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Insights into the Phylogeny or Arylamine N-Acetyltransferases in Fungi

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Abstract

Previous studies have shown that Eumycetes fungi can acylate arylamine thanks to arylamine N-acetyltransferases, xenobiotic-metabolizing enzymes also found in animals and bacteria. In this article, we present the results of mining 96 available fungal genome sequences for arylamine N-acetyltransferase genes and propose their phylogeny. The filamentous Pezizomycotina are shown to possess many putative N-acetyltransferases, whilst these are often lacking in other fungal groups. The evolution of the N-acetyltransferases is best explained by the presence of at least one gene in the opisthokont ancestor of the fungi and animal kingdoms, followed by recurrent gene losses and gene duplications. A possible horizontal gene transfer event may have occurred from bacteria to the basidiomycetous yeast Malassezia globosa.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Arvas M, Kivioja T, Mitchell A, Saloheimo M, Ussery D, Penttila M, Oliver S (2007) Comparison of protein coding gene contents of the fungal phyla Pezizomycotina and Saccharomycotina. BMC Genomics 8:325

    Article  PubMed  CAS  Google Scholar 

  • Bushley KE, Turgeon BG (2010) Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol 10:26

    Article  PubMed  CAS  Google Scholar 

  • Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–W469

    Article  PubMed  CAS  Google Scholar 

  • Durrieu G (1993) Ecologie des champignons. Masson, Paris

    Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  • Espagne E, Lespinet O, Malagnac F, Da Silva C, Jaillon O, Porcel BM, Couloux A, Aury JM, Segurens B, Poulain J, Anthouard V, Grossetete S, Khalili H, Coppin E, Dequard-Chablat M, Picard M, Contamine V, Arnaise S, Bourdais A, Berteaux-Lecellier V, Gautheret D, de Vries RP, Battaglia E, Coutinho PM, Danchin EG, Henrissat B, Khoury RE, Sainsard-Chanet A, Boivin A, Pinan-Lucarre B, Sellem CH, Debuchy R, Wincker P, Weissenbach J, Silar P (2008) The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol 9:R77

    Article  PubMed  CAS  Google Scholar 

  • Fang SH, Chung JG, Chang WC, Chang SS (1997) Evidence for arylamine N-acetyltransferase activity in the fungi Candida albicans. Toxicol Lett 92:109–116

    Article  PubMed  CAS  Google Scholar 

  • Genereux DP, Logsdon JM Jr (2003) Much ado about bacteria-to-vertebrate lateral gene transfer. Trends Genet 19:191–195

    Article  PubMed  CAS  Google Scholar 

  • Glenn AE, Bacon CW (2009) FDB2 encodes a member of the arylamine N-acetyltransferase family and is necessary for biotransformation of benzoxazolinones by Fusarium verticillioides. J Appl Microbiol 107(2):657–671

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lucking R, Thorsten Lumbsch H, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, Crous PW, Dai YC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Koljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, Mozley-Standridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schussler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A higher-level phylogenetic classification of the Fungi. Mycol Res 111:509–547

    Article  PubMed  Google Scholar 

  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O’Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schussler A, Longcore JE, O’Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lucking R, Budel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yahr R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818–822

    Article  PubMed  CAS  Google Scholar 

  • Kim D, Guengerich FP (2005) Cytochrome P450 activation of arylamines and heterocyclic amines. Annu Rev Pharmacol Toxicol 45:27–49

    Article  PubMed  CAS  Google Scholar 

  • Kroken S, Glass NL, Taylor JW, Yoder OC, Turgeon BG (2003) Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci USA 100:15670–15675

    Article  PubMed  CAS  Google Scholar 

  • Kupfer DM, Drabenstot SD, Buchanan KL, Lai H, Zhu H, Dyer DW, Roe BA, Murphy JW (2004) Introns and splicing elements of five diverse fungi. Eukaryot Cell 3:1088–1100

    Article  PubMed  Google Scholar 

  • Lamour KH, Win J, Kamoun S (2007) Oomycete genomics: new insights and future directions. FEMS Microbiol Lett 274:1–8

    Article  PubMed  CAS  Google Scholar 

  • Letunic I, Bork P (2007) Interactive Tree OF Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128

    Article  PubMed  CAS  Google Scholar 

  • Martins M, Rodrigues-Lima F, Dairou J, Lamouri A, Malagnac F, Silar P, Dupret JM (2009) An acetyltransferase conferring tolerance to toxic aromatic amine chemicals: molecular and functional studies. J Biol Chem 284:18726–18733

    Article  PubMed  CAS  Google Scholar 

  • Nielsen CB, Friedman B, Birren B, Burge CB, Galagan JE (2004) Patterns of intron gain and loss in fungi. PLoS Biol 2:e422

    Article  PubMed  CAS  Google Scholar 

  • Richards TA, Dacks JB, Jenkinson JM, Thornton CR, Talbot NJ (2006) Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Curr Biol 16:1857–1864

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues-Lima F, Dupret JM (2002) In silico sequence analysis of arylamine N-acetyltransferases: evidence for an absence of lateral gene transfer from bacteria to vertebrates and first description of paralogs in bacteria. Biochem Biophys Res Commun 293:783–792

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues-Lima F, Dairou J, Diaz CL, Rubio MC, Sim E, Spaink HP, Dupret JM (2006) Cloning, functional expression and characterization of Mesorhizobium loti arylamine N-acetyltransferases: rhizobial symbiosis supplies leguminous plants with the xenobiotic N-acetylation pathway. Mol Microbiol 60:505–512

    Article  PubMed  CAS  Google Scholar 

  • Rogozin IB, Sverdlov AV, Babenko VN, Koonin EV (2005) Analysis of evolution of exon-intron structure of eukaryotic genes. Brief Bioinform 6:118–134

    Article  PubMed  CAS  Google Scholar 

  • Schmitt I, Lumbsch HT (2009) Ancient horizontal gene transfer from bacteria enhances biosynthetic capabilities of fungi. PLoS One 4:e4437

    Article  PubMed  CAS  Google Scholar 

  • Silar P, Barreau C, Debuchy R, Kicka S, Turcq B, Sainsard-Chanet A, Sellem CH, Billault A, Cattolico L, Duprat S, Weissenbach J (2003) Characterization of the genomic organization of the region bordering the centromere of chromosome V of Podospora anserina by direct sequencing. Fungal Genet Biol 39:250–263

    Article  PubMed  CAS  Google Scholar 

  • Sim E, Sandy J, Evangelopoulos D, Fullam E, Bhakta S, Westwood I, Krylova A, Lack N, Noble M (2008) Arylamine N-acetyltransferases in mycobacteria. Curr Drug Metab 9:510–519

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tixier C, Sancelme M, Ait-Aissa S, Widehem P, Bonnemoy F, Cuer A, Truffaut N, Veschambre H (2002) Biotransformation of phenylurea herbicides by a soil bacterial strain, Arthrobacter sp. N2: structure, ecotoxicity and fate of diuron metabolite with soil fungi. Chemosphere 46:519–526

    Article  PubMed  CAS  Google Scholar 

  • Trepanier LA, Cribb AE, Spielberg SP, Ray K (1998) Deficiency of cytosolic arylamine N-acetylation in the domestic cat and wild felids caused by the presence of a single NAT1-like gene. Pharmacogenetics 8:169–179

    Article  PubMed  CAS  Google Scholar 

  • U.S. Department of Health and Human Services PHS, National Toxicology Program (2005) 11th Report on Carcinogens, Research Triangle Park, NC

  • Vagena E, Fakis G, Boukouvala S (2008) Arylamine N-acetyltransferases in prokaryotic and eukaryotic genomes: a survey of public databases. Curr Drug Metab 9:628–660

    Article  PubMed  CAS  Google Scholar 

  • Voelker D, Stetefeld N, Schirmer K, Scholz S (2008) The role of cyp1a and heme oxygenase 1 gene expression for the toxicity of 3,4-dichloroaniline in zebrafish (Danio rerio) embryos. Aquat Toxicol 86:112–120

    Article  PubMed  CAS  Google Scholar 

  • Wapinski I, Pfeffer A, Friedman N, Regev A (2007) Natural history and evolutionary principles of gene duplication in fungi. Nature 449:54–61

    Article  PubMed  CAS  Google Scholar 

  • Westwood IM, Holton SJ, Rodrigues-Lima F, Dupret JM, Bhakta S, Noble ME, Sim E (2005) Expression, purification, characterization and structure of Pseudomonas aeruginosa arylamine N-acetyltransferase. Biochem J 385:605–612

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Saunders CW, Hu P, Grant RA, Boekhout T, Kuramae EE, Kronstad JW, Deangelis YM, Reeder NL, Johnstone KR, Leland M, Fieno AM, Begley WM, Sun Y, Lacey MP, Chaudhary T, Keough T, Chu L, Sears R, Yuan B, Dawson TL Jr (2007) Dandruff-associated Malassezia genomes reveal convergent and divergent virulence traits shared with plant and human fungal pathogens. Proc Natl Acad Sci USA 104:18730–18735

    Article  PubMed  Google Scholar 

  • Zeng Q, Morales AJ, Cottarel G (2001) Fungi and humans: closer than you think. Trends Genet 17:682–684

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Roger Townsend for correcting the manuscript and three anonymous reviewers for their helpful comments.

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Correspondence to Philippe Silar.

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239_2010_9371_MOESM1_ESM.rtf

Supplementary Fig. 1 online: The alignment of fungal, animal and bacterial NAT was made with MUSCLE (Edgar 2004). Conserved amino acids are highlighted in black, similar ones in grey. The NAT motifs are underlined, and the Cys-His-Asp catalytic triad is indicated by black dots. Intron positions are indicated by the vertical red bars. Position of introns I1 and I2 of Pezizomycotina is indicated underneath the alignment. (RTF 1724 kb)

239_2010_9371_MOESM2_ESM.tif

Supplementary Fig. 2 online: Tree generated by Neighbour Joining from the alignment of Supplementary Fig. 1 online. NAT families I–VII are from Pezizomycotina. Arrow point towards the M. globosa NAT gene. (TIFF 894 kb)

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Martins, M., Dairou, J., Rodrigues-Lima, F. et al. Insights into the Phylogeny or Arylamine N-Acetyltransferases in Fungi. J Mol Evol 71, 141–152 (2010). https://doi.org/10.1007/s00239-010-9371-x

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  • DOI: https://doi.org/10.1007/s00239-010-9371-x

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