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Horizontal Gene Transfer of “Prototype” Nramp in Bacteria

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Abstract

Eukaryotic Nramp genes encode divalent metal ion permeases important for nutrition and resistance to microbial infection. Bacterial homologs encode proton-dependent transporters of manganese (MntH), and other divalent metal ions. Bacterial MntH were classified in three homology groups (A, B, C) and MntH C further subdivided in Cα, Cβ, Cγ. The proteins from C. tepidum (MntH B) and E. faecalis (MntH Cβ1, 2), divergent in sequence and hydropathy profile, conferred increased metal sensitivity when expressed in E. coli, suggesting conservation of divalent metal transport function in MntH B and C. Several genomic evidence suggest horizontal gene transfer (HGT) of mntH C genes: (i) The enterobacteria Wigglesworthia mntH Cβ gene is linked to an Asn t-RNA, and its sequence most conserved with Gram positive bacteria homologs; (ii) all the Cβ genes identified in oral streptococcaceae are associated with different potentially mobile DNA elements; (iii) Lactococcus lactis and Burkholderia mallei genomes contain an mntH gene prematurely terminated and a novel full-length mntH C gene; (iv) remarkable sequence relatedness between the unicellular alga C. reinhardtii “prototype” Nramp and some MntH Cα (e.g., Nostoc spp., Listeria spp.) suggests HGT between Eukarya and Bacteria. Other “prototype” Nramp genes (intronless, encoding proteins strongly conserved with MntH A and B proteins) identified in invertebrates represent a possible source for transfer of Nramp genes toward opportunistic bacteria. This study demonstrates complex evolution of MntH in Bacteria. It is proposed that “prototype” Nramp are ancestors of bacterial MntH C proteins, which could facilitate bacterial infection.

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References

  1. D Agranoff IM Monahan JA Mangan PD Butcher S Krishna (1999) ArticleTitleMycobacterium tuberculosis expresses a novel pH-dependent divalent cation transporter belonging to the Nramp family. J Exp Med 190 717–724 Occurrence Handle10.1084/jem.190.5.717 Occurrence Handle1:CAS:528:DyaK1MXlvFCitrg%3D Occurrence Handle10477555

    Article  CAS  PubMed  Google Scholar 

  2. L Akman S Aksoy (2001) ArticleTitleA novel application of gene arrays: Escherichia coli array provides insight into the biology of the obligate endosymbiont of tsetse flies. Proc Natl Acad Sci USA 98 7546–7551 Occurrence Handle10.1073/pnas.131057498 Occurrence Handle1:CAS:528:DC%2BD3MXkslWls7g%3D Occurrence Handle11404467

    Article  CAS  PubMed  Google Scholar 

  3. L Akman A Yamashita H Watanabe K Oshima T Shiba M Hattori S Aksoy (2002) ArticleTitleGenome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossidina. Nat Genet 32 402–407 Occurrence Handle10.1038/ng986 Occurrence Handle1:CAS:528:DC%2BD38Xot1Klsb8%3D Occurrence Handle12219091

    Article  CAS  PubMed  Google Scholar 

  4. S Aksoy (1995) ArticleTitleWigglesworthia gen. nov. and Wigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyte-associated, primary endosymbionts of tsetse flies. Int J Syst Bacteriol 45 848–851 Occurrence Handle7547309

    PubMed  Google Scholar 

  5. RD Appel A Bairoch DF Hochstrasser (1994) ArticleTitleA new generation of information retrieval tools for biologists: The example of the ExPASy WWW server. Trends Biochem Sci 19 258–260 Occurrence Handle1:STN:280:ByuA2MzkvVI%3D

    CAS  Google Scholar 

  6. A Berge M Rasmussen L Bjorck (1998) ArticleTitleIdentification of an insertion sequence located in a region encoding virulence factors of Streptococcus pyogenes. Infect Immun 66 3449–3453 Occurrence Handle1:CAS:528:DyaK1cXktFCjsb4%3D Occurrence Handle9632622

    CAS  PubMed  Google Scholar 

  7. Berkeley Drosophila Genome Project port and the Gadfly database [http://www.fruitfly.org/annot/index.html ]

  8. B Canback SG Andersson CG Kurland (2002) ArticleTitleThe global phylogeny of glycolytic enzymes. Proc Natl Acad Sci USA 99 6097–6102 Occurrence Handle10.1073/pnas.082112499 Occurrence Handle1:CAS:528:DC%2BD38XjslWnsro%3D Occurrence Handle11983902

    Article  CAS  PubMed  Google Scholar 

  9. M Cellier G Govoni S Vidal T Kwan N Groulx J Liu F Sanchez E Skamene E Schurr P Gros (1994) ArticleTitleHuman natural resistance-associated macrophage protein: cDNA cloning, chromosomal mapping, genomic organization, and tissue-specific expression. J Exp Med 180 1741–1752 Occurrence Handle1:CAS:528:DyaK2MXhtFGlsr8%3D Occurrence Handle7964458

    CAS  PubMed  Google Scholar 

  10. M Cellier G Prive A Belouchi T Kwan V Rodrigues W Chia P Gros (1995) ArticleTitleNramp defines a family of membrane proteins. Proc Natl Acad Sci 92 10089–10093 Occurrence Handle1:CAS:528:DyaK2MXovFamu7c%3D Occurrence Handle7479731

    CAS  PubMed  Google Scholar 

  11. MF Cellier I Bergevin E Boyer E Richer (2001) ArticleTitlePolyphyletic origins of bacterial Nramp transporters. Trends Genet 17 365–370 Occurrence Handle10.1016/S0168-9525(01)02364-2 Occurrence Handle1:CAS:528:DC%2BD3MXksVyntr8%3D Occurrence Handle11418195

    Article  CAS  PubMed  Google Scholar 

  12. M Chandler O Fayet (1993) ArticleTitleTranslational frameshifting in the control of transposition in bacteria. Mol Microbiol 7 497–503 Occurrence Handle1:CAS:528:DyaK3sXhs1Crsrw%3D Occurrence Handle8384687

    CAS  PubMed  Google Scholar 

  13. X Chen S Li S Aksoy (1999) ArticleTitleConcordant evolution of a symbiont with its host insect species: Molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J Mol Evol 48 49–58 Occurrence Handle1:CAS:528:DyaK1MXlvFKntw%3D%3D Occurrence Handle9873076

    CAS  PubMed  Google Scholar 

  14. XZ Chen JB Peng A Cohen H Nelson N Nelson MA Hediger (1999) ArticleTitleYeast SMF1 mediates H(+)-coupled iron uptake with concomitant uncoupled cation currents. J Biol Chem 274 35089–35094 Occurrence Handle10.1074/jbc.274.49.35089 Occurrence Handle1:CAS:528:DyaK1MXnvFyrtLY%3D Occurrence Handle10574989

    Article  CAS  PubMed  Google Scholar 

  15. C Curie JM Alonso M Le Jean JR Ecker JF Briat (2000) ArticleTitleInvolvement of NRAMP1 from Arabidopsis thaliana in iron transport. Biochem J 347 IssueIDPt 3 749–755 Occurrence Handle10.1042/0264-6021:3470749 Occurrence Handle1:CAS:528:DC%2BD3cXjsFCjsro%3D Occurrence Handle10769179

    Article  CAS  PubMed  Google Scholar 

  16. C Dale SC Welburn (2001) ArticleTitleThe endosymbionts of tsetse flies: manipulating host-parasite interactions. Int J Parasitol 31 628–631 Occurrence Handle1:STN:280:DC%2BD3M3ktVShsA%3D%3D Occurrence Handle11334953

    CAS  PubMed  Google Scholar 

  17. X De Lamballerie C Zandotti C Vignoli C Bollet P De Micco (1992) ArticleTitleA one-step microbial DNA extraction method using “Chelex 100” suitable for gene amplification. Res Microbiol 143 785–790 Occurrence Handle10.1016/0923-2508(92)90107-Y Occurrence Handle1298031

    Article  PubMed  Google Scholar 

  18. DR Demuth Y Duan HF Jenkinson R McNab S Gil RJ Lamont (1997) ArticleTitleInterruption of the Streptococcus gordonii M5 sspA/sspB intergenic region by an insertion sequence related to IS1167 of Streptococcus pneumoniae. Microbiology 143 IssueIDPt 6 2047–2055 Occurrence Handle1:CAS:528:DyaK2sXktVyksr4%3D Occurrence Handle9202480

    CAS  PubMed  Google Scholar 

  19. RF Doolittle (2002) ArticleTitleBiodiversity: Microbial genomes multiply. Nature 416 697–700 Occurrence Handle1:CAS:528:DC%2BD38XjtVKks74%3D Occurrence Handle11961543

    CAS  PubMed  Google Scholar 

  20. J D’Souza PY Cheah P Gros W Chia V Rodrigues (1999) ArticleTitleFunctional complementation of the malvolio mutation in the taste pathway of Drosophila melanogaster by the human natural resistance-associated macrophage protein 1 (Nramp-1). J Exp Biol 202 IssueIDPt 14 1909–1915 Occurrence Handle1:CAS:528:DyaK1MXls1WnsLg%3D Occurrence Handle10377272

    CAS  PubMed  Google Scholar 

  21. ExPASy Molecular Biology Server [http://ca.expasy.org/ ]

  22. MD Fleming CC Trenor III MA Su D Foernzler DR Beier WF Dietrich NC Andrews (1997) ArticleTitleMicrocytic anaemia mice have a mutation in Nramp2, a candidate iron transporter gene. Nat Genet 16 383–386 Occurrence Handle1:CAS:528:DyaK2sXkvFChtrY%3D Occurrence Handle9241278

    CAS  PubMed  Google Scholar 

  23. JR Forbes P Gros (2001) ArticleTitleDivalent-metal transport by NRAMP proteins at the interface of host-pathogen interactions. Trends Microbiol 9 397–403 Occurrence Handle10.1016/S0966-842X(01)02098-4 Occurrence Handle1:CAS:528:DC%2BD3MXmtV2jt7c%3D Occurrence Handle11514223

    Article  CAS  PubMed  Google Scholar 

  24. EA Gaucher X Gu MM Miyamoto SA Benner (2002) ArticleTitlePredicting functional divergence in protein evolution by site-specific rate shifts. Trends Biochem Sci 27 IssueID6 315–321 Occurrence Handle10.1016/S0968-0004(02)02094-7 Occurrence Handle1:CAS:528:DC%2BD38XksFOjurc%3D Occurrence Handle12069792

    Article  CAS  PubMed  Google Scholar 

  25. R Gil B Sabater-Munoz A Latorre FJ Silva A Moya (2002) ArticleTitleExtreme genome reduction in Buchnera spp.: Toward the minimal genome needed for symbiotic life. Proc Natl Acad Sci USA 99 4454–4458 Occurrence Handle10.1073/pnas.062067299 Occurrence Handle1:CAS:528:DC%2BD38XivFShtb4%3D Occurrence Handle11904373

    Article  CAS  PubMed  Google Scholar 

  26. G Glockner L Eichinger K Szafranski JA Pachebat AT Bankier PH Dear R Lehmann C Baumgart G Parra JF Abril R Guigo K Kumpf B Tunggal E Cox MA Quail M Platzer A Rosenthal AA Noegel (2002) ArticleTitleSequence and analysis of chromosome 2 of Dictyostelium discoideum. Nature 418 79–85 Occurrence Handle10.1038/nature00847 Occurrence Handle12097910

    Article  PubMed  Google Scholar 

  27. G Govoni F Canonne-Hergaux CG Pfeifer SL Marcus SD Mills DJ Hackam S Grinstein D Malo BB Finlay P Gros (1999) ArticleTitleFunctional expression of Nramp1 in vitro in the murine macrophage line RAW264.7. Infect Immun 67 2225–2232 Occurrence Handle1:CAS:528:DyaK1MXivFWiur8%3D Occurrence Handle10225878

    CAS  PubMed  Google Scholar 

  28. S Gruenheid E Pinner M Desjardins P Gros (1997) ArticleTitleNatural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome. J Exp Med 185 717–730 Occurrence Handle10.1084/jem.185.4.717 Occurrence Handle1:CAS:528:DyaK2sXhtlWnu7Y%3D Occurrence Handle9034150

    Article  CAS  PubMed  Google Scholar 

  29. X Gu J Zhang (1997) ArticleTitleA simple method for estimating the parameter of substitution rate variation among sites. Mol Biol Evol 14 IssueID11 1106–1113 Occurrence Handle1:CAS:528:DyaK2sXnt1aksrc%3D Occurrence Handle9364768

    CAS  PubMed  Google Scholar 

  30. H Gunshin B Mackenzie UV Berger Y Gunshin MF Romero WF Boron S Nussberger JL Gollan MA Hediger (1997) ArticleTitleCloning and characterization of a mammalian proton-coupled metal-ion transporter. Nature 388 482–488 Occurrence Handle10.1038/41343 Occurrence Handle1:CAS:528:DyaK2sXltFGqtbY%3D Occurrence Handle9242408

    Article  CAS  PubMed  Google Scholar 

  31. LM Guzman D Belin MJ Carson J Beckwith (1995) ArticleTitleTight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177 4121–4130 Occurrence Handle1:CAS:528:DyaK2MXmvV2gtL8%3D Occurrence Handle7608087

    CAS  PubMed  Google Scholar 

  32. DJ Hackam OD Rotstein W Zhang S Gruenheid P Gros S Grinstein (1998) ArticleTitleHost resistance to intracellular infection: mutation of natural resistance-associated macrophage protein 1 (Nramp1) impairs phagosomal acidification. J Exp Med 188 351–364 Occurrence Handle10.1084/jem.188.2.351 Occurrence Handle1:CAS:528:DyaK1cXkvVaqtLw%3D Occurrence Handle9670047

    Article  CAS  PubMed  Google Scholar 

  33. HS Heine MJ England DM Waag WR Byrne (2001) ArticleTitleIn vitro antibiotic susceptibilities of Burkholderia mallei (causative agent of glanders) determined by broth microdilution and E-test. Antimicrob Agents Chemother 45 2119–2121 Occurrence Handle10.1128/AAC.45.7.2119-2121.2001 Occurrence Handle1:CAS:528:DC%2BD3MXks1GksLo%3D Occurrence Handle11408233

    Article  CAS  PubMed  Google Scholar 

  34. SN Ho HD Hunt RM Horton JK Pullen LR Pease (1989) ArticleTitleSite-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77 51–59 Occurrence Handle1:CAS:528:DyaL1MXktVaitrk%3D Occurrence Handle2744487

    CAS  PubMed  Google Scholar 

  35. YM Hou (1999) ArticleTitleTransfer RNAs and pathogenicity islands. Trends Biochem Sci 24 295–298 Occurrence Handle10.1016/S0968-0004(99)01428-0 Occurrence Handle1:CAS:528:DC%2BD3cXjtVKruw%3D%3D Occurrence Handle10431171

    Article  CAS  PubMed  Google Scholar 

  36. WS Hu CC Yang (2001) ArticleTitleIS1550 from Mycoplasma fermentans is transposable in Escherichia coli. FEMS Microbiol Lett 198 159–164 Occurrence Handle10.1016/S0378-1097(01)00139-2 Occurrence Handle1:CAS:528:DC%2BD3MXjtFGit7w%3D Occurrence Handle11430408

    Article  CAS  PubMed  Google Scholar 

  37. N Jabado A Jankowski S Dougaparsad V Picard S Grinstein P Gros (2000) ArticleTitleNatural resistance to intracellular infections: natural resistance-associated macrophage protein 1 (Nramp1) functions as a pH-dependent manganese transporter at the phagosomal membrane. J Exp Med 192 1237–1248 Occurrence Handle10.1084/jem.192.9.1237 Occurrence Handle1:CAS:528:DC%2BD3cXnvFWgt7w%3D Occurrence Handle11067873

    Article  CAS  PubMed  Google Scholar 

  38. DT Jones WR Taylor JM Thornton (1994) ArticleTitleA model recognition approach to the prediction of all-helical membrane protein structure and topology. Biochemistry 33 3038–3049 Occurrence Handle1:CAS:528:DyaK2cXhsFyju7g%3D Occurrence Handle8130217

    CAS  PubMed  Google Scholar 

  39. DG Kehres ML Zaharik BB Finlay ME Maguire (2000) ArticleTitleThe NRAMP proteins of Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol Microbiol 36 1085–1100 Occurrence Handle10.1046/j.1365-2958.2000.01922.x Occurrence Handle1:CAS:528:DC%2BD3cXktF2lu70%3D Occurrence Handle10844693

    Article  CAS  PubMed  Google Scholar 

  40. EV Koonin KS Makarova L Aravind (2001) ArticleTitleHorizontal gene transfer in prokaryotes: quantification and classification. Annu Rev Microbiol 55 709–742 Occurrence Handle10.1146/annurev.micro.55.1.709 Occurrence Handle1:CAS:528:DC%2BD3MXnslKjtbw%3D Occurrence Handle11544372

    Article  CAS  PubMed  Google Scholar 

  41. JO Korbel B Snel MA Huynen P Bork (2002) ArticleTitleSHOT: A web server for the construction of genome phylogenies. Trends Genet 18 158–162 Occurrence Handle10.1016/S0168-9525(01)02597-5 Occurrence Handle1:CAS:528:DC%2BD38XhtlGju7g%3D Occurrence Handle11858840

    Article  CAS  PubMed  Google Scholar 

  42. S Kumar K Tamura IB Jakobsen M Nei (2001) ArticleTitleMEGA2: Molecular evolutionary genetics analysis software. Bioinformatics 17 1244–1245 Occurrence Handle1:CAS:528:DC%2BD38XmtVCktQ%3D%3D Occurrence Handle11751241

    CAS  PubMed  Google Scholar 

  43. JG Lawrence RW Hendrix S Casjens (2001) ArticleTitleWhere are the pseudogenes in bacterial genomes? Trends Microbiol 9 535–540 Occurrence Handle10.1016/S0966-842X(01)02198-9 Occurrence Handle1:CAS:528:DC%2BD3MXosFCksLw%3D Occurrence Handle11825713

    Article  CAS  PubMed  Google Scholar 

  44. J Mahillon C Leonard M Chandler (1999) ArticleTitleIS elements as constituents of bacterial genomes. Res Microbiol 150 675–687 Occurrence Handle10.1016/S0923-2508(99)00124-2 Occurrence Handle1:CAS:528:DC%2BD3cXoslWmsg%3D%3D Occurrence Handle10673006

    Article  CAS  PubMed  Google Scholar 

  45. H Makui E Roig ST Cole JD Helmann P Gros MF Cellier (2000) ArticleTitleIdentification of the Escherichia coli K-12 Nramp orthologue (MntH) as a selective divalent metal ion transporter. Mol Microbiol 35 1065–1078 Occurrence Handle10.1046/j.1365-2958.2000.01774.x Occurrence Handle1:CAS:528:DC%2BD3cXitVahu7k%3D Occurrence Handle10712688

    Article  CAS  PubMed  Google Scholar 

  46. JC Meeks J Elhai (2002) ArticleTitleRegulation of cellular differentiation in filamentous cyanobacteria in free-living and plant-associated symbiotic growth states. Microbiol Mol Biol Rev 66 94–121 Occurrence Handle1:CAS:528:DC%2BD38XislSntbY%3D Occurrence Handle11875129

    CAS  PubMed  Google Scholar 

  47. D Minerdi R Fani R Gallo A Boarino P Bonfante (2001) ArticleTitleNitrogen fixation genes in an endosymbiotic Burkholderia strain. Appl Environ Microbiol 67 725–732 Occurrence Handle10.1128/AEM.67.2.725-732.2001 Occurrence Handle1:CAS:528:DC%2BD3MXhtFSlsrY%3D Occurrence Handle11157237

    Article  CAS  PubMed  Google Scholar 

  48. L Moulin A Munive B Dreyfus C Boivin-Masson (2001) ArticleTitleNodulation of legumes by members of the beta-subclass of Proteobacteria. Nature 411 948–950 Occurrence Handle1:CAS:528:DC%2BD3MXkvVWhu7Y%3D Occurrence Handle11418858

    CAS  PubMed  Google Scholar 

  49. E Pinner S Gruenheid M Raymond P Gros (1997) ArticleTitleFunctional complementation of the yeast divalent cation transporter family SMF by NRAMP2, a member of the mammalian natural resistance-associated macrophage protein family. J Biol Chem 272 28933–28938 Occurrence Handle10.1074/jbc.272.46.28933 Occurrence Handle1:CAS:528:DyaK2sXnsVKkt7o%3D Occurrence Handle9360964

    Article  CAS  PubMed  Google Scholar 

  50. PredictProtein interface [http://cubic.bioc.columbia.edu/predictprotein/ ]

  51. The Preliminary Directory of Dictyostelium Genes—Version 2.1 Gene [http://dicty.sdsc.edu/annotationdicty.html ]

  52. Psipred v2.4 protein structure prediction server [http://bioinf.cs.ucl.ac.uk/psipred/ ]

  53. Q Que JD Helmann (2000) ArticleTitleManganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressoer family of proteins. Mol Microbiol 35 1454–1468

    Google Scholar 

  54. B Rost (1996) ArticleTitlePHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol 266 525–539 Occurrence Handle1:CAS:528:DyaK28Xltl2ntLY%3D Occurrence Handle8743704

    CAS  PubMed  Google Scholar 

  55. D Rouhbakhsh P Baumann (1995) ArticleTitleCharacterization of a putative 23S-5S rRNA operon of Buchnera aphidicola (endosymbiont of aphids) unlinked to the 16S rRNA-encoding gene. Gene 155 107–112 Occurrence Handle10.1016/0378-1119(94)00910-K Occurrence Handle1:CAS:528:DyaK2MXltl2is7s%3D Occurrence Handle7535281

    Article  CAS  PubMed  Google Scholar 

  56. CE Rubens LM Heggen JM Kuypers (1989) ArticleTitleIS861, a group B streptococcal insertion sequence related to IS150 and IS3 of Escherichia coli. J Bacteriol 171 5531–5535 Occurrence Handle1:CAS:528:DyaK3MXkt1eht74%3D Occurrence Handle2477359

    CAS  PubMed  Google Scholar 

  57. AR Sanchez-Beato E Garcia R Lopez JL Garcia (1997) ArticleTitleIdentification and characterization of IS1381, a new insertion sequence in Streptococcus pneumoniae. J Bacteriol 179 2459–2463 Occurrence Handle1:CAS:528:DyaK2sXit1GltLY%3D Occurrence Handle9079939

    CAS  PubMed  Google Scholar 

  58. FJ Silva A Latorre A Moya (2001) ArticleTitleGenome size reduction through multiple events of gene disintegration in Buchnera APS. Trends Genet 17 615–618 Occurrence Handle10.1016/S0168-9525(01)02483-0 Occurrence Handle1:CAS:528:DC%2BD3MXnslemtL4%3D Occurrence Handle11672844

    Article  CAS  PubMed  Google Scholar 

  59. JC Smoot KD Barbian JJ Van Gompel LM Smoot MS Chaussee GL Sylva DE Sturdevant SM Ricklefs SF Porcella LD Parkins SB Beres DS Campbell TM Smith Q Zhang V Kapur JA Daly LG Veasy JM Musser (2002) ArticleTitleGenome sequence and comparative microarray analysis of serotype M18 group A Streptococcus strains associated with acute rheumatic fever outbreaks. Proc Natl Acad Sci USA 99 4668–4673 Occurrence Handle10.1073/pnas.062526099 Occurrence Handle1:CAS:528:DC%2BD38XivFSgsrg%3D Occurrence Handle11917108

    Article  CAS  PubMed  Google Scholar 

  60. S Thomine R Wang JM Ward NM Crawford JI Schroeder (2000) ArticleTitleCadmium and iron transport by members of a plant metal transporter family in Arabidopsis with homology to Nramp genes. Proc Natl Acad Sci USA 97 4991–4996 Occurrence Handle1:CAS:528:DC%2BD3cXivFKis70%3D Occurrence Handle10781110

    CAS  PubMed  Google Scholar 

  61. JD Thompson TJ Gibson F Plewniak F Jeanmougin DG Higgins (1997) ArticleTitleThe CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25 4876–4882 Occurrence Handle1:CAS:528:DyaK1cXntFyntQ%3D%3D Occurrence Handle9396791

    CAS  PubMed  Google Scholar 

  62. GC Ulett BJ Currie TW Clair M Mayo N Ketheesan J Labrooy D Gal R Norton CA Smith J Barnes J Warner RG Hirst (2001) ArticleTitle Burkholderia pseudomallei virulence: Definition, stability and association with clonality. Microbes Infect 3 621–631 Occurrence Handle10.1016/S1286-4579(01)01417-4 Occurrence Handle1:CAS:528:DC%2BD3MXltVGjurw%3D Occurrence Handle11445448

    Article  CAS  PubMed  Google Scholar 

  63. P Utaisincharoen N Tangthawornchaikul W Kespichayawattana P Chaisuriya S Sirisinha (2001) ArticleTitle Burkholderia pseudomallei interferes with inducible nitric oxide synthase (iNOS) production: A possible mechanism of evading macrophage killing. Microbiol Immunol 45 307–313 Occurrence Handle1:CAS:528:DC%2BD3MXjvVSitbo%3D Occurrence Handle11386421

    CAS  PubMed  Google Scholar 

  64. Wormbase [http://www.wormbase.org/ ] Anopheles gambiae [http://www.ncbi.nlmnih gov/PMGifs/Genomes/euk_g.html ]

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Acknowledgements

We would like to thank two reviewers for their constructive comments, Dr. S. Aksoy (Yale University) for sharing Wigglesworthia genomic data and generously providing purified Wigglesworthia genomic DNA and Dr. P. Courvalin (Institut Pasteur, Paris) for kindly providing E. faecalis V583 strain. We acknowledge gratefully the NCBI online facilities (National Library of Medicine, Washington, DC), including BLAST search and Taxonomy servers and also, in particular, the contributing Microbial Genome Sequencing Projects. This work is supported by a research grant from the Canadian Institutes of Health Research. I.B. and E.R. are supported by the NSERC and CIHR, respectively. Dr. Cellier is a scholar from the Fonds pour la Recherche en Santé du Québec.

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  1. INRS-Institut Armand-Frappier, 531, Bd des prairies, Laval, PQ, Canada H7V 1B7

    Etienne Richer, Pascal Courville, Isabelle Bergevin & Mathieu F. M. Cellier

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Richer, E., Courville, P., Bergevin, I. et al. Horizontal Gene Transfer of “Prototype” Nramp in Bacteria . J Mol Evol 57, 363–376 (2003). https://doi.org/10.1007/s00239-003-2472-z

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