Cited by 74Aquaculture disease management and microbiotaParasitic Infections and DiagnosticsProtist diversity and phylogeny

The Genome of Spironucleus salmonicida Highlights a Fish Pathogen Adapted to Fluctuating Environments

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Xu, Feifei, Jerlström-Hultqvist, Jon, Einarsson, Elin, Ástvaldsson, Ásgeir, Svärd, Staffan G., Andersson, Jan O.·2014·PLoS Genetics

Abstract

Spironucleus salmonicida causes systemic infections in salmonid fish. It belongs to the group diplomonads, binucleated heterotrophic flagellates adapted to micro-aerobic environments. Recently we identified energy-producing hydrogenosomes in S. salmonicida. Here we present a genome analysis of the fish parasite with a focus on the comparison to the more studied diplomonad Giardia intestinalis. We annotated 8067 protein coding genes in the ∼12.9 Mbp S. salmonicida genome. Unlike G. intestinalis, promoter-like motifs were found upstream of genes which are correlated with gene expression, suggesting a more elaborate transcriptional regulation. S. salmonicida can utilise more carbohydrates as energy sources, has an extended amino acid and sulfur metabolism, and more enzymes involved in scavenging of reactive oxygen species compared to G. intestinalis. Both genomes have large families of cysteine-rich membrane proteins. A cluster analysis indicated large divergence of these families in the two diplomonads. Nevertheless, one of S. salmonicida cysteine-rich proteins was localised to the plasma membrane similar to G. intestinalis variant-surface proteins. We identified S. salmonicida homologs to cyst wall proteins and showed that one of these is functional when expressed in Giardia. This suggests that the fish parasite is transmitted as a cyst between hosts. The extended metabolic repertoire and more extensive gene regulation compared to G. intestinalis suggest that the fish parasite is more adapted to cope with environmental fluctuations. Our genome analyses indicate that S. salmonicida is a well-adapted pathogen that can colonize different sites in the host.

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  • The publication of the S. salmonicida genome and the development of an efficient transfection system have enabled comprehensive molecular studies to be performed.

    “recently, the publication of the Spironucleus salmonicida genome and the development of an efficient transfection system have enabled comprehensive molecular studies to be performed (14, 15).”

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  1. [1]Adl SM, Simpson AG, Lane CE, Lukes J, Bass D, et al (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59: 429– 514. 23020233 PMC3483872
  2. [2]Brugerolle G, Lee JJ (2002) Order Diplomonadida. In: Lee JJ, Leedale GF, Bradbury P, editors. An Illustrated Guide to the Protozoa, 2nd edn. Lawrence, Kansas: Society of Protozoologists. pp. 1125–1135.
  3. [3]Tovar J, León-Avila G, Sánchez LB, Sutak R, Tachezy J, et al (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426: 172– 176. 14614504
  4. [4]Jerlström-Hultqvist J, Einarsson E, Xu F, Hjort K, Ek B, et al (2013) Hydrogenosomes in the diplomonad Spironucleus salmonicida. Nat Commun 4: 2493. 24042146 PMC3778541
  5. [5]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. 15668177
  6. [6]Cooper MA, Adam RD, Worobey M, Sterling CR (2007) Population genetics provides evidence for recombination in Giardia. Curr Biol 17: 1984– 1988. 17980591
  7. [7]Andersson JO (2012) Double peaks reveal rare diplomonad sex. Trends Parasitol 28: 46– 52. 22192817
  8. [8]Andersson JO, Sjögren ÅM, 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. 17298675 PMC1805757
  9. [9]Andersson JO, Sjögren ÅM, Davis LAM, Embley TM, Roger AJ (2003) Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol 13: 94– 104. 12546782
  10. [10]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. 17901334
  11. [11]Upcroft J, Upcroft P (1998) My favorite cell: Giardia. Bioessays 20: 256– 263. 9631653
  12. [12]Adam RD (2001) Biology of Giardia lamblia. Clin Microbiol Rev 14: 447– 475. 11432808 PMC88984
  13. [13]Ankarklev J, Jerlström-Hultqvist J, Ringqvist E, Troell K, Svärd SG (2010) Behind the smile: cell biology and disease mechanisms of Giardia species. Nat Rev Microbiol 8: 413– 422. 20400969
  14. [15]Kolisko M, Cepicka I, Hampl V, Leigh J, Roger AJ, et al (2008) 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 8: 205. 18627633 PMC2496913
  15. [17]Jørgensen A, Sterud E (2006) The marine pathogenic genotype of Spironucleus barkhanus from farmed salmonids redescribed as Spironucleus salmonicida n. sp. J Eukaryot Microbiol 53: 531– 541. 17123418
  16. [19]Jørgensen A, Torp K, Bjorland MA, Poppe TT (2011) Wild arctic char Salvelinus alpinus and trout Salmo trutta: hosts and reservoir of the salmonid pathogen Spironucleus salmonicida (Diplomonadida; Hexamitidae). Dis Aquat Organ 97: 57– 63. 22235595
  17. [20]Jerlström-Hultqvist J, Einarsson E, Svärd SG (2012) Stable transfection of the diplomonad parasite Spironucleus salmonicida. Eukaryot Cell 11: 1353– 1361. 22983987 PMC3486028
  18. [21]Franzén O, Jerlström-Hultqvist J, Castro E, Sherwood E, Ankarklev J, et al (2009) Draft genome sequencing of Giardia intestinalis assemblage B isolate GS: are human giardiasis caused by two different species? PLoS Pathog 5 (8) e1000560. 19696920 PMC2723961
  19. [22]Jerlström-Hultqvist J, Franzén O, Ankarklev J, Xu F, Nohynkova E, et al (2010) Genome analysis and comparative genomics of a Giardia intestinalis assemblage E isolate. BMC Genomics 11: 543. 20929575 PMC3091692
  20. [23]Keeling PJ, Doolittle WF (1997) Widespread and ancient distribution of a noncanonical genetic code in diplomonads. Mol Biol Evol 14: 895– 901. 9287422
  21. [24]Manning G, Reiner DS, Lauwaet T, Dacre M, Smith A, et al (2011) The minimal kinome of Giardia lamblia illuminates early kinase evolution and unique parasite biology. Genome Biol 12: R66. 21787419 PMC3218828
  22. [25]O'Connell MJ, Krien MJ, Hunter T (2003) Never say never. The NIMA-related protein kinases in mitotic control. Trends Cell Biol 13: 221– 228. 12742165
  23. [26]Collins L, Penny D (2005) Complex spliceosomal organization ancestral to extant eukaryotes. Mol Biol Evol 22: 1053– 1066. 15659557
  24. [27]Franzen O, Jerlström-Hultqvist J, Einarsson E, Ankarklev J, Ferella M, et al (2013) Transcriptome profiling of Giardia intestinalis using strand-specific RNA-seq. PLoS Comput Biol 9: e1003000. 23555231 PMC3610916
  25. [28]Kamikawa R, Inagaki Y, Tokoro M, Roger AJ, Hashimoto T (2011) Split introns in the genome of Giardia intestinalis are excised by spliceosome-mediated trans-splicing. Curr Biol 21: 311– 315. 21315596
  26. [29]Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, et al (2007) Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315: 207– 212. 17218520 PMC2080659
  27. [31]Akopian D, Shen K, Zhang X, Shan SO (2013) Signal recognition particle: an essential protein-targeting machine. Annu Rev Biochem 82: 693– 721. 23414305 PMC3805129
  28. [32]Teodorovic S, Walls CD, Elmendorf HG (2007) Bidirectional transcription is an inherent feature of Giardia lamblia promoters and contributes to an abundance of sterile antisense transcripts throughout the genome. Nucleic Acids Res 35: 2544– 2553. 17403692 PMC1885649
  29. [33]Best AA, Morrison HG, McArthur AG, Sogin ML, Olsen GJ (2004) Evolution of eukaryotic transcription: insights from the genome of Giardia lamblia. Genome Res 14: 1537– 1547. 15289474 PMC509262
  30. [34]Iyer LM, Anantharaman V, Wolf MY, Aravind L (2008) Comparative genomics of transcription factors and chromatin proteins in parasitic protists and other eukaryotes. Int J Parasitol 38: 1– 31. 17949725
  31. [35]Fuentes V, Barrera G, Sanchez J, Hernandez R, Lopez-Villasenor I (2012) Functional analysis of sequence motifs involved in the polyadenylation of Trichomonas vaginalis mRNAs. Eukaryot Cell 11: 725– 734. 22467744 PMC3370463
  32. [36]Williams CF, Vacca AR, Lloyd D, Schelkle B, Cable J (2013) Non-invasive investigation of Spironucleus vortens transmission in freshwater angelfish Pterophyllum scalare. Dis Aquat Organ 105: 211– 223. 23999705
  33. [37]Januschka MM, Erlandsen SL, Bemrick WJ, Schupp DG, Feely DE (1988) A comparison of Giardia microti and Spironucleus muris cysts in the vole: an immunocytochemical, light, and electron microscopic study. J Parasitol 74: 452– 458. 3288741
  34. [38]Wood AM, Smith HV (2005) Spironucleosis (Hexamitiasis, Hexamitosis) in the ring-necked pheasant (Phasianus colchicus): detection of cysts and description of Spironucleus meleagridis in stained smears. Avian Dis 49: 138– 143. 15839427
  35. [39]Morf L, Spycher C, Rehrauer H, Fournier CA, Morrison HG, et al (2010) The transcriptional response to encystation stimuli in Giardia lamblia is restricted to a small set of genes. Eukaryot Cell 9: 1566– 1576. 20693303 PMC2950437
  36. [40]Konrad C, Spycher C, Hehl AB (2010) Selective condensation drives partitioning and sequential secretion of cyst wall proteins in differentiating Giardia lamblia. PLoS Pathog 6: e1000835. 20386711 PMC2851657
  37. [41]Rawlings ND, Morton FR, Kok CY, Kong J, Barrett AJ (2008) MEROPS: the peptidase database. Nucleic Acids Res 36: D320– 325. 17991683 PMC2238837
  38. [42]Sajid M, McKerrow JH (2002) Cysteine proteases of parasitic organ. Mol Biochem Parasitol 120: 1– 21. 11849701
  39. [43]Adam RD, Nigam A, Seshadri V, Martens CA, Farneth GA, et al (2010) The Giardia lamblia vsp gene repertoire: characteristics, genomic organization, and evolution. BMC Genomics 11: 424. 20618957 PMC2996952
  40. [44]Nash TE, Banks SM, Alling DW, Merritt JW Jr, Conrad JT (1990) Frequency of variant antigens in Giardia lamblia. Exp Parasitol 71: 415– 421. 1699782
  41. [46]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. 17183673 PMC1762436
  42. [47]Prucca CG, Slavin I, Quiroga R, Elias EV, Rivero FD, et al (2008) Antigenic variation in Giardia lamblia is regulated by RNA interference. Nature 456: 750– 754. 19079052
  43. [48]Nixon JEJ, Wang A, Field J, Morrison HG, McArthur AG, et al (2002) Evidence for lateral transfer of genes encoding ferredoxins, nitroreductases, NADH oxidase, and alcohol dehydrogenase 3 from anaerobic prokaryotes to Giardia lamblia and Entamoeba histolytica. Eukaryot Cell 1: 181– 190. 12455953 PMC118039
  44. [49]Law CJ, Maloney PC, Wang DN (2008) Ins and outs of major facilitator superfamily antiporters. Annu Rev Microbiol 62: 289– 305. 18537473 PMC2612782
  45. [50]Davidson AL, Dassa E, Orelle C, Chen J (2008) Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72: 317– 364. 18535149 PMC2415747
  46. [51]Young GB, Jack DL, Smith DW, Saier MH Jr (1999) The amino acid/auxin: proton symport permease family. Biochim Biophys Acta 1415: 306– 322. 9889387
  47. [52]Schofield PJ, Costello M, Edwards MR, O'Sullivan WJ (1990) The arginine dihydrolase pathway is present in Giardia intestinalis. Int J Parasitol 20: 697– 699. 2228433
  48. [53]Yarlett N, Martinez MP, Moharrami MA, Tachezy J (1996) The contribution of the arginine dihydrolase pathway to energy metabolism by Trichomonas vaginalis. Mol Biochem Parasitol 78: 117– 125. 8813682
  49. [54]Lacourciere GM, Mihara H, Kurihara T, Esaki N, Stadtman TC (2000) Escherichia coli NifS-like proteins provide selenium in the pathway for the biosynthesis of selenophosphate. J Biol Chem 275: 23769– 23773. 10829016
  50. [55]Lacourciere GM (2002) Selenium is mobilized in vivo from free selenocysteine and is incorporated specifically into formate dehydrogenase H and tRNA nucleosides. J Bacteriol 184: 1940– 1946. 11889101 PMC134910
  51. [56]Haft DH, Self WT (2008) Orphan SelD proteins and selenium-dependent molybdenum hydroxylases. Biol Direct 3: 4. 18289380 PMC2276186
  52. [57]Zhang Y, Turanov AA, Hatfield DL, Gladyshev VN (2008) In silico identification of genes involved in selenium metabolism: evidence for a third selenium utilization trait. BMC Genomics 9: 251. 18510720 PMC2432076
  53. [58]Kopriva S, Patron NJ, Keeling P, Leustek T (2008) Phylogenetic analysis of sulfate assimilation and cysteine biosynthesis in phototrophic organisms. In: Hell R, Dahl C, Knaff DB, Leustek T, editors. Sulfur Metabolism in Phototrophic Organisms: Springer Netherlands. pp. 31–58.
  54. [59]Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62: 157– 184. 21370978
  55. [60]Hérbert A, Casaregola S, Beckerich J-M (2011) Biodiversity in sulfurmetabolism in hemiascomycetous yeasts. FEMS Yeast Res 11: 366– 378. 21348937
  56. [61]Payne SH, Loomis WF (2006) Retention and loss of amino acid biosynthetic pathways based on analysis of whole-genome sequences. Eukaryot Cell 5: 272– 276. 16467468 PMC1405893
  57. [62]Ma K, Adams MWW (1994) Sulfide dehydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus: a new multifunctional enzyme involved in the reduction of elemental sulfur. J Bacteriol 176: 6509– 6517. 7961401 PMC197004
  58. [63]Hagen WR, Silva PJ, Amorim MA, Hagedoorn P-L, Wassink H, et al (2000) Novel structure and redox chemistry of the prosthetic groups of the iron-sulfur flavoprotein sulfide dehydrogenase from Pyrococcus furiosus; evidence for a [2Fe-2S] cluster with Asp(Cys)3 ligands. J Biol Inorg Chem 5: 527– 534. 10968624
  59. [64]Andersson JO, Roger AJ (2002) Evolutionary analyses of the small subunit of glutamate synthase: gene order conservation, gene fusions and prokaryote-to-eukaryote lateral gene transfers. Eukaryot Cell 1: 304– 310. 12455964 PMC118040
  60. [65]Bridger SL, Clarkson SM, Stirrett K, DeBarry MB, Lipscomb GL, et al (2011) Deletion strains reveal metabolic roles for key elemental sulfur-responsive proteins in Pyrococcus furiosus. J Bacteriol 193: 6498– 6504. 21965560 PMC3232869
  61. [66]Liu Y, Beer LL, Whitman WB (2012) Sulfur metabolism in archaea reveals novel processes. Environ Microbiol 14: 2632– 2644. 22626264
  62. [67]Brown DM, Upcroft JA, Upcroft P (1995) Free radical detoxification in Giardia duodenalis. Mol Biochem Parasitol 72: 47– 56. 8538699
  63. [68]Brown DM, Upcroft JA, Upcroft P (1996) A H2O-producing NADH oxidase from the protozoan parasite Giardia duodenalis. Eur J Biochem 241: 155– 161. 8898901
  64. [69]Testa F, Mastronicola D, Cabelli DE, Bordi E, Pucillo LP, et al (2011) The superoxide reductase from the early diverging eukaryote Giardia intestinalis. Free Radic Biol Med 51: 1567– 1574. 21839165
  65. [70]Vicente JB, Testa F, Mastronicola D, Forte E, Sarti P, et al (2009) Redox properties of the oxygen-detoxifying flavodiiron protein from the human parasite Giardia intestinalis. Arch Biochem Biophys 488: 9– 13. 19545535
  66. [71]Millet CO, Cable J, Lloyd D (2010) The diplomonad fish parasite Spironucleus vortens produces hydrogen. J Eukaryot Microbiol 57: 400– 404. 20726936
  67. [73]Andersson JO, Hirt RP, Foster PG, Roger AJ (2006) Evolution of four gene families with patchy phylogenetic distribution: influx of genes into protist genomes. BMC Evol Biol 6: 27. 16551352 PMC1484493
  68. [74]Mastronicola D, Testa F, Forte E, Bordi E, Pucillo LP, et al (2010) Flavohemoglobin and nitric oxide detoxification in the human protozoan parasite Giardia intestinalis. Biochem Biophys Res Commun 399: 654– 658. 20691663
  69. [75]Jerlström-Hultqvist J, Stadelmann B, Birkestedt S, Hellman U, Svärd SG (2012) Plasmid vectors for proteomic analyses in Giardia: purification of virulence factors and analysis of the proteasome. Eukaryot Cell 11: 864– 873. 22611020 PMC3416501
  70. [76]Miller JR, Delcher AL, Koren S, Venter E, Walenz BP, et al (2008) Aggressive assembly of pyrosequencing reads with mates. Bioinformatics 24: 2818– 2824. 18952627 PMC2639302
  71. [77]Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754– 1760. 19451168 PMC2705234
  72. [79]Nawrocki EP, Kolbe DL, Eddy SR (2009) Infernal 1.0: inference of RNA alignments. Bioinformatics 25: 1335– 1337. 19307242 PMC2732312
  73. [80]Consortium U (2012) Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 40: D71– 75. 22102590 PMC3245120
  74. [81]Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078– 2079. 19505943 PMC2723002
  75. [82]Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, et al (2008) Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol 9: R7. 18190707 PMC2395244
  76. [83]Majoros WH, Pertea M, Salzberg SL (2004) TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20: 2878– 2879. 15145805
  77. [84]Hyatt D, Chen GL, Locascio PF, Land ML, Larimer FW, et al (2010) Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11: 119. 20211023 PMC2848648
  78. [85]Delcher AL, Bratke KA, Powers EC, Salzberg SL (2007) Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 23: 673– 679. 17237039 PMC2387122
  79. [87]Selengut JD, Haft DH, Davidsen T, Ganapathy A, Gwinn-Giglio M, et al (2007) TIGRFAMs and Genome Properties: tools for the assignment of molecular function and biological process in prokaryotic genomes. Nucleic Acids Res 35: D260– 264. 17151080 PMC1781115
  80. [88]UniProt C (2012) Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 40: D71– 75. 22102590 PMC3245120
  81. [89]Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, et al (2000) Artemis: sequence visualization and annotation. Bioinformatics 16: 944– 945. 11120685
  82. [90]Aurrecoechea C, Brestelli J, Brunk BP, Carlton JM, Dommer J, et al (2009) GiardiaDB and TrichDB: integrated genomic resources for the eukaryotic protist pathogens Giardia lamblia and Trichomonas vaginalis. Nucleic Acids Res 37: D526– 530. 18824479 PMC2686445
  83. [91]Li L, Stoeckert CJ Jr, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178– 2189. 12952885 PMC403725
  84. [92]Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, et al (2005) ACT: the Artemis Comparison Tool. Bioinformatics 21: 3422– 3423. 15976072
  85. [93]Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 33: W686– 689. 15980563 PMC1160127
  86. [94]Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, et al (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35: 3100– 3108. 17452365 PMC1888812
  87. [95]Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28– 36. 7584402
  88. [96]Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28: 511– 515. 20436464 PMC3146043
  89. [97]Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113. 15318951 PMC517706
  90. [98]Beauregard-Racine J, Bicep C, Schliep K, Lopez P, Lapointe FJ, et al (2011) Of woods and webs: possible alternatives to the tree of life for studying genomic fluidity in E. coli. Biol Direct 6: 39. 21774799 PMC3160433
  91. [99]Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35: W182– 185. 17526522 PMC1933193
  92. [100]Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567– 580. 11152613
  93. [101]Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189– 1191. 19151095 PMC2672624

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  • Comparative Cell Biology and Evolution of Annexins in Diplomonads

    Einarsson, E., Ástvaldsson, Á., Hultenby, K., Andersson, J. O., Svärd, S. G., & Jerlström-Hultqvist, J. (2016) · mSphere · doi:10.1128/msphere.00032-15 · Cited by 15 · see citing works

    “Nothing is known about the biological role of annexins in Spironucleus, but recently, the publication of the Spironucleus salmonicida genome and the development of an efficient transfection system have enabled comprehensive molecular studies to be performed (14, 15).”
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Authors
Xu, F., Jerlström-Hultqvist, J., Einarsson, E., Ástvaldsson, Á., Svärd, S. G., & Andersson, J. O.
Affiliations
Uppsala University (SE)
Corresponding author
Andersson, Jan O.
Venue
PLoS Genetics
Published
2014-02-06
Volume
10
Issue
2
Pages
e1004053
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
OpenAlex
W1983101378
Cited by
74
References
5
Citations by year
2026: 3 · 2025: 4 · 2024: 9 · 2023: 3 · 2022: 6 · 2021: 6 · 2020: 5 · 2019: 9 · 2018: 6 · 2017: 6 · 2016: 7 · 2015: 6 · 2014: 4
FWCI
3.50
Type
journal article
Language
en
Open access
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • KTH Publication Database DiVA (KTH Royal Institute of Technology) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • Svenska Forskningsrådet Formas (2010-899)
  • Vetenskapsrådet
  • Akademiska Sjukhuset
  • Uppsala Universitet
  • Science for Life Laboratory
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
  • Life Sciences › Immunology and Microbiology › Parasitology › Parasitic Infections and Diagnostics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
Keywords
diplomonads, Giardia lamblia, genome annotation, hydrogenosomes, transcriptional regulation, carbohydrate metabolism, sulfur metabolism, reactive oxygen species scavenging, cyst wall proteins, variant surface proteins, fish pathogens, metabolic adaptation
MeSH terms
Animals, Environment, Fishes, Host-Parasite Interactions, Phylogeny, Promoter Regions, Genetic, Genome, Diplomonadida, Reactive Oxygen Species, Sequence Analysis, DNA, Molecular Sequence Annotation

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