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Potential for the Biodegradation of Atrazine Using Leaf Litter Fungi from a Subtropical Protection Area

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Abstract

The intense use of pesticides in agricultural activities for the last several decades has caused contamination of the ecosystems connected with crop fields. Despite the well-documented occurrence of pesticide biodegradation by microbes, natural attenuation of atrazine (ATZ), and its effects on ecological processes in subtropical forested areas, such as Iguaçu National Park located in Brazil, has been poorly investigated. Subtropical environments sustain a great degree of fungal biodiversity, and the patterns and roles of these organisms should be better understood. This work aimed to evaluate nine ligninolytic-producer fungi isolated from the INP edge to degrade and detoxify ATZ solutions. ATZ degradation and the main metabolites produced, including deisopropylatrazine and deethylatrazine (DEA), were analyzed using dispersive liquid–liquid microextraction followed by gas chromatography-mass spectrometer. Four fungi were able to degrade ATZ to DEA, and the other five showed potential to grow and facilitate ATZ biodegradation. Furthermore, two strains of Fusarium spp. showed an enhanced potential for detoxification according to the Allium cepa (onion) test. Although the isolates produced ligninolytic enzymes, no ligninolytic activity was observed in the biodegradation of ATZ, a feature with ecological significance. In conclusion, Ascomycota fungi from the INP edge can degrade and detoxify ATZ in solution. Increasing the knowledge of biodiversity in subtropical protected areas, such as ecosystem services provided by microbes, enhances ecosystem conservation.

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References

  1. Maqbool Z et al (2016) Perspectives of using fungi as bioresource for bioremediation of pesticides in the environment: a critical review. Environ Sci Pollut Res 23:16904–16925

    Article  Google Scholar 

  2. Moore DR et al (2017) A weight-of-evidence approach for deriving a level of concern for atrazine that is protective of aquatic plant communities. Integr Environ Assess Manag 13(4):686–701

    Article  CAS  PubMed  Google Scholar 

  3. Hansen AM et al (2013) Atrazina: Un herbicida polémico. Rev Int Contam Ambiental 29:65–84

    Google Scholar 

  4. Sousa JCG et al (2018) A review on environmental monitoring of water organic pollutants identified by EU guidelines. J Hazard Mater 344:146–162

    Article  CAS  PubMed  Google Scholar 

  5. WHO (World Health Organization) (2018) A global overview of national regulations and standards for drinking-water quality. WHO, Geneva

  6. NORTOX 500 SC. Prescripción de agrotóxico. Atrazina (2017). http://www.nortox.com.br/wp-content/uploads/2017/05/Atrazina-Nortox-500-SC-BulaVER-04-17.08.2017.pdf. Accessed 20 May 2018

  7. Singh B, Singh K (2016) Microbial degradation of herbicides. Crit Rev Microbiol 42(2):245–261

    CAS  PubMed  Google Scholar 

  8. Hayes TB et al (2002) Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci USA 99(8):5476–5480

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hirano LQL et al (2019) Effects of egg exposure to atrazine and/or glyphosate on bone development in Podocnemis unifilis (Testudines, Podocnemididae). Ecotoxicol Environ Saf 182:109400

    Article  CAS  PubMed  Google Scholar 

  10. García-Espiñeira M, Tejeda-Benitez L, Olivero-Verbel J (2018) Toxicity of atrazine- and glyphosate-based formulations on Caenorhabditis elegans. Ecotoxicol Environ Saf 156:216–222

    Article  PubMed  CAS  Google Scholar 

  11. Andleeb S et al (2016) Influence of soil pH and temperature on atrazine bioremediation. J Northe Agric Univ 23(2):12–19

    Google Scholar 

  12. Salazar-Ledesma M et al (2018) Mobility of atrazine in soils of a wastewater irrigated maize field. Agr Ecosyst Environ 255:73–83

    Article  CAS  Google Scholar 

  13. Koskinen WC, Clay SA (1997) Factors affecting atrazine fate in North Central U.S. soils. Rev Environ Contam Toxicol 151:117–165

    CAS  PubMed  Google Scholar 

  14. Smith AE, Walker A (1989) Prediction of the persistence of the triazine herbicides atrazine, cyanazine, and metribuzin in regina heavy clay. Can J Soil Sci 69:587–595

    Article  CAS  Google Scholar 

  15. Kaufman DD, Blake J (1970) Degradation of atrazine by soil fungi. Soil Biol Biochem 2(2):73–80

    Article  CAS  Google Scholar 

  16. Singh S et al (2018) Toxicity, degradation and analysis of the herbicide atrazine. Environ Chem Lett 16:211–237

    Article  CAS  Google Scholar 

  17. Martinez B et al (2001) Complete nucleotide sequence and organization of the atrazine catabolic plasmid pADP-1 from Pseudomonas sp. strain ADP. J Bacteriol 183(19):5684–5697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ma L et al (2017) Rapid biodegradation of atrazine by Ensifer sp. strain and its degradation genes. Int Biodeterior Biodegrad 116:133–140

    Article  CAS  Google Scholar 

  19. Yang X et al (2018) Biodegradation of atrazine by the novel Citricoccus sp. strain TT3. Ecotoxicol Environ Saf 147:144–150

    Article  CAS  PubMed  Google Scholar 

  20. Deshmukh R, Khardenavis AA, Purohit HJ (2016) Diverse metabolic capacities of fungi for bioremediation. Indian J Microbiol 56(3):247–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fan X, Song F (2014) Bioremediation of atrazine: recent advances and promises. J Soils Sediments 14:1727–1737

    Article  CAS  Google Scholar 

  22. Brasil Ministério do Meio Ambiente. Snuc – Sistema Nacional de Unidades de Conservação da Natureza: Lei no. 9.985, de 18 de julho de 2000; Decreto no. 4.340, de 22 de agosto de 2002; Decreto no. 5.746, de 5 de abril de 2006. Plano Estratégico Nacional de Áreas Protegidas: Decreto no. 5.758, de 13 de abril de 2006. Brasília: MMA, 2011. 76 p.

  23. ICMBio – Instituto Chico Mendes de Conservação da Biodiversidade. Parque Nacional do Iguaçu. 2019. Accessed 06 Jun 2019. http://www.icmbio.gov.br/parnaiguacu/.

  24. Salamuni R et al (2002) Parque Nacional do Iguaçu, PR - Cataratas de fama mundial. In: Schobbenhaus C et al (edn) C. Sítios Geológicos e Paleontológicos do Brasil. 1st edn. Brasilia, DNPM/CPRM - Comissão Brasileira de Sítios Geológicos e Paleobiológicos (SIGEP), pp 313–321. http://sigep.cprm.gov.br/sitio011/sitio011.htm. Accessed 2 Jul 2018

  25. Schiesari L et al (2013) Pesticide use and biodiversity conservation in the Amazonian agricultural frontier. Philosoph Trans R Soc B Biol Sci 368:1619

    Google Scholar 

  26. Tedersoo L et al (2014) Global diversity and geography of soil fungi. Science 346:6213

    Article  CAS  Google Scholar 

  27. Blackwell M (2011) The fungi: 1, 2, 3 ... 5.1 million species? Am J Bot 98:426–438

    Article  PubMed  Google Scholar 

  28. Fiskesjo G (1985) The Allium test as a standard in environmental monitoring. Hereditas 102:99–112

    Article  CAS  PubMed  Google Scholar 

  29. Leme DM, Marin-Morales MA (2009) Allium cepa test in environmental monitoring: a review on its application. Mutat Res 682:71–81

    Article  CAS  PubMed  Google Scholar 

  30. Datta S et al (2018) (2018) Assessment of genotoxic effects of pesticide and vermicompost treated soil with Allium cepa test. Sustain Environ Res 28:171–178

    Article  CAS  Google Scholar 

  31. Bending GD, Friloux M, Walker A (2002) Degradation of contrasting pesticides by white rot fungi and its relationship with ligninolytic potential. FEMS Microbiol Lett 212(1):59–63

    Article  CAS  PubMed  Google Scholar 

  32. Pereira PM et al (2013) Optimized atrazine degradation by Pleurotus ostreatus INCQS 40310: an alternative for impact reduction of herbicides used in sugarcane crops. J Microb Biochem Technol S12:006

    Google Scholar 

  33. Della-Flora A, et al (2018) Fast, cheap and easy routine quantification method for atrazine and its transformation products in water matrixes using a DLLME-GC/MS method. Anal Methods

  34. Marinho G et al (2017) Potential of the filamentous fungus Aspergillus niger AN 400 to degrade Atrazine in wastewaters. Biocatal Agric Biotechnol 9:162–167

    Article  Google Scholar 

  35. Weber RWS, Pitt D (2000) Teaching techniques for mycology: 11. Riddell’s slide cultures. Mycologist 14(3):118–120

    Article  Google Scholar 

  36. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118

    Article  CAS  PubMed  Google Scholar 

  37. Kumar S, Stecher G, Tamura K (2016) Mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    CAS  PubMed  Google Scholar 

  39. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 16(1):11–120

    Article  Google Scholar 

  40. Australian Government, Review of Atrazine - Technical report: environmental assessment. https://apvma.gov.au/node/14356. Accessed Jan 2018.

  41. Kaufman DD, Kearney PC, Sheets TJ (1965) microbial degradation of simazine microbial. J Agric Food Chem 13(3):238–242

    Article  CAS  Google Scholar 

  42. Jeffery S, Burgess LW (1990) Growth of Fusarium graminearum Schwabe group 1 on media amended with atrazine, chlorsulfuron or glyphosate in relation to temperature and osmotic potential. Soil Biol Biochem 22(5):665–670

    Article  CAS  Google Scholar 

  43. Oliveira BR et al (2015) Biodegradation of pesticides using fungi species found in the aquatic environment. Environ Sci Pollut Res 22(15):11781–11791

    Article  CAS  Google Scholar 

  44. Silveira GL et al (2017) (2017) Chemosphere toxic effects of environmental pollutants: comparative investigation using Allium cepa L. and Lactuca sativa L. Chemosphere 178:359–367

    Article  CAS  PubMed  Google Scholar 

  45. Zablotowicz RM, Weaver MA, Locke MA (2006) Microbial adaptation for accelerated atrazine mineralization/degradation in Mississippi Delta soils. Weed Sci 54:538–547

    Article  CAS  Google Scholar 

  46. Krutz LJ, Zablotowicz RM, Reddy KN (2012) Selection pressure, cropping system, and rhizosphere proximity affect atrazine degrader populations and activity in s-triazine–adapted soil. Weed Sci 60(3):516–524

    Article  CAS  Google Scholar 

  47. Douglass JF, Radosevich M, Tuovinen OH (2017) Microbial attenuation of atrazine in agricultural soils: biometer assays, bacterial taxonomic diversity, and catabolic genes. Chemosphere 176:352–360

    Article  CAS  PubMed  Google Scholar 

  48. Brien HEO et al (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71(9):5544–5550

    Article  CAS  Google Scholar 

  49. Waalwijk C et al (1996) Discordant groupings of Fusarium spp. from sections Elegans Liseola and Dlaminia based on ribosomal ITS1 and ITS2sequences. Mycology 88(3):361–368

    Article  CAS  Google Scholar 

  50. Srivastava S, Kadooka C, Uchida JY (2018) Fusarium species as pathogen on orchids. Microbiol Res 207:188–195

    Article  PubMed  Google Scholar 

  51. Tortora GJ, Funke BR, Case CL (2005) Microbiologia, 8a edn. Porto Alegre, Artemed

    Google Scholar 

  52. Janshekar H, Fiechter A (1983) Lignin: biosynthesis, application, and biodegradation. Adv Biochem Eng Biotechnol Berl 27:119–178

    CAS  Google Scholar 

  53. Gaur N, Narasimhulu K, Pydisetty Y (2018) Recent advances in the bio-remediation of persistent organic pollutants and its effect on environment. J Clean Prod 198:1602–1631

    Article  CAS  Google Scholar 

  54. Jain R, Garg V, Yadav D (2014) In vitro comparative analysis of monocrotophos degrading potential of Aspergillus flavus,Fusarium pallidoroseum and Macrophomina sp. Biodegradation 25:437–446

    Article  CAS  PubMed  Google Scholar 

  55. Karagianni EP et al (2015) Homologues of xenobiotic metabolizing N-acetyltransferases in plant-associated fungi: novel functions for an old enzyme family. Sci Rep 5:1–14

    Article  CAS  Google Scholar 

  56. De Lima DP et al (2018) Fungal bioremediation of pollutant aromatic amines. Curr Opin Green Sustain Chem 11:34–44

    Article  Google Scholar 

  57. Cocaign A et al (2013) Biotransformation of Trichoderma spp. and their tolerance to aromatic amines, a major class of pollutants. Appl Environ Microbiol 79(47):19–26

    Google Scholar 

  58. Tan LR et al (2015) A collection of cytochrome P450 monooxygenase genes involved in modification and detoxification of herbicide atrazine in rice (Oryza sativa) plants. Ecotoxicol Environ Safety 119:25–34

    Article  CAS  Google Scholar 

  59. Xing H et al (2014) Effects of atrazine and chlorpyrifos on cytochrome P450 in common carp liver. Chemosphere 104:244–250

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We want to thank to UNILA for the facilities to develop our projects and all support of DELABEN team members while the execution of this research.

Funding

The research was supported by UNILA University and we received no specific Grant from any funding agency to carry out this work.

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Authors and Affiliations

  1. Interdisciplinary Center of Life Sciences (CICV), Institute Latin American of Nature and Life Sciences (ILACNV), Federal University of Latin American Integration (UNILA), 1000 Tarquínio Joslin dos Santos Av., Jardim Universitário, Foz do Iguaçu, PR, 85870-901, Brazil

    Samantha Beatríz Esparza-Naranjo, Gessyca Fernanda da Silva, Cleto Kaveski Peres, Marcela Boroski & Rafaella Costa Bonugli-Santos

  2. Department of Microbiology, Institute of Biomedical Science, University of São Paulo (USP), 1374 Prof. Lineu Prestes Av., Cidade Universitária, São Paulo, SP, 05508-900, Brazil

    Diana Carolina Duque-Castaño & Welington Luiz Araújo

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  1. Samantha Beatríz Esparza-Naranjo
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  3. Diana Carolina Duque-Castaño
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  4. Welington Luiz Araújo
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  7. Rafaella Costa Bonugli-Santos
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Contributions

SBE, CKP, MB and RCB planned this research. SBE and MB worked analysis of ATZ degradation and the production of principal metabolites using GC–MS. SBE and RCB worked on morphological characterization, wrote the article and designed figures. GFS made the toxicity evaluation of ATZ and fungi-treated ATZ by Allium cepa test, DCD, WLA and RCB developed isolates’ molecular characterization.

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Correspondence to Rafaella Costa Bonugli-Santos.

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Esparza-Naranjo, S.B., da Silva, G.F., Duque-Castaño, D.C. et al. Potential for the Biodegradation of Atrazine Using Leaf Litter Fungi from a Subtropical Protection Area. Curr Microbiol 78, 358–368 (2021). https://doi.org/10.1007/s00284-020-02288-6

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