N-acetylation of toxic aromatic amines by fungi: Strain screening, cytotoxicity and genotoxicity evaluation, and application in bioremediation of 3,4-dichloroaniline.

Aromatic amines (AA) are one of the most commonly used classes of compounds in industry and the most common pollutants found in both soil and water. 3,4-Dichloaniline (3,4-DCA) is a persistent residue of the phenylurea herbicide in the environment. In this study, we used a colorimetric method as a new approach to screen 12 filamentous fungal strains of the genera Aspergillus, Chaetomium, Cladosporium, and Mucor to assess their capacity to perform AA N-acetylation since it is considered a potential tool in environmental bioremediation. Subsequently, the selected strains were biotransformed with different AA substrates to evaluate the product yield. The strains Aspergillus niveus 43, Aspergillus terreus 31, and Cladosporium cladosporioides showed higher efficiencies in the biotransformation of 3,4-DCA at 500 µM into its N-acetylated product. These fungal strains also showed great potential to reduce the phytotoxicity of 3,4-DCA in experiments using Lactuca sativa seeds. Furthermore, N-acetylation was shown to be effective in reducing the cytotoxic and genotoxic effects of 3,4-DCA and other AA in the immortalized human keratinocyte (HaCaT) cell line. The isolated products after biotransformation showed that fungi of the genera Aspergillus and Cladosporium appeared to have N-acetylation as the first and main AA detoxification mechanism. Finally, A. terreus 31 showed the highest 3,4-DCA bioremediation potential, and future research can be carried out on the application of this strain to form microbial consortia with great potential for the elimination of toxic AA from the environment.

[1]  R. Naidu,et al.  Ecological risk assessment for perfluorohexanesulfonic acid (PFHxS) in soil using species sensitivity distribution (SSD) approach. , 2022, Journal of hazardous materials.

[2]  P. Bhatt,et al.  Characterization of a novel glyphosate-degrading bacterial species, Chryseobacterium sp. Y16C, and evaluation of its effects on microbial communities in glyphosate-contaminated soil. , 2022, Journal of hazardous materials.

[3]  U. Vijayalakshmi,et al.  Fungal Diversity and Its Role in Mycoremediation , 2022, Geomicrobiology Journal.

[4]  L. Alba,et al.  Enhanced Biodegradation of Phenylurea Herbicides by Ochrobactrum anthrophi CD3 Assessment of Its Feasibility in Diuron-Contaminated Soils , 2022, International journal of environmental research and public health.

[5]  N. Oanh,et al.  Composition of bacterial community and isolation of bacteria responsible for diuron degradation in sediment and soil under anaerobic condition , 2021, Archives of Microbiology.

[6]  P. Bhatt,et al.  Novel pathway of acephate degradation by the microbial consortium ZQ01 and its potential for environmental bioremediation. , 2021, Journal of hazardous materials.

[7]  R. Ruller,et al.  New derivatives of the iridoid specioside from fungal biotransformation , 2021, Applied Microbiology and Biotechnology.

[8]  P. Bhatt,et al.  Emerging Strategies for the Bioremediation of the Phenylurea Herbicide Diuron , 2021, Frontiers in Microbiology.

[9]  T. Felföldi,et al.  Comparative Investigation of 15 Xenobiotic-Metabolizing N-Acetyltransferase (NAT) Homologs from Bacteria , 2021, Applied and environmental microbiology.

[10]  Ajar Nath Yadav,et al.  Myco-remediation: A mechanistic understanding of contaminants alleviation from natural environment and future prospect. , 2021, Chemosphere.

[11]  M. Kulp,et al.  Bioremediation of lindane contaminated soil: Exploring the potential of actinobacterial strains. , 2021, Chemosphere.

[12]  N. Oanh,et al.  Anaerobic Degradation of Propanil in Soil and Sediment Using Mixed Bacterial Culture , 2021, Current Microbiology.

[13]  K. Wakabayashi,et al.  o-Anisidine Dimer, 2-Methoxy-N4-(2-methoxyphenyl) Benzene-1,4-diamine, in Rat Urine Associated with Urinary bladder Carcinogenesis. , 2021, Chemical research in toxicology.

[14]  D. B. Silva,et al.  Plant–Microbe Interactions for Bioremediation of Pesticides , 2021 .

[15]  Kyungho Choi,et al.  Effects of 3,4-dichloroaniline (3,4-DCA) and 4,4'-methylenedianiline (4,4'-MDA) on sex hormone regulation and reproduction of adult zebrafish (Danio rerio). , 2020, Chemosphere.

[16]  K. Vähäkangas,et al.  Toxicity of diuron metabolites in human cells. , 2020, Environmental toxicology and pharmacology.

[17]  N. Akhtar,et al.  Mycoremediation: Expunging environmental pollutants , 2020, Biotechnology reports.

[18]  Yongzhen Peng,et al.  Simultaneous methanethiol and dimethyl sulfide removal in a single-stage biotrickling filter packed with polyurethane foam: Performance, parameters and microbial community analysis. , 2019, Chemosphere.

[19]  SOME AROMATIC AMINES AND RELATED COMPOUNDS VOLUME 127 IARC MONOGRAPHS ON THE IDENTIFICATION OF CARCINOGENIC HAZARDS TO HUMANS , 2019 .

[20]  A. C. D. Monreal,et al.  New Bis copper complex ((Z) ‐4 ‐ ((4‐chlorophenyl) amino) ‐4‐oxobut‐2‐enoyl) oxy): Cytotoxicity in 4T1 cells and their toxicogenic potential in Swiss mice , 2018, Toxicology and applied pharmacology.

[21]  D. D. de Lima,et al.  Fungal bioremediation of pollutant aromatic amines , 2018, Current Opinion in Green and Sustainable Chemistry.

[22]  Svetoslav H. Slavov,et al.  Computational identification of structural factors affecting the mutagenic potential of aromatic amines: study design and experimental validation , 2018, Archives of Toxicology.

[23]  J. M. Sáez,et al.  Comparative study of single and mixed cultures of actinobacteria for the bioremediation of co-contaminated matrices , 2018 .

[24]  Andrea Luca Tasca,et al.  State of the art of the environmental behaviour and removal techniques of the endocrine disruptor 3,4-dichloroaniline , 2018, Journal of environmental science and health. Part A, Toxic/hazardous substances & environmental engineering.

[25]  E. A. de Almeida,et al.  Diuron metabolites act as endocrine disruptors and alter aggressive behavior in Nile 2 tilapia ( Oreochromis niloticus ) 3 4 , 2017 .

[26]  R. Bischoff,et al.  Physicochemical Parameters Affecting the Electrospray Ionization Efficiency of Amino Acids after Acylation , 2017, Analytical chemistry.

[27]  N. Nardi,et al.  Vitamin D: Correlation with biochemical and body composition changes in a southern Brazilian population and induction of cytotoxicity in mesenchymal stem cells derived from human adipose tissue. , 2017, Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie.

[28]  Richard S Judson,et al.  Retrospective mining of toxicology data to discover multispecies and chemical class effects: Anemia as a case study , 2017, Regulatory toxicology and pharmacology : RTP.

[29]  A. Beatriz,et al.  N-Acetylation of Aromatic Amines by the Soil Fungus Aspergillus japonicus (UFMS 48.136) , 2017 .

[30]  E. Gomes,et al.  Evaluation of Diuron Tolerance and Biotransformation by Fungi from a Sugar Cane Plantation Sandy-Loam Soil. , 2016, Journal of agricultural and food chemistry.

[31]  P. Tiwari,et al.  Plant secondary metabolism linked glycosyltransferases: An update on expanding knowledge and scopes. , 2016, Biotechnology advances.

[32]  R. Hung,et al.  Applications of Aspergillus in Plant Growth Promotion , 2016 .

[33]  J. Dairou,et al.  Screen for soil fungi highly resistant to dichloroaniline uncovers mostly Fusarium species. , 2015, Fungal genetics and biology : FG & B.

[34]  In-Jung Lee,et al.  Endophytic fungi promote plant growth and mitigate the adverse effects of stem rot: an example of Penicillium citrinum and Aspergillus terreus , 2015 .

[35]  R. Nogales,et al.  Biodegradation of 3,4 dichloroaniline by fungal isolated from the preconditioning phase of winery wastes subjected to vermicomposting. , 2014, Journal of hazardous materials.

[36]  S. Pfuhler,et al.  N-acetylation of three aromatic amine hair dye precursor molecules eliminates their genotoxic potential. , 2014, Mutagenesis.

[37]  Samuel M. Cohen,et al.  Diuron metabolites and urothelial cytotoxicity: in vivo, in vitro and molecular approaches. , 2013, Toxicology.

[38]  A. Lamouri,et al.  Biotransformation of Trichoderma spp. and Their Tolerance to Aromatic Amines, a Major Class of Pollutants , 2013, Applied and Environmental Microbiology.

[39]  Miguel Roehrs,et al.  Biodegradation of Herbicide Propanil and Its Subproduct 3,4-Dichloroaniline in Water , 2012 .

[40]  C. Mougin,et al.  Pesticide-Derived Aromatic Amines and Their Biotransformation , 2011 .

[41]  A. Lamouri,et al.  An Acetyltransferase Conferring Tolerance to Toxic Aromatic Amine Chemicals , 2009, The Journal of Biological Chemistry.

[42]  L. R. Ribeiro,et al.  Protective effect of beta-glucan extracted from Saccharomyces cerevisiae, against DNA damage and cytotoxicity in wild-type (k1) and repair-deficient (xrs5) CHO cells. , 2007, Toxicology in vitro : an international journal published in association with BIBRA.

[43]  H. Spaink,et al.  Cloning, functional expression and characterization of Mesorhizobium loti arylamine N‐acetyltransferases: rhizobial symbiosis supplies leguminous plants with the xenobiotic N‐acetylation pathway , 2006, Molecular microbiology.

[44]  A. Soares,et al.  Acute effects of 3,4-dichloroaniline on biomarkers and spleen histology of the common goby Pomatoschistus microps. , 2006, Chemosphere.

[45]  N. Cochet,et al.  Environmental impact of diuron transformation: a review. , 2004, Chemosphere.

[46]  F. Pompeo,et al.  An approach to identifying novel substrates of bacterial arylamine N-acetyltransferases. , 2003, Bioorganic & medicinal chemistry.

[47]  G. Rankin,et al.  Characterization of 2-amino-4,5-dichlorophenol (2A45CP) in vitro toxicity in renal cortical slices from male Fischer 344 rats. , 2002, Toxicology.

[48]  D. Boucher,et al.  Effets sur le spermatozoïde humain du Diuron (3-(3,4-dichlorophényl)-1,1-diméthyl-urée) et de l’un de ses produits de transformation, la 3,4-dichloroaniline (3,4-DCA) (Etude préliminaire) , 2001 .

[49]  A. Carvalho,et al.  Acute effects of 3,4-dichloroaniline on blood of male Wistar rats. , 1998, Chemosphere.

[50]  M. Noble,et al.  Purification, characterization, and crystallization of an N-hydroxyarylamine O-acetyltransferase from Salmonella typhimurium. , 1998, Protein expression and purification.

[51]  P. Joseph-Nathan,et al.  Sensitivity of the H/D isotope shifts of the 13C nuclear shielding to the nitrogen lone pair delocalization in anilines and acetanilides , 1991 .

[52]  T. Mosmann Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. , 1983, Journal of immunological methods.