The distant siblings - A phylogenomic roadmap illuminates the origins of extant diversity in fungal aromatic polyketide biosynthesis

Genome Biology and Evolution

Volumn 7, Issue 11, 2015, Pages 3132-3154

  Koczyk, Grzegorz ^a   Dawidziuk, Adam ^a   Popiel, Delfina ^a  

^a INSTITUTE OF PLANT GENETICS   (Poland)

Author keywords

Duplication; Horizontal transfer; Loss; Polyketide; Secondary metabolism; Sources of diversity

Indexed keywords

POLYKETIDE; POLYKETIDE SYNTHASE;

ASCOMYCETES; BAYES THEOREM; BIOLOGICAL MODEL; CONSERVED SEQUENCE; ENZYMOLOGY; FUNGAL GENOME; GENE DUPLICATION; GENETICS; HORIZONTAL GENE TRANSFER; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; PROTEIN TERTIARY STRUCTURE; SPECIES DIFFERENTIATION; STATISTICAL MODEL; SYNTENY;

ASCOMYCOTA; BAYES THEOREM; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE TRANSFER, HORIZONTAL; GENETIC SPECIATION; GENOME, FUNGAL; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; PHYLOGENY; POLYKETIDE SYNTHASES; POLYKETIDES; PROTEIN STRUCTURE, TERTIARY; SYNTENY;

EID: 84957051521     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evv204     Document Type: Article

References (70)

1. Aguileta G, et al. 2008. Assessing the performance of single-copy genes for recovering robust phylogenies. Syst Biol. 57:613-627.
2. Ahuja M, et al. 2012. Illuminating the Diversity of Aromatic Polyketide Synthases in Aspergillus nidulans. J Am Chem Soc. 134:8212-8221.
3. Andersen MR, et al. 2013. Accurate prediction of secondary metabolite gene clusters in filamentous fungi. Proc Natl Acad Sci U S A. 110:E99-E107.
4. Anisimova M, et al. 2013. State-of the art methodologies dictate new standards for phylogenetic analysis. BMC Evol Biol. 13:161.
5. Atanasova L, Knox BP, Kubicek CP, Druzhinina IS, Baker SE. 2013. The polyketide synthase gene pks4 of Trichoderma reesei provides pigmentation and stress resistance. Eukaryot Cell. 12:1499-1508.
6. Bansal MS, Alm EJ, Kellis M. 2012. Efficient algorithms for the reconciliation problem with gene duplication, horizontal transfer and loss. Bioinformatics 28:i283-i291.
7. Bansal MS, Alm EJ, Kellis M. 2013. Reconciliation revisited: handling multiple optima when reconciling with duplication, transfer, and loss. J Comp Biol. 20:738-754.
8. Benson DA, et al. 2015. GenBank. Nucleic Acids Res. 43:D30-D35.
9. Bergmann S, et al. 2007. Genomics-driven discovery of PKS-NRPS hybrid metabolites from Aspergillus nidulans. Nat Chem Biol. 3:213-217.
10. Bie TD, Cristianini N, Demuth JP, Hahn MW. 2006. CAFE: a computational tool for the study of gene family evolution. Bioinformatics 22:1269-1271.
11. Blin K, et al. 2013. antiSMASH 2.0-a versatile platform for genome mining of secondary metabolite producers. Nucleic Acids Res. 41:W204-W212.
12. Boussau B, et al. 2013. Genome-scale coestimation of species and gene trees. Genome Res. 23:323-330.
13. Boussau B, Gouy M. 2006. Efficient likelihood computations with nonreversible models of evolution. Syst Biol. 55:756-768.
14. Bradshaw RE, et al. 2013. Fragmentation of an aflatoxin-like gene cluster in a forest pathogen. New Phytol. 198:525-535.
15. Brown DW, Butchko RAE, Baker SE, Proctor RH. 2012. Phylogenomic and functional domain analysis of polyketide synthases in Fusarium. Fungal Biol. 116:318-331.
16. Bushley KE, Turgeon BG. 2010. Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol. 10:26.
17. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. 2009. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972-1973.
18. Chan CX, Mahbob M, Ragan MA. 2013. Clustering evolving proteins into homologous families. BMC Bioinformatics 14:120.
19. Chang J-M, Di Tommaso P, Notredame C. 2014. TCS: a new multiple sequence alignment reliability measure to estimate alignment accuracy and improve phylogenetic tree reconstruction. Mol Biol Evol. 31:1625-1637.
20. Chiang Y-M, et al. 2011. Characterization of a polyketide synthase in Aspergillus niger whose product is a precursor for both dihydroxynaphthalene (DHN) melanin and naphtho-g-pyrone. Fungal Genet Biol. 48:430-437.
21. Cock PJA, et al. 2009. Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25:1422-1423.
22. Cox RJ. 2007. Polyketides, proteins and genes in fungi: programmed nano-machines begin to reveal their secrets. Org Biomol Chem. 5:2010-2026.
23. Darriba D, Taboada GL, Doallo R, Posada D. 2011. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164-1165.
24. Delgado JA, Al-Azzam O, Denton AM, Markell SG, Goswami RS. 2012. A resource for the in silico identification of fungal polyketide synthases from predicted fungal proteomes. Mol Plant Pathol. 13:494-507.
25. Douzery EJP, Snell EA, Bapteste E, Delsuc F, Philippe H. 2004. The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? Proc Natl Acad Sci U S A. 101:15386-15391.
26. Doyon J-P, Ranwez V, Daubin V, Berry V. 2011. Models, algorithms and programs for phylogeny reconciliation. Brief Bioinform. 12:392-400.
27. Ebersberger I, et al. 2012. A consistent phylogenetic backbone for the fungi. Mol Biol Evol. 29:1319-1334.
28. Eddy SR. 2009. A new generation of homology search tools based on probabilistic inference. Genome Inform. 23:205-211.
29. Enright AJ, Van Dongen S, Ouzounis CA. 2002. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 30:1575-1584.
30. Felsenstein J. 1989. PHYLIP-Phylogeny Inference Package (Version 3.2). Cladistics 5:164-166.
31. Finn RD, et al. 2014. Pfam: the protein families database. Nucleic Acids Res. 42:D222-D230.
32. Flicek P, et al. 2014. Ensembl 2014. Nucleic Acids Res. 42:D749-D755.
33. Foerstner KU, Doerks T, Creevey CJ, Doerks A, Bork P. 2008. A computational screen for type I polyketide synthases in metagenomics shotgun data. PLoS One e3515.
34. Frickey T, Lupas A. 2004. CLANS: a Java application for visualizing protein families based on pairwise similarity. Bioinformatics 20:3702-3704.
35. Gerke J, et al. 2012. Breaking the silence: protein stabilization uncovers silenced biosynthetic gene clusters in the fungus Aspergillus nidulans. Appl Environ Microbiol. 78:8234-8244.
36. Grigoriev IV, et al. 2012. The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res. 40:D26-D32.
37. Gueidan C, Ruibal C, de Hoog GS, Schneider H. 2011. Rock-inhabiting fungi originated during periods of dry climate in the late Devonian and middle Triassic. Fungal Biol. 115:987-996.
38. Huerta-Cepas J, Dopazo J, Gabaldón T. 2010. ETE: a python Environment for Tree Exploration. BMC Bioinformatics 11:24.
39. Husník F, Chrudimský T, Hypša V. 2011. Multiple origins of endosymbiosis within the Enterobacteriaceae (γ-Proteobacteria): convergence of complex phylogenetic approaches. BMC Biol. 9:87.
40. Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 30:772-780.
41. Khaldi N, et al. 2010. SMURF: genomic mapping of fungal secondary metabolite clusters. Fungal Genet Biol. 47:736-741.
42. Khaldi N, Wolfe KH. 2011. Evolutionary origins of the fumonisin secondary metabolite gene cluster inFusarium verticillioides and Aspergillus niger. Int J Evol Biol. 2011:423821.
43. 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 U S A. 100:15670-15675.
44. Lartillot N, Lepage T, Blanquart S. 2009. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25:2286-2288.
45. Lartillot N, Rodrigue N, Stubbs D, Richer J. 2013. PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Syst Biol. 62:611-615.
46. Li Y, Chooi Y-H, Sheng Y, Valentine JS, Tang Y. 2011. Comparative characterization of fungal anthracenone and naphthacenedione biosynthetic pathways reveals an a-hydroxylation-dependent Claisen-like cyclization catalyzed by a dimanganese thioesterase. J Am Chem Soc. 133:15773-15785.
47. Li Y, et al. 2010. Classification, prediction, and verification of the regioselectivity of fungal polyketide synthase product template domains. J Biol Chem. 285:22764-22773.
48. Marchler-Bauer A, et al. 2015. CDD: NCBI's conserved domain database. Nucleic Acids Res. 43:D222-D226.
49. Marthey S, et al. 2008. FUNYBASE: a FUNgal phYlogenomic dataBASE. BMC Bioinformatics 9:456.
50. Minh BQ, NguyenMAT, von Haeseler A. 2013. Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol. 30:1188-1195.
51. Nielsen ML, et al. 2011. A genome-wide polyketide synthase deletion library uncovers novel genetic links to polyketides and meroterpenoids in Aspergillus nidulans. FEMS Microbiol Lett. 321:157-166.
52. O'Donnell K, et al. 2013. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genet Biol. 52:20-31.
53. Ohm RA, et al. 2012. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog. 8:e1003037.
54. Price MN, Dehal PS, Arkin AP. 2010. FastTree 2-approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490.
55. Proctor RH, et al. 2013. Birth, death and horizontal transfer of the fumonisin biosynthetic gene cluster during the evolutionary diversification of Fusarium. Mol Microbiol. 90:290-306.
56. Rose PW, et al. 2013. The RCSB Protein Data Bank: new resources for research and education. Nucleic Acids Res. 41:D475-D482.
57. Rousseeuw PJ. 1987. Silhouettes: a graphical aid to the interpretation and validation of cluster analysis. J Comput Appl Math. 20:53-65.
58. Sanchez JF, Somoza AD, Keller NP, Wang CCC. 2012. Advances in Aspergillus secondary metabolite research in the post-genomic era. Nat Prod Rep. 29:351-371.
59. Schmitt I, Lumbsch HT. 2009. Ancient horizontal gene transfer from bacteria enhances biosynthetic capabilities of fungi. PLoS One 4:e4437.
60. Slot JC, Rokas A. 2011. Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr Biol. 21:134-139.
61. Spanu PD, et al. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543-1546.
62. Sung G-H, Poinar GO Jr, Spatafora JW. 2008. The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal-arthropod symbioses. Mol Phylogenet Evol. 49:495-502.
63. Szollosi GJ, Davín AA, Tannier E, Daubin V, Boussau B. 2015. Genomescale phylogenetic analysis finds extensive gene transfer among fungi. Philos Trans R Soc Lond B Biol Sci. 370(1678). pii:20140335.
64. Szollosi GJ, Rosikiewicz W, Boussau B, Tannier E, Daubin V. 2013. Efficient exploration of the space of reconciled gene trees. Syst Biol. 62:901-912.
65. Szollosi GJ, Tannier E, Lartillot N, Daubin V. 2013. Lateral gene transfer from the dead. Syst Biol. 62:386-397.
66. Talevich E, Invergo BM, Cock PJ, Chapman BA. 2012. Bio.Phylo: a unified toolkit for processing, analyzing and visualizing phylogenetic trees in Biopython. BMC Bioinformatics 13:209.
67. UniProt Consortium. 2014. Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res. 42:D191-D198.
68. Wang H, Fewer DP, Holm L, Rouhiainen L, Sivonen K. 2014. Atlas of nonribosomal peptide and polyketide biosynthetic pathways reveals common occurrence of nonmodular enzymes. Proc Natl Acad Sci U S A. 111:9259-9264.
69. Wang H, Xu Z, Gao L, Hao B. 2009. A fungal phylogeny based on 82 complete genomes using the composition vector method. BMC Evol Biol. 9:195.
70. Xu Y, et al. 2014. Insights into the biosynthesis of 12-membered resorcylic acid lactones from heterologous production in Saccharomyces cerevisiae. ACS Chem Biol. 9:1119-1127.