Draft genome sequencing of Giardia intestinalis assemblage B isolate GS: Is human giardiasis caused by two different species?

PLoS Pathogens

Volumn 5, Issue 8, 2009, Pages

  Franzén, Oscar ^a   Jerlström Hultqvist, Jon ^b   Castro, Elsie ^c   Sherwood, Ellen ^a   Ankarklev, Johan ^b   Reiner, David S ^d   Palm, Daniel ^c   Andersson, Jan O ^e   Andersson, Björn ^a   Svärd, Staffan G ^b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^d BURNHAM INSTITUTE   (United States)

^e UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; MEMBRANE PROTEIN; MEMBRANE PROTEIN HCMP; NUCLEOTIDE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; MESSENGER RNA; PROTOZOAL PROTEIN; PROTOZOAL RNA;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA POLYMORPHISM; GENE FREQUENCY; GENE SEQUENCE; GENOME; GENOMICS; GIARDIA LAMBLIA; GIARDIASIS; HETEROZYGOSITY; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE ISOLATION; PROMOTER REGION; SYNTENY; TETRAPLOIDY; ANIMAL; BACTERIAL GENOME; CLASSIFICATION; GENETIC POLYMORPHISM; GENETICS; HUMAN; INTRON; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; PHYLOGENY; PORPHYROMONAS GINGIVALIS; RNA SPLICING; SEQUENCE ALIGNMENT;

ANIMALIA; GIARDIA; GIARDIA INTESTINALIS;

ANIMALS; BASE SEQUENCE; GENE FREQUENCY; GENOME, BACTERIAL; GENOME, PROTOZOAN; GIARDIA LAMBLIA; GIARDIASIS; HUMANS; INTRONS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, GENETIC; PORPHYROMONAS GINGIVALIS; PROMOTER REGIONS, GENETIC; PROTOZOAN PROTEINS; RNA SPLICING; RNA, MESSENGER; RNA, PROTOZOAN; SEQUENCE ALIGNMENT; SYNTENY;

EID: 70049088650     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000560     Document Type: Article

References (83)

1. Adam RD (2001) Biology of Giardia lamblia. Clin Microbiol Rev 14: 447-475.
2. Caccio SM, Ryan U (2008) Molecular epidemiology of giardiasis. Mol Biochem Parasitol 160: 75-80.
3. Farthing MJ (1997) The molecular pathogenesis of giardiasis. J Pediatr Gastroenterol Nutr 24: 79-88.
4. Buret AG (2007) Mechanisms of epithelial dysfunction in giardiasis. Gut 56: 316-317.
5. Gilman RH, Marquis GS, Miranda E, Vestegui M, Martinez H (1988) Rapid reinfection by Giardia lamblia after treatment in a hyperendemic Third World community. Lancet 1: 343-345. (Pubitemid 18057770)
6. Homan WL, Mank TG (2001) Human giardiasis: genotype linked differences in clinical symptomatology. Int J Parasitol 31: 822-826. (Pubitemid 32524167)
7. Read C, Walters J, Robertson ID, Thompson RC (2002) Correlation between genotype of Giardia duodenalis and diarrhoea. Int J Parasitol 32: 229-231. (Pubitemid 34112630)
8. Haque R, Roy S, Kabir M, Stroup SE, Mondal D, et al. (2005) Giardia assemblage A infection and diarrhea in Bangladesh. J Infect Dis 192: 2171-2173. (Pubitemid 41779218)
9. Bernander R, Palm JE, Svard SG (2001) Genome ploidy in different stages of the Giardia lamblia life cycle. Cell Microbiol 3: 55-62. (Pubitemid 32107426)
10. Lu SQ, Baruch AC, Adam RD (1998) Molecular comparison of Giardia lamblia isolates. Int J Parasitol 28: 1341-1345.
11. Teodorovic S, Braverman JM, Elmendorf HG (2007) Unusually low levels of genetic variation among Giardia lamblia isolates. Eukaryot Cell 6: 1421-1430. (Pubitemid 47257711)
12. von Allmen N, Bienz M, Hemphill A, Muller N (2005) Quantitative assessment of sense and antisense transcripts from genes involved in antigenic variation (vsp genes) and encystation (cwp 1 gene) of Giardia lamblia clone GS/M-83-H7. Parasitology 130: 389-396. (Pubitemid 40516288)
13. Bienz M, Siles-Lucas M, Muller N (2001) Use of a novel DNA melting profile assay for the identification of PCR-amplified genomic sequences encoding for variant-specific surface proteins from the clonal GS/M-83-H7 line of Giardia lamblia. Parasitol Res 87: 1011-1015. (Pubitemid 33036144)
14. Nash TE (2002) Surface antigenic variation in Giardia lamblia. Mol Microbiol 45: 585-590.
15. Nash TE, Herrington DA, Losonsky GA, Levine MM (1987) Experimental human infections with Giardia lamblia. J Infect Dis 156: 974-984. (Pubitemid 18017076)
16. Byrd LG, Conrad JT, Nash TE (1994) Giardia lamblia infections in adult mice. Infect Immun 62: 3583-3585.
17. Nash TE, McCutchan T, Keister D, Dame JB, Conrad JD, et al. (1985) Restriction-endonuclease analysis of DNA from 15 Giardia isolates obtained from humans and animals. J Infect Dis 152: 64-73. (Pubitemid 15038835)
18. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, et al. (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415. (Pubitemid 40994675)
19. Carlton JM, Escalante AA, Neafsey D, Volkman SK (2008) Comparative evolutionary genomics of human malaria parasites. Trends Parasitol 24: 545-550.
20. Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, et al. (2007) Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317: 1921-1926.
21. Droege M, Hill B (2008) The Genome Sequencer FLX System - longer reads, more applications, straight forward bioinformatics and more complete data sets. J Biotechnol 136: 3-10.
22. Wheeler DA, Srinivasan M, Egholm M, Shen Y, Chen L, et al. (2008) The complete genome of an individual by massively parallel DNA sequencing. Nature 452: 872-876. (Pubitemid 351550870)
23. Green RE, Malaspinas AS, Krause J, Briggs AW, Johnson PL, et al. (2008) A complete Neandertal mitochondrial genome sequence determined by high-throughput sequencing. Cell 134: 416-426.
24. Pearson BM, Gaskin DJ, Segers RP, Wells JM, Nuijten PJ, et al. (2007) The complete genome sequence of Campylobacter jejuni strain 81116 (NCTC11828). J Bacteriol 189: 8402-8403. (Pubitemid 350178958)
25. Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, et al. (1996) Life with 6000 genes. Science 274: 546563-547547
26. Katinka MD, Duprat S, Cornillot E, Metenier G, Thomarat F, et al. (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414: 450-453. (Pubitemid 34173726)
27. Abrahamsen MS, Templeton TJ, Enomoto S, Abrahante JE, Zhu G, et al. (2004) Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304: 441-445.
28. Gibbs MJ, Smeianov VV, Steele JL, Upcroft P, Efimov BA (2006) Two families of rep-like genes that probably originated by interspecies recombination are represented in viral, plasmid, bacterial, and parasitic protozoan genomes. Mol Biol Evol 23: 1097-1100. (Pubitemid 43781582)
29. Kinane DF, Galicia JC, Gorr SU, Stathopoulou PG, Benakanakere M (2008) P. gingivalis interactions with epithelial cells. Front Biosci 13: 966-984.
30. Mark Welch D, Meselson M (2000) Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288: 1211-1215.
31. Lebbad M, Ankarklev J, Tellez A, Leiva B, Andersson JO, et al. (2008) Dominance of Giardia assemblage B in Leon, Nicaragua. Acta Trop 106: 44-53.
32. Elmendorf HG, Singer SM, Pierce J, Cowan J, Nash TE (2001) Initiator and upstream elements in the alpha2-tubulin promoter of Giardia lamblia. Mol Biochem Parasitol 113: 157-169. (Pubitemid 32209292)
33. Knodler LA, Svard SG, Silberman JD, Davids BJ, Gillin FD (1999) Developmental gene regulation in Giardia lamblia: first evidence for an encystation-specific promoter and differential 5′ mRNA processing. Mol Microbiol 34: 327-340.
34. Huang YC, Su LH, Lee GA, Chiu PW, Cho CC, et al. (2008) Regulation of cyst wall protein promoters by Myb2 in Giardia lamblia. J Biol Chem 283: 31021-31029.
35. Lopez AB, Sener K, Trosien J, Jarroll EL, van Keulen H (2007) UDP-N-acetylglucosamine 4′-epimerase from the intestinal protozoan Giardia intestinalis lacks UDP-glucose 4′-epimerase activity. J Eukaryot Microbiol 54: 154-160. (Pubitemid 46525396)
36. von Allmen N, Bienz M, Hemphill A, Muller N (2004) Experimental infections of neonatal mice with cysts of Giardia lamblia clone GS/M-83-H7 are associated with an antigenic reset of the parasite. Infect Immun 72: 4763-4771. (Pubitemid 38989337)
37. Chen XS, White WT, Collins LJ, Penny D (2008) Computational identification of four spliceosomal snRNAs from the deep-branching eukaryote Giardia intestinalis. PLoS ONE 3: e3106. doi:10.1371/journal.pone.0003106.
38. Nash TE, Mowatt MR (1992) Characterization of a Giardia lamblia variant-specific surface protein (VSP) gene from isolate GS/M and estimation of the VSP gene repertoire size. Mol Biochem Parasitol 51: 219-227.
39. Bienz M, Siles-Lucas M, Wittwer P, Muller N (2001) vsp gene expression by Giardia lamblia clone GS/M-83-H7 during antigenic variation in vivo and in vitro. Infect Immun 69: 5278-5285. (Pubitemid 32786458)
40. Davids BJ, Reiner DS, Birkeland SR, Preheim SP, Cipriano MJ, et al. (2006) A new family of giardial cysteine-rich non-VSP protein genes and a novel cyst protein. PLoS ONE 1: e44. doi:10.1371/journal.pone.0000044.
41. Weiland ME, McArthur AG, Morrison HG, Sogin ML, Svard SG (2005) Annexin-like alpha giardins: a new cytoskeletal gene family in Giardia lamblia. Int J Parasitol 35: 617-626.
42. Steuart RF, O'Handley R, Lipscombe RJ, Lock RA, Thompson RC (2008) Alpha 2 giardin is an assemblage A-specific protein of human infective Giardia duodenalis. Parasitology 135: 1621-1627.
43. Brown DM, Upcroft JA, Edwards MR, Upcroft P (1998) Anaerobic bacterial metabolism in the ancient eukaryote Giardia duodenalis. Int J Parasitol 28: 149-164.
44. Field J, Rosenthal B, Samuelson J (2000) Early lateral transfer of genes encoding malic enzyme, acetyl-CoA synthetase and alcohol dehydrogenases from anaerobic prokaryotes to Entamoeba histolytica. Mol Microbiol 38: 446-455. (Pubitemid 30947459)
45. Andersson JO, Sjogren AM, Davis LA, Embley TM, Roger AJ (2003) Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol 13: 94-104.
46. Andersson JO, Sjogren AM, Horner DS, Murphy CA, Dyal PL, et al. (2007) 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 8: 51.
47. Hopkins AL, Groom CR (2002) The druggable genome. Nat Rev Drug Discov 1: 727-730.
48. Chen YH, Su LH, Huang YC, Wang YT, Kao YY, et al. (2008) UPF1, a conserved nonsense-Mmediated mRNA decay factor, regulates cyst wall protein transcripts in Giardia lamblia. PLoS ONE 3: e3609.
49. Blakesley RW, Hansen NF, Mullikin JC, Thomas PJ, McDowell JC, et al. (2004) An intermediate grade of finished genomic sequence suitable for comparative analyses. Genome Res 14: 2235-2244.
50. Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9: 605-618.
51. Andersson JO (2009) Gene transfer and diversification of microbial eukaryotes. Ann Rev Microbiol 63: in press.
52. Cooper MA, Adam RD, Worobey M, Sterling CR (2007) Population genetics provides evidence for recombination in Giardia. Curr Biol 17: 1984-1988. (Pubitemid 350088486)
53. Poxleitner MK, Carpenter ML, Mancuso JJ, Wang CJ, Dawson SC, et al. (2008) Evidence for karyogamy and exchange of genetic material in the binucleate intestinal parasite Giardia intestinalis. Science 319: 1530-1533.
54. Melo SP, Gomez V, Castellanos IC, Alvarado ME, Hernandez PC, et al. (2008) Transcription of meiotic-like-pathway genes in Giardia intestinalis. Mem Inst Oswaldo Cruz 103: 347-350. (Pubitemid 352026439)
55. Ramesh MA, Malik SB, Logsdon JM Jr (2005) A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr Biol 15: 185-191.
56. Malik SB, Pightling AW, Stefaniak LM, Schurko AM, Logsdon JM Jr (2008) An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. PLoS ONE 3: e2879.
57. Reiner DS, Ankarklev J, Troell K, Palm D, Bernander R, et al. (2008) Synchronisation of Giardia lamblia: identification of cell cycle stage-specific genes and a differentiation restriction point. Int J Parasitol 38: 935-944.
58. Karanis P, Ey PL (1998) Characterization of axenic isolates of Giardia intestinalis established from humans and animals in Germany. Parasitol Res 84: 442-449. (Pubitemid 28257172)
59. Svard SG, Meng TC, Hetsko ML, McCaffery JM, Gillin FD (1998) Differentiation-associated surface antigen variation in the ancient eukaryote Giardia lamblia. Mol Microbiol 30: 979-989.
60. Chen N, Upcroft JA, Upcroft P (1995) A Giardia duodenalis gene encoding a protein with multiple repeats of a toxin homologue. Parasitology 111(Pt 4): 423-431.
61. Mayrhofer G, Andrews RH, Ey PL, Chilton NB (1995) Division of Giardia isolates from humans into two genetically distinct assemblages by electrophoretic analysis of enzymes encoded at 27 loci and comparison with Giardia muris. Parasitology 111(Pt 1): 11-17.
62. De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56: 879-886.
63. Cracraft J (1983) Species concepts and speciation analysis. Curr Ornithol 1: 159-187.
64. Nixon KC, W QD (1990) An amplification of the phylogenetic species concept. Cladistics 6: 211-223.
65. Rosen DE (1979) Fishes from the uplands and intermontane basins of Guatemala: revisionary studies and comparative geography. BullAmMusNatHist 162: 267-376.
66. Singer SM, Yee J, Nash TE (1998) Episomal and integrated maintenance of foreign DNA in Giardia lamblia. Mol Biochem Parasitol 92: 59-69. (Pubitemid 28159987)
67. Tumova P, Hofstetrova K, Nohynkova E, Hovorka O, Kral J (2007) Cytogenetic evidence for diversity of two nuclei within a single diplomonad cell of Giardia. Chromosoma 116: 65-78. (Pubitemid 46179023)
68. Adam RD (1992) Chromosome-size variation in Giardia lamblia: the role of rDNA repeats. Nucleic Acids Res 20: 3057-3061.
69. Monis PT, Caccio SM, Thompson RC (2009) Variation in Giardia: towards a taxonomic revision of the genus. Trends Parasitol 25: 93-100.
70. Ringqvist E, Palm JE, Skarin H, Hehl AB, Weiland M, et al. (2008) Release of metabolic enzymes by Giardia in response to interaction with intestinal epithelial cells. Mol Biochem Parasitol 159: 85-91. (Pubitemid 351621902)
71. Ewing B, Green P (1998) Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8: 186-194.
72. Chevreux B, Wetter T, Suhai S (1999) Genome Sequence Assembly Using Trace Signals and Additional Sequence Information Computer Science and Biology. pp 45-56.
73. Delcher AL, Harmon D, Kasif S, White O, Salzberg SL (1999) Improved microbial gene identification with GLIMMER. Nucleic Acids Res 27: 4636-4641.
74. Badger JH, Olsen GJ (1999) CRITICA: coding region identification tool invoking comparative analysis. Mol Biol Evol 16: 512-524.
75. Field D, Garrity G, Gray T, Morrison N, Selengut J, et al. (2008) The minimum information about a genome sequence (MIGS) specification. Nat Biotechnol 26: 541-547. (Pubitemid 351668038)
76. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J (2005) ACT: the Artemis Comparison Tool. Bioinformatics 21: 3422-3423.
77. Pan X, Stein L, Brendel V (2005) SynBrowse: a synteny browser for comparative sequence analysis. Bioinformatics 21: 3461-3468. (Pubitemid 41235988)
78. Rice P, Longden I, Bleasby A (2000) EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
79. Olson SA (2002) EMBOSS opens up sequence analysis. European Molecular Biology Open Software Suite. Brief Bioinform 3: 87-91.
80. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955-964.
81. Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics Chapter 2: Unit 2 3.
82. Keane TM, Naughton TJ, McInerney JO (2004) ModelGenerator: amino acid and nucleotide substitution model selection.
83. 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)