Large genomic differences between the morphologically indistinguishable diplomonads Spironucleus barkhanus and Spironucleus salmonicida

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Roxström Lindquist, Katarina ^a   Jerlström Hultqvist, Jon ^a   Jørgensen, Anders ^b   Troell, Karin ^a   Svärd, Staffan G ^a   Andersson, Jan O ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b NORWEGIAN VETERINARY INSTITUTE   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC DNA; OXYGEN; SELENOCYSTEINE;

ARTICLE; CODON USAGE; COMMENSAL; CONTROLLED STUDY; DIPLOMONADIDA; EUKARYOTE EVOLUTION; EXPRESSED SEQUENCE TAG; FISH; FLAGELLUM; FLOW CYTOMETRY; GENE DUPLICATION; GENE FREQUENCY; GENETIC CODE; GENETIC SELECTION; GENETIC VARIABILITY; GENOME SIZE; GIARDIA LAMBLIA; HAPLOIDY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PLOIDY; SPECIES DIFFERENCE; SPECIES IDENTIFICATION; UNINDEXED SEQUENCE; AMINO ACID SEQUENCE; ANIMAL; CLASSIFICATION; CYTOLOGY; GENETICS; GENOME; MOLECULAR GENETICS; PARASITOLOGY; SALMONID; SEQUENCE ALIGNMENT;

DIPLOMONADIDA; EUKARYOTA; GIARDIA INTESTINALIS; PROTISTA; SPIRONUCLEUS; SPIRONUCLEUS BARKHANUS;

AMINO ACID SEQUENCE; ANIMALS; DIPLOMONADIDA; GENOME; MOLECULAR SEQUENCE DATA; SALMONIDAE; SEQUENCE ALIGNMENT;

EID: 77951056014     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-258     Document Type: Article

References (67)

1. McGrath CL, Katz LA. Genome diversity in microbial eukaryotes. Trends Ecol Evol 2004, 19:32-38. 10.1016/j.tree.2003.10.007, 16701223.
2. Schurko AM, Neiman M, Logsdon JM. Signs of sex: what we know and how we know it. Trends Ecol Evol 2009, 24:208-217. 10.1016/j.tree.2008.11.010, 19282047.
3. Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, et al. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 2005, 52:399-451. 10.1111/j.1550-7408.2005.00053.x, 16248873.
4. Kolisko M, Cepicka I, Hampl V, Leigh J, Roger AJ, Kulda J, Simpson AG, Flegr J. Molecular phylogeny of diplomonads and enteromonads based on SSU rRNA, alpha-tubulin and HSP90 genes: implications for the evolutionary history of the double karyomastigont of diplomonads. BMC Evol Biol 2008, 8:205. 10.1186/1471-2148-8-205, 2496913, 18627633.
5. Brugerolle G, Lee JJ. Order Diplomonadida. An Illustrated Guide to the Protozoa 2002, 1125-1135. Lawrence, Kansas: Society of Protozoologists, Lee JJ, Leedale GF, Bradbury P, 2.
6. Monis PT, Caccio SM, Thompson RC. Variation in Giardia : towards a taxonomic revision of the genus. Trends Parasitol 2009, 25:93-100. 10.1016/j.pt.2008.11.006, 19135417.
7. Franzén O, Jerlström-Hultqvist J, Castro E, Sherwood E, Ankarklev J, Reiner D, Palm D, Andersson JO, Andersson B, Svärd S. Draft genome sequencing of Giardia intestinalis assemblage B isolate GS: are human giardiasis caused by two different species?. PLoS Pathog 2009, 5(8).
8. Kolisko M, Cepicka I, Hampl V, Kulda J, Flegr J. The phylogenetic position of enteromonads: a challenge for the present models of diplomonad evolution. Int J Syst Evol Microbiol 2005, 55:1729-1733. 10.1099/ijs.0.63542-0, 16014510.
9. Jørgensen A, Sterud E. Phylogeny of Spironucleus (Eopharyngia: Diplomonadida: Hexamitinae). Protist 2007, 158:247-254. 10.1016/j.protis.2006.12.003, 17292667.
10. Sterud E, Poppe TT, Bornø G. Intracellular infection with Spironucleus barkhanus (Diplomonadida, Hexamitidae) in farmed Arctic char Salvelinus alpinus. Dis Aquat Organ 2003, 56:155-161. 10.3354/dao056155, 14598991.
11. Jørgensen A, Sterud E. The marine pathogenic genotype of Spironucleus barkhanus from farmed salmonids redescribed as Spironucleus salmonicida n. sp. J Eukaryot Microbiol 2006, 53:531-541. 10.1111/j.1550-7408.2006.00144.x, 17123418.
12. Kent ML, Ellis J, Fournie JW, Dawe SC, Bagshaw JW, Whitaker DJ. Systemic hexamitid (Protozoa, Diplomonadida) infection in seawater pen-reared Chinook salmon Oncorhynchus tshawytscha. Dis Aquat Organ 1992, 14:81-89.
13. Poppe TT, Mo TA, Iversen L. Disseminated hexamitosis in sea-caged Atlantic salmon Salmo salar. Dis Aquat Organ 1992, 14:91-97.
14. Andersson JO, Sjögren T, Horner DS, Murphy CA, Dyal PL, Svärd SG, Logsdon JM, Ragan MA, Hirt RP, Roger AJ. A genomic survey of the fish parasite Spironucleus salmonicida indicates genomic plasticity among diplomonads and significant lateral gene transfer in eukaryote genome evolution. BMC Genomics 2007, 8:51. 10.1186/1471-2164-8-51, 1805757, 17298675.
15. Joint Genome Institute - Spironucleus vortens genome project. , http://genome.jgi-psf.org/Spivo0/Spivo0.info.html
16. Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, et al. Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 2007, 317:1921-1926. 10.1126/science.1143837, 17901334.
17. Keeling PJ, Doolittle WF. Widespread and ancient distribution of a noncanonical genetic code in diplomonads. Mol Biol Evol 1997, 14:895-901.
18. Bernander R, Palm JE, Svärd SG. Genome ploidy in different stages of the Giardia lamblia life cycle. Cell Microbiol 2001, 3:55-62. 10.1046/j.1462-5822.2001.00094.x, 11207620.
19. Yu LZ, Birky JCW, Adam RD. The two nuclei of Giardia each have complete copies of the genome and are partitioned equationally at cytokinesis. Eukaryot Cell 2002, 1:191-199. 10.1128/EC.1.2.191-199.2002, 118032, 12455954.
20. Mark Welch D, Meselson M. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 2000, 288:1211-1215. 10.1126/science.288.5469.1211, 10817991.
21. Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, Olsen GJ, Best AA, Cande WZ, Chen F, Cipriano MJ, et al. Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 2007, 317:1921-1926. 10.1126/science.1143837, 17901334.
22. Poxleitner MK, Carpenter ML, Mancuso JJ, Wang CJ, Dawson SC, Cande WZ. Evidence for karyogamy and exchange of genetic material in the binucleate intestinal parasite Giardia intestinalis. Science 2008, 319:1530-1533. 10.1126/science.1153752, 18339940.
23. Adam RD. Biology of Giardia lamblia. Clin Microbiol Rev 2001, 14:447-475. 10.1128/CMR.14.3.447-475.2001, 88984, 11432808.
24. Biagini GA, Yarlett N, Ball GE, Billetz AC, Lindmark DG, Martinez MP, Lloyd D, Edwards MR. Bacterial-like energy metabolism in the amitochondriate protozoon Hexamita inflata. Mol Biochem Parasitol 2003, 128:11-19. 10.1016/S0166-6851(03)00025-2, 12706792.
25. Andersson JO, Hirt RP, Foster PG, Roger AJ. Evolution of four gene families with patchy phylogenetic distribution: influx of genes into protist genomes. BMC Evol Biol 2006, 6:27. 10.1186/1471-2148-6-27, 1484493, 16551352.
26. Nash TE. Surface antigenic variation in Giardia lamblia. Mol Microbiol 2002, 45:585-590. 10.1046/j.1365-2958.2002.03029.x, 12139606.
27. Weiland ME, McArthur AG, Morrison HG, Sogin ML, Svärd SG. Annexin-like alpha giardins: a new cytoskeletal gene family in Giardia lamblia. Int J Parasitol 2005, 35:617-626. 10.1016/j.ijpara.2004.12.009, 15862575.
28. Field J, Rosenthal B, Samuelson J. Early lateral transfer of genes encoding malic enzyme, acetyl-CoA synthetase and alcohol dehydrogenases from anaerobic prokaryotes to Entamoeba histolytica. Mol Microbiol 2000, 38:446-455. 10.1046/j.1365-2958.2000.02143.x, 11069669.
29. Andersson JO, Sjögren T, Davis LAM, Embley TM, Roger AJ. Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol 2003, 13:94-104. 10.1016/S0960-9822(03)00003-4, 12546782.
30. Andersson JO. Gene transfer and diversification of microbial eukaryotes. Annu Rev Microbiol 2009, 63:177-193. 10.1146/annurev.micro.091208.073203, 19575565.
31. Romero H, Zhang Y, Gladyshev VN, Salinas G. Evolution of selenium utilization traits. Genome Biol 2005, 6:R66. 10.1186/gb-2005-6-8-r66, 1273633, 16086848.
32. Erpin project. , http://tagc.univ-mrs.fr/erpin/
33. Gautheret D, Lambert A. Direct RNA motif definition and identification from multiple sequence alignments using secondary structure profiles. J Mol Biol 2001, 313:1003-1011. 10.1006/jmbi.2001.5102, 11700055.
34. Zhang Y, Romero H, Salinas G, Gladyshev VN. Dynamic evolution of selenocysteine utilization in bacteria: a balance between selenoprotein loss and evolution of selenocysteine from redox active cysteine residues. Genome Biol 2006, 7:17.
35. Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q, Wortman JR, Bidwell SL, Alsmark UC, Besteiro S, et al. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 2007, 315:207-212. 10.1126/science.1132894, 2080659, 17218520.
36. Que X, Svärd SG, Meng TC, Hetsko ML, Aley SB, Gillin FD. Developmentally regulated transcripts and evidence of differential mRNA processing in Giardia lamblia. Mol Biochem Parasitol 1996, 81:101-110. 10.1016/0166-6851(96)02698-9, 8892309.
37. Mazumder B, Seshadri V, Fox PL. Translational control by the 3'-UTR: the ends specify the means. Trends Biochem Sci 2003, 28:91-98. 10.1016/S0968-0004(03)00002-1, 12575997.
38. Chen SL, Lee W, Hottes AK, Shapiro L, McAdams HH. Codon usage between genomes is constrained by genome-wide mutational processes. Proc Natl Acad Sci USA 2004, 101:3480-3485. 10.1073/pnas.0307827100, 373487, 14990797.
39. Knight RD, Freeland SJ, Landweber LF. A simple model based on mutation and selection explains trends in codon and amino-acid usage and GC composition within and across genomes. Genome Biol 2001, 2:0010.
40. Lafay B, Sharp PM. Synonymous codon usage variation among Giardia lamblia genes and isolates. Mol Biol Evol 1999, 16:1484-1495.
41. Novembre JA. Accounting for background nucleotide composition when measuring codon usage bias. Mol Biol Evol 2002, 19:1390-1394.
42. Marth GT, Korf I, Yandell MD, Yeh RT, Gu Z, Zakeri H, Stitziel NO, Hillier L, Kwok PY, Gish WR. A general approach to single-nucleotide polymorphism discovery. Nat Genet 1999, 23:452-456. 10.1038/70570, 10581034.
43. Qiu XY, Wu LY, Huang HS, McDonel PE, Palumbo AV, Tiedje JM, Zhou JZ. Evaluation of PCR-generated chimeras: mutations, and heteroduplexes with 16S rRNA gene-based cloning. Appl Environ Microbiol 2001, 67:880-887. 10.1128/AEM.67.2.880-887.2001, 92662, 11157258.
44. Dawson SC, Pham JK, House SA, Slawson EE, Cronembold D, Cande WZ. Stable transformation of an episomal protein-tagging shuttle vector in the piscine diplomonad Spironucleus vortens. BMC Microbiol 2008, 8:71. 10.1186/1471-2180-8-71, 2386477, 18445284.
45. National Center for Biotechnology Information. , http://www.ncbi.nlm.nih.gov/
46. Caccio SM, Ryan U. Molecular epidemiology of giardiasis. Mol Biochem Parasitol 2008, 160:75-80. 10.1016/j.molbiopara.2008.04.006, 18501440.
47. Lebbad M, Ankarklev J, Tellez A, Leiva B, Andersson JO, Svärd S. Dominance of Giardia assemblage B in Leon, Nicaragua. Acta Trop 2008, 106:44-53. 10.1016/j.actatropica.2008.01.004, 18325480.
48. Fan JB, Korman SH, Cantor CR, Smith CL. Giardia lamblia : haploid genome size determined by pulsed field gel electrophoresis is less than 12 Mb. Nucleic Acids Res 1991, 19:1905-1908. 10.1093/nar/19.8.1905, 328122, 2030969.
49. Ramesh MA, Malik SB, Logsdon JM. A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr Biol 2005, 15:185-191.
50. Cooper MA, Adam RD, Worobey M, Sterling CR. Population genetics provides evidence for recombination in Giardia. Curr Biol 2007, 17:1984-1988. 10.1016/j.cub.2007.10.020, 17980591.
51. Keister DB. Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 1983, 77:487-488. 10.1016/0035-9203(83)90120-7, 6636276.
52. Jørgensen A, Sterud E. SSU rRNA gene sequence reveals two genotypes of Spironucleus barkhanus (Diplomonadida) from farmed and wild Arctic charr Salvelinus alpinus. Dis Aquat Organ 2004, 62:93-96. 10.3354/dao062093, 15648835.
53. Laboratory of Phil Green. , http://www.phrap.org/
54. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004, 14:1188-1190. 10.1101/gr.849004, 419797, 15173120.
55. DOE Joint Genome Institute. , http://www.jgi.doe.gov/
56. O'Brien EA, Koski LB, Zhang Y, Yang L, Wang E, Gray MW, Burger G, Lang BF. TBestDB: a taxonomically broad database of expressed sequence tags (ESTs). Nucleic Acids Res 2007, 35:D445-451. 10.1093/nar/gkl770, 1899108, 17202165.
57. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402. 10.1093/nar/25.17.3389, 146917, 9254694.
58. Frickey T, Lupas AN. PhyloGenie: automated phylome generation and analysis. Nucleic Acids Res 2004, 32:5231-5238. 10.1093/nar/gkh867, 521674, 15459293.
59. ModelGenerator: amino acid and nucleotide substitution model selection. , http://bioinf.nuim.ie/software/modelgenerator
60. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22:2688-2690. 10.1093/bioinformatics/btl446, 16928733.
61. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755. 10.1093/bioinformatics/17.8.754, 11524383.
62. Supek F, Vlahovicek K. INCA: synonymous codon usage analysis and clustering by means of self-organizing map. Bioinformatics 2004, 20:2329-2330. 10.1093/bioinformatics/bth238, 15059815.
63. Correspondence analysis of codon usage. , http://codonw.sourceforge.net/
64. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 1997, 25:4876-4882. 10.1093/nar/25.24.4876, 147148, 9396791.
65. Bininda-Emonds OR. transAlign: using amino acids to facilitate the multiple alignment of protein-coding DNA sequences. BMC Bioinformatics 2005, 6:156.
66. Yang Z, Nielsen R. Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol 2000, 17:32-43.
67. Yang Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007, 24:1586-1591. 10.1093/molbev/msm088, 17483113.