic Acids Research, 41(D1), D36–D42. https://doi.org/10.1093/nar/gks1195 DOI: https://doi.org/10.1093/nar/gks1195
Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: More models, new heuristics and parallel computing. Nature Methods, 9, 772–772. https://doi.org/10.1038/nmeth.2109 DOI: https://doi.org/10.1038/nmeth.2109
Edler, D., Klein, J., Antonelli, A., & Silvestro, D. (2020). raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution, 12(2), 373–377. https://doi.org/10.1111/2041-210X.13512 DOI: https://doi.org/10.1111/2041-210X.13512
Espinoza, C., Herrera-García, C. D., Espinosa-García, V., Couttolenc, A., Andrade-Torres, A., Padrón, J. M., & Trigos, A. (2021). The antiproliferative potential of fungi associated with coral and algae collected from a Veracruz Reef System, Gulf of Mexico. Latin American Journal of Aquatic Research, 49(5), 843–849. https://doi.org/10.3856/vol49-issue5-fulltext-2704 DOI: https://doi.org/10.3856/vol49-issue5-fulltext-2704
Ezeonuegbu, B. A., Abdullahi, M. D., Whong, C. M. Z., Sohunago, J. W., Kassem, H. S., Yaro, C. A., Hetta, H. F., Mostafa-Hedeab, G., Zouganelis, G. D., & Batiha, G. E. (2022). Characterization and phylogeny of fungi isolated from industrial wastewater using multiple genes. Scientific Reports, 12(1), 2094. https://doi.org/10.1038/s41598-022-05820-9 DOI: https://doi.org/10.1038/s41598-022-05820-9
Farkas, K., Walker, D. I., Adriaenssens, E. M., McDonald, J. E., Hillary, L. S., Malham, S. K., & Jones, D. L. (2020). Viral indicators for tracking domestic wastewater contamination in the aquatic environment. Water Research, 181, 115926. https://doi.org/10.1016/j.watres.2020.115926 DOI: https://doi.org/10.1016/j.watres.2020.115926
Fotedar, R., Chatting, M., Kolecka, A., Zeyara, A., Al Malki, A., Kaul, R., Bukhari, S. J., Moaiti, M. A., Febbo, E. J., Boekhout, T., & Fell, J. W. (2022). Communities of culturable yeasts and yeast-like fungi in oligotrophic hypersaline coastal waters of the Arabian Gulf surrounding Qatar. Antonie van Leeuwenhoek, 115(5), 609–633. https://doi.org/10.1007/s10482-022-01722-y DOI: https://doi.org/10.1007/s10482-022-01722-y
Gardes, M., & Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes—Application to the identification of mycorrhizae and rusts. Molecular Ecology, 2(2), 113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x DOI: https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
González-Vázquez, J. A., Hernández-Vivar, E., Rojas-Serna, C., & Valle-Morales, J. (2019). Diagnosis of water circulation in an estuary: A case study of the Jamapa River and the Mandinga lagoons, Veracruz, Mexico. Ciencias Marinas, 45(1), 1–16. https://doi.org/10.7773/cm.v45i1.2923 DOI: https://doi.org/10.7773/cm.v45i1.2923
Graça, D., Fernandes, I., Cássio, F., & Pascoal, C. (2023). Eco-physiological responses of aquatic fungi to three global change stressors highlight the importance of intraspecific trait variability. Microbial Ecology, 85(4), 1215–1225. https://doi.org/10.1007/s00248-022-02007-7 DOI: https://doi.org/10.1007/s00248-022-02007-7
Grossart, H. P., & Rojas-Jimenez, K. (2016). Aquatic fungi: Targeting the forgotten in microbial ecology. Current Opinion in Microbiology, 31, 140–145. https://doi.org/10.1016/j.mib.2016.03.016 DOI: https://doi.org/10.1016/j.mib.2016.03.016
Grossart, H. P., Van den Wyngaert, S., Kagami, M., Wurzbacher, C., Cunliffe, M., & Rojas-Jimenez, K. (2019). Fungi in aquatic ecosystems. Nature Reviews Microbiology, 17(6), 339–354. https://doi.org/10.1038/s41579-019-0175-8 DOI: https://doi.org/10.1038/s41579-019-0175-8
Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.
Hof, H., & Schrecker, J. (2024). Fusarium spp.: Infections and intoxications. GMS Infectious Diseases, 12, Doc04. https://doi.org/10.3205/id000089
Katoh, K., Rozewicki, J., & Yamada, K. D. (2019). MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20(4), 1160–1166. https://doi.org/10.1093/bib/bbx108 DOI: https://doi.org/10.1093/bib/bbx108
Katotomichelakis, M., Nikolaidis, C., Makris, M., Proimos, E., Aggelides, X., Constantinidis, T. C., Papadakis, C. E., & Danielides, V. (2016). Alternaria and Cladosporium calendar of Western Thrace: Relationship with allergic rhinitis symptoms. The Laryngoscope, 126(2), E51–E56. https://doi.org/10.1002/lary.25594 DOI: https://doi.org/10.1002/lary.25594
Kil, Y. S., Risinger, A. L., Petersen, C. L., Mooberry, S. L., & Cichewicz, R. H. (2020). Leucinostatins from Ophiocordyceps spp. and Purpureocillium spp. demonstrate selective antiproliferative effects in cells representing the luminal androgen receptor subtype of triple negative breast cancer. Journal of Natural Products, 83(6), 2010–2024. https://doi.org/10.1021/acs.jnatprod.0c00404 DOI: https://doi.org/10.1021/acs.jnatprod.0c00404
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874. https://doi.org/10.1093/molbev/msw054 DOI: https://doi.org/10.1093/molbev/msw054
Liu, D., Coloe, S., Baird, R., & Pederson, J. (2000). Rapid mini-preparation of fungal DNA for PCR. Journal of Clinical Microbiology, 38(1), 471–471. https://doi.org/10.1128/JCM.38.1.471-471.2000 DOI: https://doi.org/10.1128/JCM.38.1.471-471.2000
Liu, L., Cao, Y. R., Zhang, C. C., Fan, H. F., Guo, Z. Y., Yang, H. Y., Chen, M., Han, J. J., Xu, J., Zhang, K. Q., & Liang, L. M. (2019). An efficient gene disruption system for the nematophagous fungus Purpureocillium lavendulum. Fungal Biology, 123(4), 274–282. https://doi.org/10.1016/j.funbio.2018.10.009 DOI: https://doi.org/10.1016/j.funbio.2018.10.009
Liu, R., Bao, Z. X., Li, G. H., Li, C. Q., Wang, S. L., Pan, X. R., Zhang, K. Q., & Zhao, P. J. (2022). Identification of nematicidal metabolites from Purpureocillium lavendulum. Microorganisms, 10(7), 1343. https://doi.org/10.3390/microorganisms10071343 DOI: https://doi.org/10.3390/microorganisms10071343
Liu, R., Khan, R. A. A., Yue, Q., Jiao, Y., Yang, Y., Li, Y., & Xie, B. (2020). Discovery of a new antifungal lipopeptaibol from Purpureocillium lilacinum using MALDI-TOF-IMS. Biochemical and Biophysical Research Communications, 527(3), 689–695. https://doi.org/10.1016/j.bbrc.2020.05.021 DOI: https://doi.org/10.1016/j.bbrc.2020.05.021
Lumbreras-Martínez, H., Espinoza, C., Fernández, J. J., Norte, M., Lagunes, I., Padrón, J. M., López-Portillo, J., & Trigos, A. (2018). Bioprospecting of fungi with antiproliferative activity from the mangrove sediment of the Tampamachoco coastal lagoon, Veracruz, Mexico. Scientia Fungorum, 48, 53–60. https://doi.org/10.33885/sf.2018.48.1234 DOI: https://doi.org/10.33885/sf.2018.48.1234
Maddison, W. P., & Maddison, D. R. (2019). Mesquite: A modular system for evolutionary analysis (Version 3.61) [Computer software]. http://www.mesquiteproject.org
Magwaza, N., Nxumalo, E., Mamba, B., & Msagati, T. (2017). The occurrence and diversity of waterborne fungi in African aquatic systems: Their impact on water quality and human health. International Journal of Environmental Research and Public Health, 14(5), 546. https://doi.org/10.3390/ijerph14050546 DOI: https://doi.org/10.3390/ijerph14050546
Mohamed, G. A., & Ibrahim, S. R. M. (2021). Untapped potential of marine-associated Cladosporium species: An overview on secondary metabolites, biotechnological relevance, and biological activities. Marine Drugs, 19(11), 645. https://doi.org/10.3390/md19110645 DOI: https://doi.org/10.3390/md19110645
Monapathi, M. E., Bezuidenhout, C. C., & Rhode, O. H. J. (2017). Water quality and antifungal susceptibility of opportunistic yeast pathogens from rivers. Water Science and Technology, 75(6), 1319–1331. https://doi.org/10.2166/wst.2016.580 DOI: https://doi.org/10.2166/wst.2016.580
Monks, A., Scudiero, D., Skehan, P., Shoemaker, R., Paull, K., Vistica, D., Hose, C., Langley, J., Cronise, P., Vaigro-Wolff, A., Gray-Goodrich, M., Campbell, H., Mayo, J., Boyd, M., & Boyd, V. (1991). Feasibility of a high-flux anticancer drug screen using a diverse panel of cultured human tumor cell lines. JNCI: Journal of the National Cancer Institute, 83(11), 757–766. https://doi.org/10.1093/jnci/83.11.757 DOI: https://doi.org/10.1093/jnci/83.11.757
Murrison, L. B., Brandt, E. B., Myers, J. B., & Hershey, G. K. K. (2019). Environmental exposures and mechanisms in allergy and asthma development. Journal of Clinical Investigation, 129(4), 1504–1515. https://doi.org/10.1172/JCI124612 DOI: https://doi.org/10.1172/JCI124612
Newman, D. J., & Cragg, G. M. (2020). Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019. Journal of Natural Products, 83(3), 770–803. https://doi.org/10.1021/acs.jnatprod.9b01285 DOI: https://doi.org/10.1021/acs.jnatprod.9b01285
Niu, G., Wang, X., Gao, W., Cui, L., & Li, J. (2024). Leucinostatins from fungal extracts block malaria transmission to mosquitoes. Parasites & Vectors, 17(1), 401. https://doi.org/10.1186/s13071-024-06450-y DOI: https://doi.org/10.1186/s13071-024-06450-y
Numberger, D., Zoccarato, L., Woodhouse, J., Ganzert, L., Sauer, S., Márquez, J. R. G., Domisch, S., Grossart, H. P., & Greenwood, A. D. (2022). Urbanization promotes specific bacteria in freshwater microbiomes including potential pathogens. Science of the Total Environment, 845, 157321. https://doi.org/10.1016/j.scitotenv.2022.157321 DOI: https://doi.org/10.1016/j.scitotenv.2022.157321
Orellana, E. A., & Kasinski, A. L. (2016). Sulforhodamine B (SRB) assay in cell culture to investigate cell proliferation. Bio-Protocol, 6(21), e1984. https://doi.org/10.21769/BioProtoc.1984 DOI: https://doi.org/10.21769/BioProtoc.1984
Ortiz-Lozano, L. D., Arceo-Briseño, P., Granados-Barba, A., Salas-Monreal, D., & Jiménez-Badillo, M. de L. (2010). Capítulo 5: Zona costera. En E. I. Rivera Arriaga, I. Azuz-Adeath, L. Alpuche Gual, & G. J. Villalobos-Zapata (Eds.), Atlas del patrimonio natural, histórico y cultural de Veracruz (pp. 124–147). Gobierno del Estado de Veracruz.
Ortiz-Vera, M. P., Olchanheski, L. R., Gonçalves da Silva, E., Rezende de Lima, F., del Pilar Martinez, L. R., Sato, M. I., Jaffé, R., Alves, R., Ichiwaki, S., Padilla, G., & Luiz Araújo, W. (2018). Influence of water quality on diversity and composition of fungal communities in a tropical river. Scientific Reports, 8(1), 14799. https://doi.org/10.1038/s41598-018-33162-y DOI: https://doi.org/10.1038/s41598-018-33162-y
Patridge, E., Gareiss, P., Kinch, M. S., & Hoyer, D. (2016). An analysis of FDA-approved drugs: Natural products and their derivatives. Drug Discovery Today, 21(2), 204–207. https://doi.org/10.1016/j.drudis.2015.01.009 DOI: https://doi.org/10.1016/j.drudis.2015.01.009
Pierce, M. L., & Ward, J. E. (2019). Gut microbiomes of the Eastern oyster (Crassostrea virginica) and the blue mussel (Mytilus edulis): Temporal variation and the influence of marine aggregate-associated microbial communities. mSphere, 4(6), e00730-19. https://doi.org/10.1128/mSphere.00730-19 DOI: https://doi.org/10.1128/mSphere.00730-19
Rambaut, A. (2016). FigTree (Version 1.4.3) [Computer software]. Institute of Evolutionary Biology, University of Edinburgh. http://tree.bio.ed.ac.uk/software/figtree
Rivera Arriaga, E. I., Azuz-Adeath, I., Alpuche Gual, L., & Villalobos-Zapata, G. J. (Eds.). (2010). Cambio climático en México: Un enfoque costero y marino. Universidad Autónoma de Campeche.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. https://doi.org/10.1093/sysbio/sys029 DOI: https://doi.org/10.1093/sysbio/sys029
Salcedo-Garduño, M. G., Castañeda-Chávez, M. R., Lango-Reynoso, F., Landeros-Sánchez, C., Sosa-Villalobos, C. A., & Galaviz-Villa, I. (2019). Influence of physicochemical parameters on phytoplankton distribution in the lagoon system of Mandinga, Mexico. Revista Bio Ciencias, 6, e427. https://doi.org/10.15741/revbio.06.e427 DOI: https://doi.org/10.15741/revbio.06.e427
Sirimangkalakitti, N., Lin, J., Harada, K., Setiawan, A., Arisawa, M., & Arai, M. (2024). Chemical constituents and anticancer activities of marine-derived fungus Trichoderma lixii. Molecules, 29(9), 2048. https://doi.org/10.3390/molecules29092048 DOI: https://doi.org/10.3390/molecules29092048
van Tilburg Bernardes, E., Gutierrez, M. W., & Arrieta, M. C. (2020). The fungal microbiome and asthma. Frontiers in Cellular and Infection Microbiology, 10, 583418. https://doi.org/10.3389/fcimb.2020.583418 DOI: https://doi.org/10.3389/fcimb.2020.583418
White, T. J., Bruns, T. D., Lee, S. B., & Taylor, J. W. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. En M. A. Innis, D. H. Gelfand, J. J. Sninsky, & T. J. White (Eds.), PCR protocols: A guide to methods and applications (pp. 315–322). Academic Press. DOI: https://doi.org/10.1016/B978-0-12-372180-8.50042-1
World Health Organization. (2002). Sistemas de tratamiento de aguas residuales. Centro Panamericano de Ingeniería Sanitaria y Ciencias del Ambiente.
Zhang, Z., Schwartz, S., Wagner, L., & Miller, W. (2000). A greedy algorithm for aligning DNA sequences. Journal of Computational Biology, 7(1–2), 203–214. https://doi.org/10.1089/10665270050081478 DOI: https://doi.org/10.1089/10665270050081478
Published
Issue
Section
License
Copyright (c) 2026 Revista de Biología Tropical

This work is licensed under a Creative Commons Attribution 4.0 International License.
Creative Commons Attribution 4.0 License (CC BY 4.0)
Attribution (BY) • (BY) You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work).
