Screening of potential biosurfactant-producing yeasts isolated from the mangroves of the Paranaguá Estuarine Complex (PEC)
Abstract
Mangroves have been critical to discovering microbial diversity and for their use in biotechnological resources. The Paranaguá Estuarine Complex (PEC) is surrounded by mangroves that are exposed to anthropogenic actions resulting from industrial and seaport activities. The present study evaluated the molecular diversity of mangrove yeast isolates obtained from the PEC. Furthermore, the ability of these microorganisms to degrade oil was researched using the redox indicator 2,6-dichlorophenol indophenol (DCPIP) and dehydrogenase activity assays. Biosurfactant production was screened using the blue agar plate method, drop-collapse test, tilted glass slide test, oil spreading method, and emulsification assay. Internal Transcribed Spacer (ITS) sequencing revealed a great diversity of yeast species in the PEC, including Candida sp., C. parapsilosis, C. tropicalis, Meyerozyma carpophila, M. guilliermondii, and Debaryomyces hansenii. The isolates D. hansenii A2M1(1A), M. carpophila P2M5(74), and Candida sp. P2M3(74) tested positive for DCPIP and dehydrogenase activity. All isolates showed positive results in the blue agar plate method. The isolates M. carpophila A2M3(20), D. hansenii A2M3(15), C. tropicalis A2C5(2), C. parapsilosis A2C5, and M. carpophila P2M3(42) indicated activity in the tilted glass slide test. The isolates C. tropicalis A2C5(2), M. carpophila P2M3(42), and M. carpophila P2M5(74) showed activity in the emulsification assay. These findings provide important information about the composition of yeasts in the PEC mangrove, highlighting their potential for application in bioremediation processes of environments contaminated by petroleum.
Downloads
References
Adetunji, A. I., & Olaniran, A. O. (2021). Production and potential biotechnological applications of microbial surfactants: An overview. Saudi Journal of Biological Sciences, 28(1), 669–679.
Al-Dhabaan, F. A. (2021). Isolation and identification of crude oil-degrading yeast strains from Khafji oil field, Saud Arabia. Saudi Journal of Biological Sciences, 28(10), 5786–5792. https://doi.org/10.1016/j.sjbs.2021.06.030
Al-Hawash, A. B., Alkooranee, J. T., Abbood, H. A., Zhang, J., Sun, J., Zhang, X., & Ma, F. (2018). Isolation and characterization of two crude oil-degrading fungi strains from Rumaila oil field, Iraq. Biotechnology Reports, 17, 104–109. https://doi.org/10.1016/j.btre.2017.12.006
Barakat, K. M. (2017). Mycodegradation of crude petroleum oil by locally marine Candida tropicalis. Microbiology Research Journal International, 21(6), 1–10. https://doi.org/10.9734/MRJI/2017/37082
Bhattacharyya, A., Majumder, N. S., Basak, P., Mukherji, S., Roy, D., Nag, S., & Ghosh, A. (2015). Diversity and distribution of archaea in the mangrove sediment of sundarbans. Archaea, 2015. https://doi.org/10.1155/2015/968582
Bidoia, E. D., Montagnolli, R. N., & Lopes, P. R. M. (2010). Microbial biodegradation potential of hydrocarbons evaluated by colorimetric technique: A case study. Applied Microbiology and Biotechnology, 7, 1277–1288.
Braddock, J. F., & Catterall, P. H. (1999). A simple method for enumerating gasoline- and diesel-degrading microorganisms. Bioremediation Journal, 3(2), 81–84. https://doi.org/10.1080/10889869991219226
Castellani, A. (1963). The “water cultivation” of pathogenic fungi. Journal of Tropical Medicine and Hygiene, 66(1), 283–284.
Doyle, J. J., & Doyle, J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin, 19(1), 11–15.
Edgar, R. C. (2004). Muscle: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32(5), 1792–1797. https://doi.org/10.1093/nar/gkh340
Ferreira, A. C., & Lacerda, L. D. (2016). Degradation and conservation of Brazilian mangroves, status, and perspectives. Ocean & Coastal Management, 125, 38–46. https://doi.org/10.1016/j.ocecoaman.2016.03.011
Ganapathy, B., Yahya, A., & Ibrahim, N. (2019). Bioremediation of palm oil mill effluent (POME) using indigenous Meyerozyma guilliermondii. Environmental Science and Pollution Research, 26(11), 11113–11125. https://doi.org/10.1007/s11356-019-04334-8
Garg, M., & Chatterjee, M. (2018). Isolation, characterization and antibacterial effect of biosurfactant from Candida parapsilosis. Biotechnology Reports, 18, e00251. https://doi.org/10.1016/j.btre.2018.e00251
Gargouri, B., Mhiri, N., Karray, F., Aloui, F., & Sayadi, S. (2015). Isolation and characterization of hydrocarbon-degrading yeast strains from petroleum contaminated industrial wastewater. Biomed Research International, 2015, 929424. https://doi.org/10.1155/2015/929424
Hamilton, S. E., & Casey, D. (2016). Creation of a high spatio‐temporal resolution global database of continuous mangrove forest cover for the 21st century (CGMFC‐21). Global Ecology and Biogeography, 25(6), 729–738. https://doi.org/10.1111/geb.12449
Hanson, K., Desai, J. D., & Desai, A. J. (1993). A rapid and simple screening technique for potential crude oil-degrading microorganisms. Biotechnology Techniques, 7(10), 745–748. https://doi.org/10.1007/BF00152624
Hesham, A., Alamri, S. A., Khan, S., Mahmoud, M. E., & Mahmoud, H. M. (2009). Isolation and molecular genetic characterization of a yeast strain able to degrade petroleum polycyclic aromatic hydrocarbons. African Journal of Biotechnology, 8(10), 2218–2223. https://doi.org/10.5897/AJB09.016
Jia, S. L., Chi, Z., Liu, G. L., Hu, Z., & Chi, Z. M. (2020). Fungi in mangrove ecosystems and their potential applications. Critical Reviews in Biotechnology, 40(6), 852–864. https://doi.org/10.1080/07388551.2020.1789063
Jiang, J., Jin, M., Li, X., Meng, Q., Niu, J., & Long, X. (2020). Recent progress and trends in the analysis and identification of rhamnolipids. Applied Microbiology and Biotechnology, 104(19), 8171–8186. https://doi.org/10.1007/s00253-020-10841-3
Kaur, J., Kaur, S., Kumar, M., Krishnan, P., & Minhas, A. P. (2022). Studies on production, optimization and machine learning-based prediction of biosurfactant from Debaryomyces hansenii CBS767. International Journal of Environmental Science and Technology, 19, 8465–8478. https://doi.org/10.1007/s13762-021-03639-x
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096
Lima, S., Oliveira, A., Golin, R., Lopes, V., Caixeta, D., Lima, Z., & Morais, E. (2019). Isolation and characterization of hydrocarbon-degrading bacteria from gas station leaking-contaminated groundwater in the Southern Amazon, Brazil. Brazilian Journal of Biology, 80(2), 354–361. https://doi.org/10.1590/1519-6984.208611
Loeto, D., Jongman, M., Lekote, L., Muzila, M., Mokomane, M., Motlhanka, K., & Zhou, N. (2021). Biosurfactant production by halophilic yeasts isolated from extreme environments in Botswana. FEMS Microbiology Letters, 368(20), fnab146. https://doi.org/10.1093/femsle/fnab146
Marchand, C., St-Arnaud, M., Hogland, W., Bell, T. H., & Hijri, M. (2017). Petroleum biodegradation capacity of bacteria and fungi isolated from petroleum-contaminated soil. International Biodeterioration & Biodegradation, 116, 48–57. https://doi.org/10.1016/j.ibiod.2016.09.030
Morikawa, M., Hirata, Y., & Imanaka, T. (2000). A study on the structure–function relationship of lipopeptide biosurfactants. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 1488(3), 211–218. https://doi.org/10.1016/s1388-1981(00)00124-4
Nwaguma, I. V., Chikere, C. B., & Okpokwasili, G. C. (2019). Effect of cultural conditions on biosurfactant production by Candida sp. isolated from the sap of Elaeis guineensis. Biotechnology Journal International, 23(3), 1–14. https://doi.org/10.9734/bji/2019/v23i330079
Rog, S. M., Clarke, R. H., & Cook, C. N. (2017). More than marine: Revealing the critical importance of mangrove ecosystems for terrestrial vertebrates. Diversity and Distributions, 23(2), 221–230. https://doi.org/10.1111/ddi.12514
Romañach, S. S., De Angelis, D. L., Koh, H. L., Li, Y., Teh, S. Y., Barizan, R. S. R., & Zhai, L. (2018). Conservation and restoration of mangroves: Global status, perspectives, and prognosis. Ocean & Coastal Management, 154, 72–82. https://doi.org/10.1016/j.ocecoaman.2018.01.009
Rubio-Ribeaux, D., Silva Andrade, R. F., Silva, G. S., Holanda, R. A., Pele, M. A., Nunes, P., ... & Campos-Takaki, G. M. (2017). Promising biosurfactant produced by a new Candida tropicalis UCP 1613 strain using substrates from renewable-resources. African Journal of Microbiology Research, 11(23), 981-991. https://doi.org/10.5897/AJMR2017.8486
Santos, E. M. S, Lira, I. R. A. S., Meira, H. M., Aguiar, J. S., Rufino, R. D., Almeida, D. G., & Luna, J. M. (2021). Enhanced oil removal by a non-toxic biosurfactant formulation. Energies, 14(2), 467. https://doi.org/10.3390/en14020467
Satpute, S. K., Banpurkar, A. G., Dhakephalkar, P. K., Banat, I. M., & Chopade, B. A. (2010). Methods for investigating biosurfactants and bioemulsifiers: A review. Critical Reviews in Biotechnology, 30(2), 127–144. https://doi.org/10.3109/07388550903427280
Sharma, P., Sangwan, S., & Kaur, H. (2019). Process parameters for biosurfactant production using yeast Meyerozyma guilliermondii YK32. Environmental Monitoring and Assessment, 191(9), 1–13. https://doi.org/10.1007/s10661-019-7665-z
Siegmund, I., & Wagner, F. (1991). A new method for detecting rhamnolipids excreted by Pseudomonas species during growth on mineral agar. Biotechnology Techniques, 5(4), 265–268. https://doi.org/10.1007/BF02438660
Silva, F. S. F., Ferreira, V. C., Catter, K. M., Viana, A. P. Q., Mendonça, K. V., Sousa, O. V., & Fernandes Vieira, R. H. (2017). Produção de biossurfactantes por cepas bacterianas de origem marinha utilizando querosene como fonte de carbono. Revista de Ciências Ambientais, 11(1), 07–18. https://doi.org/10.18316/rca.v11i1.2652
Souza Queiroz, L., Rossi, S., Calvet-Mir, L., Ruiz-Mallén, I., García-Betorz, S., Salvà-Prat, J., & Andrade Meireles, A. J. (2017). Neglected ecosystem services: Highlighting the socio-cultural perception of mangroves in decision-making processes. Ecosystem Services, 26, 137–145. https://doi.org/10.1016/j.ecoser.2017.06.013
Truskewycz, A., Gundry, T. D., Khudur, L. S., Kolobaric, A., Taha, M., Aburto-Medina, A., & Shahsavari, E. (2019). Petroleum hydrocarbon contamination in terrestrial ecosystems-fate and microbial responses. Molecules, 24(18), 3400. https://doi.org/10.3390/molecules24183400
Varjani, S. J., & Upasani, V. N. (2016). Biodegradation of petroleum hydrocarbons by oleophilic strain of Pseudomonas aeruginosa NCIM5514. Bioresource Technology, 222, 195–201. https://doi.org/10.1016/j.biortech.2016.10.006
Varjani, S. J., & Upasani, V. N. (2017). Critical review on biosurfactant analysis, purification and characterization using rhamnolipid as a model biosurfactant. Bioresource Technology, 232, 389–397. https://doi.org/10.1016/j.biortech.2017.02.047
Vu, D., Groenewald, M., Szöke, S., Cardinali, G., Eberhardt, U., Stielow, B., & Robert, V. (2016). DNA barcoding analysis of more than 9 000 yeast isolates contributes to quantitative thresholds for yeast species and genera delimitation. Studies in Mycology, 85(1), 91–105. https://doi.org/10.1016/j.simyco.2016.11.007
White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols: A Guide to Methods and Applications, 18(1), 315–322.
Yang, C.-W., Lee, C.-C., Ku, H., & Chang, B.-V. (2017). Bacterial communities associated with anaerobic debromination of decabromodiphenyl ether from mangrove sediment. Environmental Science and Pollution Research, 24(6), 5391–5403. https://doi.org/10.1007/s11356-016-8259-8
Yurkov, A. M., Dlauchy, D., & Péter, G. C. (2017). Meyerozyma amylolytica sp. nov. from temperate deciduous trees and the transfer of five Candida species to the genus Meyerozyma. International Journal of Systematic and Evolutionary Microbiology, 67(10), 3977–3981. https://doi.org/10.1099/ijsem.0.002232
Zhu, Y.-G., Zhao, Y., Li, B., Huang, C.-L., Zhang, S.-Y., Yu, S., & Su, J.-Q. (2017). Continental-scale pollution of estuaries with antibiotic resistance genes. Nature Microbiology, 2(4), 16270. https://doi.org/10.1038/nmicrobiol.2016.270
Copyright (c) 2025 Matheus Sampaio Araujo, Caroline Alves Cordeiro, Danyelle Stringari, Josiane Aparecida Gomes-Figueiredo (Autor)
This work is licensed under a Creative Commons Attribution 4.0 International License.
DECLARATION OF ORIGINALITY AND COPYRIGHTS
I Declare that current article is original and has not been submitted for publication, in part or in whole, to any other national or international journal.
The copyrights belong exclusively to the authors. Published content is licensed under Creative Commons Attribution 4.0 (CC BY 4.0) guidelines, which allows sharing (copy and distribution of the material in any medium or format) and adaptation (remix, transform, and build upon the material) for any purpose, even commercially, under the terms of attribution.
Read this link for further information on how to use CC BY 4.0 properly.
1.png)
3.png){kind=logo}
