Extensive Intra-Kingdom Horizontal Gene Transfer Converging on a Fungal Fructose Transporter Gene

PLoS Genetics

Volumn 9, Issue 6, 2013, Pages

  Coelho, Marco A ^a   Gonçalves, Carla ^a   Sampaio, José Paulo ^a   Gonçalves, Paula ^a  

^a UNIVERSIDADE NOVA DE LISBOA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; FRUCTOSE; FRUCTOSE TRANSPORTER; RNA POLYMERASE; UNCLASSIFIED DRUG;

ARTICLE; ASCOMYCETES; ASPERGILLUS; BIOCHEMISTRY; BIOGENESIS; EVOLUTIONARY ADAPTATION; FSY1 GENE; FUNGAL GENOME; FUNGAL STRAIN; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENE LOCUS; GENETIC CODE; GENETIC ORGANIZATION; HETEROLOGOUS EXPRESSION; HORIZONTAL GENE TRANSFER; NONHUMAN; PEZIZOMYCOTINA; PHYLOGENY; SACCHAROMYCES;

ASCOMYCOTA; DATABASES, GENETIC; EVOLUTION, MOLECULAR; FUNGAL PROTEINS; GENE TRANSFER, HORIZONTAL; GENOME, FUNGAL; MEMBRANE TRANSPORT PROTEINS; PHYLOGENY; SEQUENCE HOMOLOGY, AMINO ACID;

ASCOMYCOTA; FUNGI; PROKARYOTA;

EID: 84879649208     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003587     Document Type: Article

References (97)

1. Mira A, Martin-Cuadrado AB, D'Auria G, Rodriguez-Valera F, (2010) The bacterial pan-genome:a new paradigm in microbiology. Int Microbiol 13: 45-57.
2. Koonin EV, (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39: 309-338.
3. Puigbo P, Wolf YI, Koonin EV, (2010) The tree and net components of prokaryote evolution. Genome Biol Evol 2: 745-756.
4. Andersson JO, (2009) Horizontal gene transfer between microbial eukaryotes. Methods Mol Biol 532: 473-487.
5. Doolittle WF, (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14: 307-311.
6. Gordon JL, Byrne KP, Wolfe KH, (2009) Additions, losses, and rearrangements on the evolutionary route from a reconstructed ancestor to the modern Saccharomyces cerevisiae genome. PLoS Genet 5: e1000485.
7. Brown CA, Murray AW, Verstrepen KJ, (2010) Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr Biol 20: 895-903.
8. Cliften P, Sudarsanam P, Desikan A, Fulton L, Fulton B, et al. (2003) Finding functional features in Saccharomyces genomes by phylogenetic footprinting. Science 301: 71-76.
9. Kellis M, Patterson N, Endrizzi M, Birren B, Lander ES, (2003) Sequencing and comparison of yeast species to identify genes and regulatory elements. Nature 423: 241-254.
10. Marcet-Houben M, Gabaldon T, (2010) Acquisition of prokaryotic genes by fungal genomes. Trends Genet 26: 5-8.
11. Syvanen M, (2012) Evolutionary implications of horizontal gene transfer. Annu Rev Genet 46: 341-358.
12. Slot JC, Rokas A, (2010) Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi. Proc Natl Acad Sci U S A 107: 10136-10141.
13. Slot JC, Rokas A, (2011) Horizontal transfer of a large and highly toxic secondary metabolic gene cluster between fungi. Curr Biol 21: 134-139.
14. Novo M, Bigey F, Beyne E, Galeote V, Gavory F, et al. (2009) Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc Natl Acad Sci U S A 106: 16333-16338.
15. Gibbons JG, Rokas A, (2012) The function and evolution of the Aspergillus genome. Trends Microbiol 21 (1): 14-22.
16. Slot JC, Hibbett DS, (2007) Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: a phylogenetic study. PLoS One 2: e1097.
17. Khaldi N, Collemare J, Lebrun MH, Wolfe KH, (2008) Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol 9: R18.
18. Khaldi N, Wolfe KH, (2011) Evolutionary origins of the fumonisin secondary metabolite gene cluster in Fusarium verticillioides and Aspergillus niger. Int J Evol Biol 2011: 423821.
19. McDonald TR, Dietrich FS, Lutzoni F, (2012) Multiple horizontal gene transfers of ammonium transporters/ammonia permeases from prokaryotes to eukaryotes: toward a new functional and evolutionary classification. Mol Biol Evol 29: 51-60.
20. Richards TA, Leonard G, Soanes DM, Talbot NJ, (2011) Gene transfer into the fungi. Fungal Biology Reviews 25: 98-110.
21. Hellborg L, Woolfit M, Arthursson-Hellborg M, Piskur J, (2008) Complex evolution of the DAL5 transporter family. BMC Genomics 9: 164.
22. Lin Z, Li WH, (2011) Expansion of hexose transporter genes was associated with the evolution of aerobic fermentation in yeasts. Mol Biol Evol 28: 131-142.
23. Powell AJ, Conant GC, Brown DE, Carbone I, Dean RA, (2008) Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens. BMC Genomics 9: 147.
24. Chow EW, Morrow CA, Djordjevic JT, Wood IA, Fraser JA, (2012) Microevolution of Cryptococcus neoformans driven by massive tandem gene amplification. Mol Biol Evol 29: 1987-2000.
25. Montanini B, Viscomi AR, Bolchi A, Martin Y, Siverio JM, et al. (2006) Functional properties and differential mode of regulation of the nitrate transporter from a plant symbiotic ascomycete. Biochem J 394: 125-134.
26. Schüssler A, Martin H, Cohen D, Fitz M, Wipf D, (2006) Characterization of a carbohydrate transporter from symbiotic glomeromycotan fungi. Nature 444: 933-936.
27. Saier MH Jr, Yen MR, Noto K, Tamang DG, Elkan C, (2009) The Transporter Classification Database: recent advances. Nucleic Acids Res 37: D274-278.
28. Gonçalves P, Rodrigues de Sousa H, Spencer-Martins I, (2000) FSY1, a novel gene encoding a specific fructose/H+ symporter in the type strain of Saccharomyces carlsbergensis. J Bacteriol 182: 5628-5630.
29. Libkind D, Hittinger CT, Valério E, Gonçalves C, Dover J, et al. (2011) Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast. Proc Natl Acad Sci U S A 108: 14539-14544.
30. Leandro MJ, Fonseca C, Gonçalves P, (2009) Hexose and pentose transport in ascomycetous yeasts: an overview. FEMS Yeast Res 9: 511-525.
31. Anjos J, de Sousa HR, Roca C, Cassio F, Luttik M, et al. (2012) Fsy1, the sole hexose-proton transporter characterized in Saccharomyces yeasts, exhibits a variable fructose:H+ stoichiometry. Biochim Biophys Acta 1828: 201-207.
32. Rodrigues de Sousa H, Spencer-Martins I, Gonçalves P, (2004) Differential regulation by glucose and fructose of a gene encoding a specific fructose/H+ symporter in Saccharomyces sensu stricto yeasts. Yeast 21: 519-530.
33. Diezemann A, Boles E, (2003) Functional characterization of the Frt1 sugar transporter and of fructose uptake in Kluyveromyces lactis. Curr Genet 43: 281-288.
34. Doehlemann G, Molitor F, Hahn M, (2005) Molecular and functional characterization of a fructose specific transporter from the gray mold fungus Botrytis cinerea. Fungal Genet Biol 42: 601-610.
35. Galeote V, Novo M, Salema-Oom M, Brion C, Valério E, et al. (2010) FSY1, a horizontally transferred gene in the Saccharomyces cerevisiae EC1118 wine yeast strain, encodes a high-affinity fructose/H+ symporter. Microbiology 156: 3754-3761.
36. Santos J, Sousa MJ, Cardoso H, Inácio J, Silva S, et al. (2008) Ethanol tolerance of sugar transport, and the rectification of stuck wine fermentations. Microbiology 154: 422-430.
37. Parrent JL, James TY, Vasaitis R, Taylor AF, (2009) Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses. BMC Evol Biol 9: 148.
38. Fitzpatrick DA, Logue ME, Stajich JE, Butler G, (2006) A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol 6: 99.
39. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, et al. (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443: 818-822.
40. 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.
41. Kurtzman CP (2011) Discussion of teleomorphic and anamorphic ascomycetous yeasts and yeast-like taxa. In: Kurtzman CP, Fell JW, Boekhout T, editors. The Yeasts, a Taxonomic Study. 5th ed. New York: Elsevier. pp. 293-307.
42. Desjardins CA, Champion MD, Holder JW, Muszewska A, Goldberg J, et al. (2011) Comparative genomic analysis of human fungal pathogens causing paracoccidioidomycosis. PLoS Genet 7: e1002345.
43. Leonard G, Richards TA, (2012) Genome-scale comparative analysis of gene fusions, gene fissions, and the fungal tree of life. Proc Natl Acad Sci U S A 109: 21402-21407.
44. Butler G, Rasmussen MD, Lin MF, Santos MA, Sakthikumar S, et al. (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459: 657-662.
45. Santos MA, Gomes AC, Santos MC, Carreto LC, Moura GR, (2011) The genetic code of the fungal CTG clade. C R Biol 334: 607-611.
46. Sugita T, Nakase T, (1999) Non-universal usage of the leucine CUG codon and the molecular phylogeny of the genus Candida. Syst Appl Microbiol 22: 79-86.
47. Kellis M, Birren BW, Lander ES, (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617-624.
48. Louis VL, Despons L, Friedrich A, Martin T, Durrens P, et al. (2012) Pichia sorbitophila, an Interspecies Yeast Hybrid, Reveals Early Steps of Genome Resolution After Polyploidization. G3 (Bethesda) 2: 299-311.
49. Cason DT, Spencer-Martins I, van Uden N, (1986) Transport of fructose by a proton symport in a brewing yeast. FEMS Microbiology Letters 36: 307-309.
50. Wieczorke R, Krampe S, Weierstall T, Freidel K, Hollenberg CP, et al. (1999) Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae. FEBS Lett 464: 123-128.
51. Sharpton TJ, Stajich JE, Rounsley SD, Gardner MJ, Wortman JR, et al. (2009) Comparative genomic analyses of the human fungal pathogens Coccidioides and their relatives. Genome Res 19: 1722-1731.
52. Fairhead C, Dujon B, (2006) Structure of Kluyveromyces lactis subtelomeres: duplications and gene content. FEMS Yeast Res 6: 428-441.
53. Fedorova ND, Khaldi N, Joardar VS, Maiti R, Amedeo P, et al. (2008) Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4: e1000046.
54. Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, et al. (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438: 1105-1115.
55. Denayrolles M, de Villechenon EP, Lonvaud-Funel A, Aigle M, (1997) Incidence of SUC-RTM telomeric repeated genes in brewing and wild wine strains of Saccharomyces. Curr Genet 31: 457-461.
56. Halme A, Bumgarner S, Styles C, Fink GR, (2004) Genetic and epigenetic regulation of the FLO gene family generates cell-surface variation in yeast. Cell 116: 405-415.
57. Stanhope MJ, Lupas A, Italia MJ, Koretke KK, Volker C, et al. (2001) Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates. Nature 411: 940-944.
58. Fitzpatrick DA, (2012) Horizontal gene transfer in fungi. FEMS Microbiol Lett 329: 1-8.
59. Rosewich UL, Kistler HC, (2000) Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol 38: 325-363.
60. League GP, Slot JC, Rokas A, (2012) The ASP3 locus in Saccharomyces cerevisiae originated by horizontal gene transfer from Wickerhamomyces. FEMS Yeast Res 12 (7): 859-63.
61. Richards TA, Soanes DM, Jones MD, Vasieva O, Leonard G, et al. (2011) Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc Natl Acad Sci U S A 108: 15258-15263.
62. Ma LJ, van der Does HC, Borkovich KA, Coleman JJ, Daboussi MJ, et al. (2010) Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464: 367-373.
63. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, et al. (2006) Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38: 953-956.
64. Doidy J, Grace E, Kühn C, Simon-Plas F, Casieri L, et al. (2012) Sugar transporters in plants and in their interactions with fungi. Trends Plant Sci 17: 413-422.
65. Loureiro-Dias MC, (1988) Movements of protons coupled to glucose transport in yeasts. A comparative study among 248 yeast strains. Antonie Van Leeuwenhoek 54: 331-343.
66. Brandão RL, Loureiro-Dias MC, (1990) Regulation of Sugar Transport Systems in Fusarium oxysporum var. lini. Appl Environ Microbiol 56: 2417-2420.
67. Lingner U, Munch S, Deising HB, Sauer N, (2011) Hexose transporters of a hemibiotrophic plant pathogen: functional variations and regulatory differences at different stages of infection. J Biol Chem 286: 20913-20922.
68. Kim H, Woloshuk CP, (2011) Functional characterization of fst1 in Fusarium verticillioides during colonization of maize kernels. Mol Plant Microbe Interact 24: 18-24.
69. Koonin EV, Makarova KS, Aravind L, (2001) Horizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55: 709-742.
70. Archibald JM, (2009) The puzzle of plastid evolution. Curr Biol 19: R81-88.
71. Keeling PJ, Palmer JD, (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9: 605-618.
72. Hoekstra RF, (1994) Population genetics of filamentous fungi. Antonie Van Leeuwenhoek 65: 199-204.
73. Walton JD, (2000) Horizontal gene transfer and the evolution of secondary metabolite gene clusters in fungi: an hypothesis. Fungal Genet Biol 30: 167-171.
74. Fitzpatrick DA, Logue ME, Butler G, (2008) Evidence of recent interkingdom horizontal gene transfer between bacteria and Candida parapsilosis. BMC Evol Biol 8: 181.
75. Hall C, Dietrich FS, (2007) The reacquisition of biotin prototrophy in Saccharomyces cerevisiae involved horizontal gene transfer, gene duplication and gene clustering. Genetics 177: 2293-2307.
76. Rolland T, Neuveglise C, Sacerdot C, Dujon B, (2009) Insertion of horizontally transferred genes within conserved syntenic regions of yeast genomes. PLoS One 4: e6515.
77. Hall C, Brachat S, Dietrich FS, (2005) Contribution of horizontal gene transfer to the evolution of Saccharomyces cerevisiae. Eukaryot Cell 4: 1102-1115.
78. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
79. Castresana J, (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-552.
80. Stamatakis A, (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
81. Gertz EM, Yu YK, Agarwala R, Schaffer AA, Altschul SF, (2006) Composition-based statistics and translated nucleotide searches: improving the TBLASTN module of BLAST. BMC Biol 4: 41.
82. Stanke M, Diekhans M, Baertsch R, Haussler D, (2008) Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics 24: 637-644.
83. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
84. Pina-Martins F, Paulo OS, (2008) concatenator: sequence data matrices handling made easy. Mol Ecol Resour 8: 1254-1255.
85. Bryant D, Moulton V, (2004) Neighbor-net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21: 255-265.
86. Huson DH, (1998) SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14: 68-73.
87. Huson DH, Bryant D, (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23: 254-267.
88. Shimodaira H, Hasegawa M, (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Molecular Biology and Evolution 16: 1114.
89. Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis (Version 2.75). Available: http://mesquiteproject.org.
90. Pagel M, (1999) The Maximum Likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Systematic Biology 48: 612-622.
91. Lewis PO, (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Syst Biol 50: 913-925.
92. Byrne KP, Wolfe KH, (2005) The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res 15: 1456-1461.
93. Fitzpatrick DA, O'Gaora P, Byrne KP, Butler G, (2010) Analysis of gene evolution and metabolic pathways using the Candida Gene Order Browser. BMC Genomics 11: 290.
94. Arnaud MB, Chibucos MC, Costanzo MC, Crabtree J, Inglis DO, et al. (2010) The Aspergillus Genome Database, a curated comparative genomics resource for gene, protein and sequence information for the Aspergillus research community. Nucleic Acids Res 38: D420-427.
95. Gonçalves P, Valerio E, Correia C, de Almeida JM, Sampaio JP, (2011) Evidence for divergent evolution of growth temperature preference in sympatric Saccharomyces species. PLoS One 6: e20739.
96. Gietz RD, Schiestl RH, (2007) High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method. Nat Protoc 2: 31-34.
97. Spencer-Martins I, van Uden N, (1985) Catabolite interconversion of glucose transport systems in the yeast Candida wickerhamii. Biochim Biophys Acta 812: 168-172.