Multiple horizontal gene transfers of ammonium transporters/ammonia permeases from prokaryotes to eukaryotes: Toward a new functional and evolutionary classification

Molecular Biology and Evolution

Volumn 29, Issue 1, 2012, Pages 51-60

  McDonald, Tami R ^a   Dietrich, Fred S ^b   Lutzoni, Francxois ^a  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ammonium transporter; Fungal and plant evolution; Horizontal gene transfer; Lichen symbiosis; Methylammonium permease

Indexed keywords

AMMONIA; AMMONIUM TRANSPORTER; MEMBRANE PROTEIN; PERMEASE; UNCLASSIFIED DRUG;

ARTICLE; ASCOMYCETES; CELL LINEAGE; CLADISTICS; CRYSTAL STRUCTURE; EUKARYOTE; FUNGUS; GENE REPLACEMENT THERAPY; GENOME; HORIZONTAL GENE TRANSFER; INHERITANCE; LICHEN (ORGANISM); MOLECULAR EVOLUTION; NONHUMAN; PARENT; PHYLOGENY; PROGENY; PROKARYOTE; PROTEIN FAMILY;

AMMONIA; ANIMALS; ARCHAEA; BACTERIA; CATION TRANSPORT PROTEINS; CHLOROPHYTA; EUKARYOTA; EVOLUTION, MOLECULAR; FUNGI; GENE TRANSFER, HORIZONTAL; PHYLOGENY; QUATERNARY AMMONIUM COMPOUNDS; RHODOPHYTA;

ASCOMYCOTA; EMBRYOPHYTA; EUKARYOTA; FUNGI; PEZIZOMYCOTINA; PROKARYOTA;

EID: 84862891355     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msr123     Document Type: Article

References (66)

1. Ahmadjian V. 1993. The lichen symbiosis. New York: John Wiley.
2. Andrade SL, Dickmanns A, Ficner R, Einsle O. 2005. Crystal structure of the archaeal ammonium transporter Amt-1 from Archaeoglobus fulgidus. Proc Natl Acad Sci U S A. 102:14994-14999. (Pubitemid 41513323)
3. Armaleo D, May S. 2009. Sizing the fungal and algal genomes of the lichen Cladonia grayi through quantitative PCR. Symbiosis 49:43-51.
4. Armaleo D, Sun X, Culberson C. 2011. Insights from the first putative biosynthetic gene cluster for a lichen depside and depsidone. Mycologia 103; 0; 10-335v1-10-335.
5. Bhattacharya D, Yoon HS, Hedges SB, Hackett JD. 2009 Eukaryotes (Eukaryota). In: Hedges SB, Kumar S, editors. The timetree of life. New York: Oxford University Press. p 116-120.
6. Blair JE. 2009. Fungi. In: Hedges SB, Kumar S, editors. The timetree of Life. New York: Oxford University Press. p 215-219.
7. Brock TD, Brock KM, Belly RT, Weiss RL. 1972. Sulfolobus: A new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch Mikrobiol. 84:54-68.
8. Clark DA, Norris PR. 1996. Acidimicrobium ferrooxidans gen. nov., sp. nov.: Mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiology 142:785-790.
9. Couturier J, Montanini B, Martin F, Brun A, Blaudez D, Chalot M. 2007. The expanded family of ammonium transporters in the perennial poplar plant. New Phytol. 174:137-150. (Pubitemid 46333295)
10. Dopson M, Baker-Austin C, Hind A, Bowman JP, Bond PL. 2004. Characterization of Ferroplasma isolates and Ferroplasma acidarmanus sp. nov., extreme acidophiles from acid mine drainage and industrial bioleaching environments. Appl Environ Microbiol. 70:2079-2088. (Pubitemid 38500506)
11. Futterer O, Angelov A, Liesegang H, Gottschalk G, Schleper C, Schepers B, Dock C, Antranikian G, Liebl W. 2004. Genome sequence of Picrophilus torridus and its implications for life around pH 0. Proc Natl Acad Sci U S A. 101:9091-9096. (Pubitemid 38781616)
12. Gogarten JP, Doolittle WF, Lawrence JG. 2002. Prokaryotic evolution in light of gene transfer. Mol Biol Evol. 19:2226-2238. (Pubitemid 35440456)
13. Goltsman DS, Denef VJ, Singer SW, et al. (17 co-Authors). 2009. Community genomic and proteomic analyses of chemoautotrophic iron-oxidizing "Leptospirillum rubarum" (Group II) and "Leptospirillum ferrodiazotrophum" (Group III) bacteria in acid mine drainage biofilms. Appl Environ Microbiol. 75:4599-4615.
14. Gruswitz F, Chaudhary S, Ho JD, Schlessinger A, Pezeshki B, Ho CM, Sali A, Westhoff CM, Stroud RM. 2010. Function of human Rh based on structure of RhCG at 2.1 A. Proc. Natl Acad Sci U S A. 107:9638-9643.
15. Gueidan C, Roux C, Lutzoni F. 2007. Using a multigene phylogenetic analysis to assess generic delineation and character evolution in Verrucariaceae (Verrucariales, Ascomycota). Mycol Res. 111:1145-1168. (Pubitemid 350116567)
16. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 52:696-704. (Pubitemid 37365050)
17. Hibbett DS, Binder M, Bischoff JF, et al. (67 co-Authors). 2007. A higher-level phylogenetic classification of the Fungi. Mycol Res. 111:509-547. (Pubitemid 46915419)
18. Huang CH, Peng J. 2005. Evolutionary conservation and diversification of Rh family genes and proteins. Proc Natl Acad Sci U S A. 102:15512-15517. (Pubitemid 41528088)
19. Itoh T, Suzuki K, Sanchez PC, Nakase T. 1999. Caldivirga maquilingensis gen. nov., sp. nov., a new genus of rod-shaped crenarchaeote isolated from a hot spring in the Philippines. Int J Syst Bacteriol. 49(Pt 3):1157-1163.
20. James TY, Kauff F, Schoch CL, et al. (70 co-Authors). 2006. Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818-822. (Pubitemid 44622687)
21. Javelle A, Andre B, Marini AM, Chalot M. 2003. High-Affinity ammonium transporters and nitrogen sensing in mycorrhizas. Trends Microbiol. 11:53-55. (Pubitemid 36207496)
22. Javelle A, Lupo D, Zheng L, Li XD, Winkler FK, Merrick M. 2006. An unusual twin-his arrangement in the pore of ammonia channels is essential for substrate conductance. J Biol Chem. 281:39492-39498. (Pubitemid 46041909)
23. Keeling P, Leander BS, Simpson A. 2009. Eukaryotes. Eukaryota, Organisms with nucleated cells. Version 28 October 2009. Available from: Http://tolweb.org/Eukaryotes/3/2009.10.28. In The Tree of Life Web Project. [cited 2011 May 27]. Available from: Http://tolweb.org.
24. Kelly DP, Wood AP. 2000. Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol. 50(Pt 2):511-516. (Pubitemid 30167492)
25. Khademi S, O'Connell J 3rd, Remis J, Robles-Colmenares Y, Miercke LJ, Stroud RM. 2004. Mechanism of ammonia transport by Amt/MEP/Rh: Structure of AmtB at 1.35 A. Science 305:1587-1594. (Pubitemid 39296348)
26. Kustu S, Inwood W. 2006. Biological gas channels for NH3 and CO2: Evidence that Rh (Rhesus) proteins are CO2 channels. Transfus Clin Biol. 13:103-110.
27. Lamoureux G, Javelle A, Baday S, Wang S, Berneche S. 2010. Transport mechanisms in the ammonium transporter family. Transfus Clin Biol. 17:168-175.
28. Lamoureux G, Klein ML, Berneche S. 2007. A stable water chain in the hydrophobic pore of the AmtB ammonium transporter. Biophys J. 92:L82-L84. (Pubitemid 46684557)
29. Li X, Jayachandran S, Nguyen HH, Chan MK. 2007. Structure of the Nitrosomonas europaea Rh protein. Proc Natl Acad Sci U S A. 104:19279-19284.
30. Li X, Lupo D, Zheng L, Winkler F. 2006. Structural and functional insights into the AmtB/Mep/Rh protein family. Transfus Clin Biol. 13:165-169.
31. Lopez-Pedrosa A, Gonzalez-Guerrero M, Valderas A, Azcon-Aguilar C, Ferrol N. 2006. GintAMT1 encodes a functional high-Affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet Biol. 43:102-110. (Pubitemid 43227995)
32. Lorenz MC, Heitman J. 1998. The MEP2 ammonium permease regulates pseudohyphal differentiation in Saccharomyces cerevisiae. EMBO J. 17:1236-1247. (Pubitemid 28105503)
33. Ludewig U, von Wiren N, Frommer WB. 2002. Uniport of NH4+ by the root hair plasma membrane ammonium transporter LeAMT1;1. J Biol Chem. 277:13548-13555. (Pubitemid 34967951)
34. Lutzoni F, Kauff F, Cox JC, et al. (44 co-Authors). 2004. Assembling the fungal tree of life: Progress, classification, and evolution of subcellular traits. Am J Bot. 91:1446-1480. (Pubitemid 43193713)
35. Lutzoni F, Pagel M, Reeb V. 2001. Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411:937-940. (Pubitemid 32601487)
36. Maddison DR, Maddison WP. 2005. MacClade 4. Sunderland (MA): Sinauer Associates.
37. Marcet-Houben M, Gabaldon T. 2010. Acquisition of prokaryotic genes by fungal genomes. Trends Genet. 26:5-8.
38. Marini AM, Soussi-Boudekou S, Vissers S, Andre B. 1997. A family of ammonium transporters in Saccharomyces cerevisiae. Mol Cell Biol. 17:4282-4293. (Pubitemid 27318104)
39. Marini AM, Urrestarazu A, Beauwens R, Andre B. 1997. The Rh (rhesus) blood group polypeptides are related to NH4+ transporters. Trends Biochem Sci. 22:460-461. (Pubitemid 27515910)
40. Marini AM, Vissers S, Urrestarazu S, Andre B. 1994. Cloning and expression of the MEP1 gene encoding an ammonium transporter in Saccharomyces cerevisiae. EMBO J. 13(15):3456-3463. (Pubitemid 24246181)
41. Mayer M, Dynowski M, Ludewig U. 2006. Ammonium ion transport by the AMT/Rh homologue LeAMT1;1. Biochem J. 396:431-437. (Pubitemid 44228158)
42. Mayer M, Ludewig U. 2006. Role of AMT1;1 in NH4+ acquisition in Arabidopsis thaliana. Plant Biol (Stuttg). 8:522-528. (Pubitemid 44140744)
43. McDonald SM, Plant JN, Worden AZ. 2010. The mixed lineage nature of nitrogen transport and assimilation in marine eukaryotic phytoplankton: A case study of Micromonas. Mol Biol Evol. 27:2268-2283.
44. Monahan BJ, Fraser JA, Hynes MJ, Davis MA. 2002. Isolation and characterization of two ammonium permease genes, meaA and mepA, from Aspergillus nidulans. Eukaryot Cell. 1:85-94. (Pubitemid 36562351)
45. Montanini B, Moretto N, Soragni E, Percudani R, Ottonello S. 2002. A high-Affinity ammonium transporter from the mycorrhizal ascomycete Tuber borchii. Fungal Genet Biol. 36:22-34.
46. Ninnemann O, Jauniaux JC, Frommer WB. 1994. Identification of a high affinity NH4+ transporter from plants. EMBO J. 13(15):3464-3471. (Pubitemid 24246182)
47. Nylander JAA. 2004. MrModeltest v2. Program distributed by the author. Uppsala (Sweden): Evolutionary Biology Centre, Uppsala University.
48. Posada D. 2008. jModelTest: Phylogenetic model averaging. Mol Biol Evol. 25:1253-1256. (Pubitemid 351882013)
49. Richards TA, Soanes DM, Foster PG, Leonard G, Thornton CR, Talbot NJ. 2009. Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell. 21:1897-1911.
50. Rutherford JC, Lin X, Nielsen K, Heitman J. 2008. Amt2 permease is required to induce ammonium-responsive invasive growth and mating in Cryptococcus neoformans. Eukaryot Cell. 7:237-246. (Pubitemid 351959690)
51. Schleper C, Puehler G, Holz I, Gambacorta A, Janekovic D, Santarius U, Klenk HP, Zillig W. 1995. Picrophilus gen. nov., fam. nov.: A novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. J Bacteriol. 177:7050-7059.
52. Schleper C, Puhler G, Klenk HP, Zillig W. 1996. Picrophilus oshimae and Picrophilus torridus fam. nov., gen. nov., sp. nov., two species of hyperacidophilic, thermophilic, heterotrophic, aerobic archaea. Int J Syst Bacteriol. 46:814-816.
53. Schoch CL, Sung GH, Lopez-Giraldez F, et al. (64 co-Authors). 2009. The Ascomycota tree of life: A phylum-wide phylogeny clarifies the origin and evolution of fundamental reproductive and ecological traits. Syst Biol. 58:224-239.
54. She Q, Singh RK, Confalonieri F, et al. (31 co-Authors). 2001. The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc Natl Acad Sci U S A. 98:7835-7840. (Pubitemid 32642647)
55. Simmons EG. 1992. Alternaria taxonomy: Current status, viewpoint, challenge. In: Chelkowski J, Visconti A, editors. Alternaria: Biology, plant diseases and metabolites. New York: Elsevier. p 1-36.
56. Slot JC, Hibbett DS. 2007. Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: A phylogenetic study. PLoS One. 2(10):e1097.
57. Sohlenkamp C, Wood CC, Roeb GW, Udvardi MK. 2002. Characterization of Arabidopsis AtAMT2, a high-Affinity ammonium transporter of the plasma membrane. Plant Physiol. 130:1788-1796. (Pubitemid 36035177)
58. Stamatakis A, Ludwig T, Meier H. 2005. RAxML-III: A fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456-463. (Pubitemid 40310232)
59. Suzuki T, Iwasaki T, Uzawa T, Hara K, Nemoto N, Kon T, Ueki T, Yamagishi A, Oshima T. 2002. Sulfolobus tokodaii sp. nov. (f. Sulfolobus sp. strain 7), a new member of the genus Sulfolobus isolated from Beppu Hot Springs, Japan. Extremophiles 6:39-44. (Pubitemid 41490491)
60. Swofford DL. 2002. PAUP*: Phylogenetic analysis using parsimony (*and other methods). Sunderland (MA): Sinauer Associates.
61. Trembley ML, Ringli C, Honegger R. 2002. Morphological and molecular analysis of early stages in the resynthesis of the lichen Baeomyces rufus. Mycol Res. 106(7):768-776. (Pubitemid 35197635)
62. Valdes J, Quatrini R, Hallberg K, Dopson M, Valenzuela PD, Holmes DS. 2009. Draft genome sequence of the extremely acidophilic bacterium Acidithiobacillus caldus ATCC 51756 reveals metabolic versatility in the genus Acidithiobacillus. J Bacteriol. 191:5877-5878.
63. Winkler FK. 2006. Amt/MEP/Rh proteins conduct ammonia. Pflugers Arch. 451:701-707. (Pubitemid 43228053)
64. Yang H, Xu Y, Zhu W, Chen K, Jiang H. 2007. Detailed mechanism for AmtB conducting NH4+/NH3: Molecular dynamics simulations. Biophys J. 92:877-885. (Pubitemid 46203217)
65. Zheng L, Kostrewa D, Berneche S, Winkler FK, Li XD. 2004. The mechanism of ammonia transport based on the crystal structure of AmtB of Escherichia coli. Proc Natl Acad Sci U S A. 101:17090-17095. (Pubitemid 39627779)
66. Zolan ME, Pukkila PJ. 1986. Inheritance of DNA methylation in Coprinus cinereus. Mol Cell Biol. 6:195-200. (Pubitemid 16182098)