Pyrene degradation by marine-derived ascomycete: process optimization, toxicity, and metabolic analyses

Abstract

Marine-derived fungi are relevant genetic resources for bioremediation of saline environments/processes. Among the five fungi recovered from marine sponges able to degrade pyrene (Py) and benzo[a]pyrene (BaP), Tolypocladium sp. strain CBMAI 1346 and Xylaria sp. CBMAI 1464 presented the best removal rates of Py and BaP, respectively. Since the decrease in BaP was related to mycelial adsorption, a combined strategy was applied for the investigation of Py degradation by the fungus Tolypocladium sp. CBMAI 1346. The selected fungus was able to degrade about 95% of Py after 7 days of incubation (optimized conditions), generating metabolites different from the ones found before optimization. Metabolites and transcriptomic data revealed that the degradation occurred mainly by the cytochrome P450 pathway. Putative monooxygenases and dioxygenases found in the transcriptome may play an important role. After 21 days of degradation, no toxicity was found in the optimized culture conditions. The findings from the present study highlight the potential of marine-derived fungi to degrade environmental pollutants and convey innovative information related to the metabolism of pyrene.

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References

  1. Abbondanzi F, Campisi T, Focanti M, Guerra R, Iacondini A (2005) Assessing degradation capability of aerobic indigenous microflora in PAH-contaminated brackish sediments. Mar Environ Res 59:419–434. https://doi.org/10.1016/j.marenvres.2004.06.006

    Article  CAS  Google Scholar 

  2. Alexander FJ, King CK, Reichelt-Brushett AJ, Harrison PL (2017) Fuel oil and dispersant toxicity to the Antarctic sea urchin (Sterechinus neumayeri). Environ Toxicol Chem 36:1563–1571. https://doi.org/10.1002/etc.3679

    Article  CAS  Google Scholar 

  3. Anastasi A, Coppola T, Prigione V, Varese GC (2009) Pyrene degradation and detoxification in soil by a consortium of basidiomycetes isolated from compost: role of laccases and peroxidases. J Hazard Mater 165:1229–1233. https://doi.org/10.1016/j.jhazmat.2008.10.032

    Article  CAS  Google Scholar 

  4. Argumedo-Delira R, Alarcón A, Ferrera-Cerrato R, Almaraz JJ, Peña-Cabriales JJ (2012) Tolerance and growth of 11 Trichoderma strains to crude oil, naphthalene, phenanthrene and benzo[a]pyrene. J Environ Manag 95:S291–S299. https://doi.org/10.1016/j.jenvman.2010.08.011

    Article  CAS  Google Scholar 

  5. Arora DS, Gill PK (2001) Comparison of two assay procedures for lignin peroxidase. Enzym Microb Technol 28:602–605. https://doi.org/10.1016/S0141-0229(01)00302-7

    Article  CAS  Google Scholar 

  6. Arulazhagan P, Al-Shekri K, HudaQ GJJ, Basahi MM, Jeyakumar D (2017) Biodegradation of polycyclic aromatic hydrocarbons by an acidophilic Stenotrophomonas maltophilia strain AJH1 isolated from a mineral mining site in Saudi Arabia. Extremophiles 21:163–174. https://doi.org/10.1007/s00792-016-0892-0

    Article  CAS  Google Scholar 

  7. Bhadury P, Bik H, Lambshead JD, Austen MC, Smerdon GR, Rogers AD (2011) Molecular diversity of fungal phylotypes co-amplified alongside nematodes from coastal and deep-sea marine environments. PLoS One 6:1–8. https://doi.org/10.1371/journal.pone.0026445

    Article  CAS  Google Scholar 

  8. Birolli WG, de Santos AD, Alvarenga N et al (2017) Biodegradation of anthracene and several PAHs by the marine-derived fungus Cladosporium sp. CBMAI 1237. Mar Pollut Bull 129:525–533. https://doi.org/10.1016/j.marpolbul.2017.10.023

    Article  CAS  Google Scholar 

  9. Bonugli-Santos RC, Vieira GAL, Collins C, Fernandes TCC, Marin-Morales MA, Murray P, Sette LD (2016) Enhanced textile dye decolorization by marine-derived basidiomycete Peniophora sp. CBMAI 1063 using integrated statistical design. Environ Sci Pollut Res 23:8659–8668. https://doi.org/10.1007/s11356-016-6053-2

    Article  CAS  Google Scholar 

  10. Bugni TS, Ireland CM (2004) Marine-derived fungi: a chemically and biologically diverse group of microorganisms. Nat Prod Rep 21:143–163. https://doi.org/10.1039/B301926H

    Article  CAS  Google Scholar 

  11. Cerniglia CE (1984) Microbial metabolism of polycyclic aromatic hydrocarbons. Adv Appl Microbiol 30:31–71. https://doi.org/10.1016/S0065-2164(08)70052-2

    Article  CAS  Google Scholar 

  12. Cerniglia CE (1997) Fungal metabolism of polycyclic aromatic hydrocarbons: past, present and future applications in bioremediation. J Ind Microbiol Biotechnol 19:324–333. https://doi.org/10.1038/sj.jim.2900459

    Article  CAS  Google Scholar 

  13. Cerniglia CE, Sutherland JB (2001) Bioremediation of polycyclic aromatic hydrocarbons by ligninolytic and non-ligninolytic fungi. In: Gadd G (ed) Fungi in bioremediation. Cambridge University Press, Cambridge, p 481

    Google Scholar 

  14. Darma UZ, Aziz NAA, Zulkefli SZ, Mustafa M (2016) Identification of phenanthrene and pyrene degrading bacteria from used engine oil contaminated soil. Int J Sci Eng Res 7:680–686

    Google Scholar 

  15. Fouillaud M, Venkatachalam M, Llorente M, Magalon H, Cuet P, Dufossé L (2017) Biodiversity of pigmented fungi isolated from marine environment in La Réunion Island, Indian Ocean: new resources for colored metabolites. J Fungi 3:36. https://doi.org/10.3390/jof3030036

    Article  CAS  Google Scholar 

  16. Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435. https://doi.org/10.1093/nar/gkn176

    Article  CAS  Google Scholar 

  17. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J, Couger MB, Eccles D, Li B, Lieber M, MacManes MD, Ott M, Orvis J, Pochet N, Strozzi F, Weeks N, Westerman R, William T, Dewey CN, Henschel R, LeDuc RD, Friedman N, Regev A (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512. https://doi.org/10.1038/nprot.2013.084

    Article  CAS  Google Scholar 

  18. Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15. https://doi.org/10.1016/j.jhazmat.2009.03.137

    Article  CAS  Google Scholar 

  19. Johnson AR, Wick LY, Harms H (2005) Principles of microbial PAH degradation in soil. Environ Pollut 133:71–84. https://doi.org/10.1016/j.envpol.2004.04.015

    Article  CAS  Google Scholar 

  20. Jones EBG, Suetrong S, Sakayaroj J, Bahkali AH, Abdel-Wahab MA, Boekhout T, Pang KL (2015) Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Divers 73:1–72. https://doi.org/10.1007/s13225-015-0339-4

    Article  Google Scholar 

  21. Juhasz AL, Naidu R (2000) Bioremediation of high molecular weight polycyclic aromatic hydrocarbons: a review of the microbial degradation of benzo[a]pyrene. Int Biodeterior Biodegrad 45:57–88. https://doi.org/10.1016/S0964-8305(00)00052-4

    Article  CAS  Google Scholar 

  22. Kadri T, Rouissi T, Kaur Brar S, Cledon M, Sarma S, Verma M (2017) Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by fungal enzymes: a review. J Environ Sci (China) 51:52–74. https://doi.org/10.1016/j.jes.2016.08.023

    Article  Google Scholar 

  23. Kazunga C, Aitken MD (2000) Products from the incomplete metabolism of pyrene by polycyclic aromatic hydrocarbon-degrading bacteria. Appl Environ Microbiol 66:1917–1922

    Article  CAS  Google Scholar 

  24. Kester DR, Duedall IW, Connors DN, Pytkowicz RM (1967) Preparation of artificial seawater. Limnol Oceanogr 12:176–179

    Article  CAS  Google Scholar 

  25. Kuwahara M, Glenn JK, Morgan MA, Gold MH (1984) Separation and characterization of two extracelluar H2O2-dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Lett 169:247–250. https://doi.org/10.1016/0014-5793(84)80327-0

    Article  CAS  Google Scholar 

  26. Lily MK, Bahuguna A, Dangwal K, Garg V (2009) Degradation of benzo [a] pyrene by a novel strain Bacillus subtilis BMT4I (MTCC 9447). Braz J Microbiol 40:884–892. https://doi.org/10.1590/S1517-838220090004000020

    Article  CAS  Google Scholar 

  27. Luan TG, Yu KSH, Zhong Y, Zhou HW, Lan CY, Tam NFY (2006) Study of metabolites from the degradation of polycyclic aromatic hydrocarbons (PAHs) by bacterial consortium enriched from mangrove sediments. Chemosphere 65:2289–2296. https://doi.org/10.1016/j.chemosphere.2006.05.013

    Article  CAS  Google Scholar 

  28. Luo S, Chen B, Lin L, Wang X, Tam NF, Luan T (2014) Pyrene degradation accelerated by constructed consortium of bacterium and microalga: effects of degradation products on the microalgal growth. Environ Sci Technol 48:13917–13924. https://doi.org/10.1021/es503761j

    Article  CAS  Google Scholar 

  29. Menezes CBA, Bonugli-Santos RC, Miqueletto PB, Passarini MRZ, Silva CHD, Justo MR, Leal RR, Fantinatti-Garboggini F, Oliveira VM, Berlinck RGS, Sette LD (2010) Microbial diversity associated with algae, ascidians and sponges from the north coast of São Paulo state, Brazil. Microbiol Res 165:466–482. https://doi.org/10.1016/j.micres.2009.09.005

    Article  Google Scholar 

  30. Otero IVR, Ferro M, Bacci M, Ferreira H, Sette LD (2017) De novo transcriptome assembly: a new laccase multigene family from the marine-derived basidiomycete Peniophora sp. CBMAI 1063. AMB Express 7:11. https://doi.org/10.1186/s13568-017-0526-7

    Article  CAS  Google Scholar 

  31. Passarini MRZ, Rodrigues MVN, da Silva M, Sette LD (2011a) Marine-derived filamentous fungi and their potential application for polycyclic aromatic hydrocarbon bioremediation. Mar Pollut Bull 62:364–370. https://doi.org/10.1016/j.marpolbul.2010.10.003

    Article  CAS  Google Scholar 

  32. Passarini MRZ, Sette LD, Rodrigues MVN (2011b) Improved extraction method to evaluate the degradation of selected PAHs by marine fungi grown in fermentative medium. J Braz Chem Soc 22:564–570. https://doi.org/10.1590/S0103-50532011000300022

    Article  CAS  Google Scholar 

  33. Passarini MRZ, Santos C, Lima N, Berlinck RGS, Sette LD (2013) Filamentous fungi from the Atlantic marine sponge Dragmacidon reticulatum. Arch Microbiol 195:99–111. https://doi.org/10.1007/s00203-012-0854-6

    Article  CAS  Google Scholar 

  34. Pozdnyakova N (2012) Involvement of the ligninolytic system of white rot and litter-decomposing fungi in the degradation of polycyclic aromatic hydrocarbons. Review article. Biotechnol Res Int 2012:243217. https://doi.org/10.1155/2012/243217

    Article  CAS  Google Scholar 

  35. Selvin J, Ninawe AS, Seghal Kiran G, Lipton AP (2010) Sponge-microbial interactions: ecological implications and bioprospecting avenues. Crit Rev Microbiol 36:82–90. https://doi.org/10.3109/10408410903397340

    Article  CAS  Google Scholar 

  36. Seo JS, Keum YS, Li QX (2009) Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 2009(6):278–309. https://doi.org/10.3390/ijerph6010278

    Article  CAS  Google Scholar 

  37. Smith MR (1990) The biodegradation of aromatic hydrocarbons by bacteria. Biodegradation 1:191–206. https://doi.org/10.1007/bf00058836

    Article  CAS  Google Scholar 

  38. Souza HML, Taniguchi S, Bícego MC, Oliveira LA, Oliveira TCS, Barroso HS, Zanotto SP (2015) Polycyclic aromatic hydrocarbons in superficial sediments of the Negro River in the Amazon region of Brazil. J Braz Chem Soc 26:1438–1449. https://doi.org/10.5935/0103-5053.20150112

    CAS  Article  Google Scholar 

  39. Szklarz GD, Antibus RK, Sinsabaugh RL, Linkins AE (1989) Production of phenol oxidases and peroxidases by wood-rotting fungi. Mycologia 81:234. https://doi.org/10.2307/3759705

    Article  CAS  Google Scholar 

  40. Ukiwe LN, Egereonu UU, Njoku PC, Nwoko CIA, Allinor JI (2013) Polycyclic aromatic hydrocarbons degradation techniques: a review. Int J Chem 5:43–55. https://doi.org/10.5539/ijc.v5n4p43

    Article  CAS  Google Scholar 

  41. Vieira GAL, Magrini MJ, Bonugli-Santos RC, Rodrigues MVN, Sette LD (2018) Polycyclic aromatic hydrocarbons degradation by marine-derived basidiomycetes: optimization of the degradation process. Brazilian J Microbiol 49:1–8. https://doi.org/10.1016/j.bjm.2018.04.007

    Article  CAS  Google Scholar 

  42. Vite-Vallejo O, Palomares LA, Dantán-González E, Ayala-Castro HG, Martínez-Anaya C, Valderrama B, Folch-Mallol J (2009) The role of N-glycosylation on the enzymatic activity of a Pycnoporus sanguineus laccase. Enzym Microb Technol 45:233–239. https://doi.org/10.1016/j.enzmictec.2009.05.007

    Article  CAS  Google Scholar 

  43. Wang G (2006) Diversity and biotechnological potential of the sponge-associated microbial consortia. J Ind Microbiol Biotechnol 33:545–551. https://doi.org/10.1007/s10295-006-0123-2

    Article  CAS  Google Scholar 

  44. Wang C, Sun H, Li J, Li Y, Zhang Q (2009) Enzyme activities during degradation of polycyclic aromatic hydrocarbons by white rot fungus Phanerochaete chrysosporium in soils. Chemosphere 77:733–738. https://doi.org/10.1016/j.chemosphere.2009.08.028

    Article  CAS  Google Scholar 

  45. Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y (2012) DbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40:445–451. https://doi.org/10.1093/nar/gks479

    Article  CAS  Google Scholar 

  46. Zdobnov EM, Apweiler R (2001) InterProScan—an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17:847–848. https://doi.org/10.1093/bioinformatics/17.9.847

    Article  CAS  Google Scholar 

  47. Zhong Y, Luan T, Lin L, Liu H, Tam NFY (2011) Production of metabolites in the biodegradation of phenanthrene, fluoranthene and pyrene by the mixed culture of Mycobacterium sp. and Sphingomonas sp. Bioresour Technol 102:2965–2972. https://doi.org/10.1016/j.biortech.2010.09.113

    Article  CAS  Google Scholar 

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Acknowledgments

MRSV thanks the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (no. 2011/18769-3) and Coordenação de Aperfeiçoamento Pessoal de Nível Superior (CAPES) for her scholarships. GALV thanks the FAPESP (no. 2018/03372-0) for her technical grant. IVRO thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (no. 170714/2017-9) for his scholarship. LDS thanks the CNPq for her Productivity Fellowship (303145/2016-1). The authors would like to thank Lucas Miotelo for the assistance with the article images.

Funding

This study was financed by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (grant nos. 2013/19486-0 and 2016/07957-7).

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Correspondence to Lara D. Sette.

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Vasconcelos, M.R.S., Vieira, G.A.L., Otero, I.V.R. et al. Pyrene degradation by marine-derived ascomycete: process optimization, toxicity, and metabolic analyses. Environ Sci Pollut Res 26, 12412–12424 (2019). https://doi.org/10.1007/s11356-019-04518-2

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Keywords

  • PAH degradation
  • Artemia
  • Experimental design
  • Marine biotechnology
  • Transcriptome