Differential locus expansion distinguishes Toxoplasmatinae species and closely related strains of Toxoplasma gondii

mBio

Volumn 5, Issue 1, 2014, Pages

  Adomako Ankomah, Yaw ^a   Wier, Gregory M ^a   Borges, Adair L ^a   Wand, Hannah E ^a   Boyle, Jon P ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE ANTIGEN; SAG1 ANTIGEN; SECRETORY PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELLULAR DISTRIBUTION; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; COPY NUMBER VARIATION; EXON; EXPRESSED SEQUENCE TAG; GENE CLUSTER; GENE DUPLICATION; GENE EXPRESSION; GENE FUNCTION; GENE LOCUS; MOUSE; MULTIGENE FAMILY; NEOSPORA CANINUM; NONHUMAN; PARASITE IDENTIFICATION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; TOXOPLASMA GONDII; TOXOPLASMOSIS; UPREGULATION;

COMPARATIVE GENOMIC HYBRIDIZATION; COMPUTATIONAL BIOLOGY; DNA, PROTOZOAN; GENE DUPLICATION; GENETIC LOCI; GENETIC VARIATION; SARCOCYSTIDAE; SYNTENY;

EID: 84903363826     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01003-13     Document Type: Article

References (55)

1. Lélu M, Villena I, Dardé ML, Aubert D, Geers R, Dupuis E, Marnef F, Poulle ML, Gotteland C, Dumètre A, Gilot-Fromont E. 2012. Quantitative estimation of the viability of Toxoplasma gondii oocysts in soil. Appl. Environ. Microbiol. 78:5127-5132. http://dx.doi.org/10.1128/ AEM.00246-12.
2. de Moura L, Bahia-Oliveira LM, Wada MY, Jones JL, Tuboi SH, Carmo EH, Ramalho WM, Camargo NJ, Trevisan R, Graça RM, da Silva AJ, Moura I, Dubey JP, Garrett DO. 2006. Waterborne toxoplasmosis, Brazil, from field to gene. Emerg. Infect. Dis. 12:326-329. http:// dx.doi.org/10.3201/eid1202.041115.
3. Dardé ML. 2008. Toxoplasma gondii, "new" genotypes and virulence. Parasite 15:366-371. http://dx.doi.org/10.1051/parasite/2008153366.
4. Dubey JP, Graham DH, Dahl E, Hilali M, El-Ghaysh A, Sreekumar C, Kwok OC, Shen SK, Lehmann T. 2003. Isolation and molecular characterization of Toxoplasma gondii from chickens and ducks from Egypt. Vet. Parasitol. 114:89-95. http://dx.doi.org/10.1016/S0304-4017(03)00133-X.
5. Maines TR, Jayaraman A, Belser JA, Wadford DA, Pappas C, Zeng H, Gustin KM, Pearce MB, Viswanathan K, Shriver ZH, Raman R, Cox NJ, Sasisekharan R, Katz JM, Tumpey TM. 2009. Transmission and pathogenesis of swine-origin 2009 A(H1N1) influenza viruses in ferrets and mice. Science 325:484-487. http://dx.doi.org/10.1126/science.1177238.
6. Malhotra D, Sebat J. 2012. CNVs: harbingers of a rare variant revolution in psychiatric genetics. Cell 148:1223-1241. http://dx.doi.org/10.1016/ j.cell.2012.02.039.
7. Almal SH, Padh H. 2012. Implications of gene copy-number variation in health and diseases. J. Hum. Genet. 57:6-13. http://dx.doi.org/10.1038/ jhg.2011.108.
8. Parham P, Norman PJ, Abi-Rached L, Guethlein LA. 2011. Variable NK cell receptors exemplified by human KIR3DL1/S1. J. Immunol. 187: 11-19. http://dx.doi.org/10.4049/jimmunol.0902332.
9. Kugelberg E, Kofoid E, Andersson DI, Lu Y, Mellor J, Roth FP, Roth JR. 2010. The tandem inversion duplication in Salmonella enterica: selection drives unstable precursors to final mutation types. Genetics 185:65-80. http://dx.doi.org/10.1534/genetics.110.114074.
10. Schmidt JM, Good RT, Appleton B, Sherrard J, Raymant GC, Bogwitz MR, Martin J, Daborn PJ, Goddard ME, Batterham P, Robin C. 2010. Copy number variation and transposable elements feature in recent, ongoing adaptation at the Cyp6g1 locus. PLoS Genet. 6:e1000998. http:// dx.doi.org/10.1371/journal.pgen.1000998.
11. Bergthorsson U, Andersson DI, Roth JR. 2007. Ohno's dilemma: evolution of new genes under continuous selection. Proc. Natl. Acad. Sci. U. S. A. 104:17004-17009. http://dx.doi.org/10.1073/pnas.0707158104.
12. Moran GP, Coleman DC, Sullivan DJ. 2011. Comparative genomics and the evolution of pathogenicity in human pathogenic fungi. Eukaryot. Cell 10:34-42. http://dx.doi.org/10.1128/EC.00242-10.
13. Ogata H, Renesto P, Audic S, Robert C, Blanc G, Fournier PE, Parinello H, Claverie JM, Raoult D. 2005. The genome sequence of Rickettsia felis identifies the first putative conjugative plasmid in an obligate intracellular parasite. PLoS Biol. 3:e248. http://dx.doi.org/10.1371/ journal.pbio.0030248.
14. Pasternak ND, Dzikowski R. 2009. PfEMP1: an antigen that plays a key role in the pathogenicity and immune evasion of the malaria parasite Plasmodium falciparum. Int. J. Biochem. Cell Biol. 41:1463-1466. http:// dx.doi.org/10.1016/j.biocel.2008.12.012.
15. Rottmann M, McNamara C, Yeung BK, Lee MC, Zou B, Russell B, Seitz P, Plouffe DM, Dharia NV, Tan J, Cohen SB, Spencer KR, González-Páez GE, Lakshminarayana SB, Goh A, Suwanarusk R, Jegla T, Schmitt EK, Beck HP, Brun R, Nosten F, Renia L, Dartois V, Keller TH, Fidock DA, Winzeler EA, Diagana TT. 2010. Spiroindolones, a potent compound class for the treatment of malaria. Science 329:1175-1180. http:// dx.doi.org/10.1126/science.1193225.
16. Hayton K, Gaur D, Liu A, Takahashi J, Henschen B, Singh S, Lambert L, Furuya T, Bouttenot R, Doll M, Nawaz F, Mu J, Jiang L, Miller LH, Wellems TE. 2008. Erythrocyte binding protein PfRH5 polymorphisms determine species-specific pathways of Plasmodium falciparum invasion. Cell Host Microbe 4:40-51. http://dx.doi.org/10.1016/ j.chom.2008.06.001.
17. Reese ML, Zeiner GM, Saeij JP, Boothroyd JC, Boyle JP. 2011. Polymorphic family of injected pseudokinases is paramount in Toxoplasma virulence. Proc. Natl. Acad. Sci. U. S. A. 108:9625-9630. http://dx.doi.org/ 10.1073/pnas.1015980108.
18. Boothroyd JC, Dubremetz JF. 2008. Kiss and spit: the dual roles of Toxoplasma rhoptries. Nat. Rev. Microbiol. 6:79-88. http://dx.doi.org/ 10.1038/nrmicro1800.
19. Kim SK, Karasov A, Boothroyd JC. 2007. Bradyzoite-specific surface antigen SRS9 plays a role in maintaining Toxoplasma persistence in the brain and in host control of parasite replication in the intestine. Infect. Immun. 75:1626-1634. http://dx.doi.org/10.1128/IAI.01862-06.
20. Saeij JP, Boyle JP, Coller S, Taylor S, Sibley LD, Brooke-Powell ET, Ajioka JW, Boothroyd JC. 2006. Polymorphic secreted kinases are key virulence factors in toxoplasmosis. Science 314:1780-1783. http:// dx.doi.org/10.1126/science.1133690.
21. Taylor S, Barragan A, Su C, Fux B, Fentress SJ, Tang K, Beatty WL, Hajj HE, Jerome M, Behnke MS, White M, Wootton JC, Sibley LD. 2006. A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314:1776-1780. http://dx.doi.org/ 10.1126/science.1133643.
22. Pernas L, Boothroyd JC. 2010. Association of host mitochondria with the parasitophorous vacuole during Toxoplasma infection is not dependent on rhoptry proteins ROP2/8. Int. J. Parasitol. 40:1367-1371. http:// dx.doi.org/10.1016/j.ijpara.2010.07.002.
23. Fox BA, Falla A, Rommereim LM, Tomita T, Gigley JP, Mercier C, Cesbron-Delauw MF, Weiss LM, Bzik DJ. 2011. Type II Toxoplasma gondii KU80 knockout strains enable functional analysis of genes required for cyst development and latent infection. Eukaryot. Cell 10:1193-1206. http://dx.doi.org/10.1128/EC.00297-10.
24. Kehrer-Sawatzki H, Cooper DN. 2007. Structural divergence between the human and chimpanzee genomes. Hum. Genet. 120:759-778. http:// dx.doi.org/10.1007/s00439-006-0270-6.
25. Rieseberg LH, Blackman BK. 2010. Speciation genes in plants. Ann. Bot. 106:439-455. http://dx.doi.org/10.1093/aob/mcq126.
26. Mugridge NB, Morrison DA, Jäkel T, Heckeroth AR, Tenter AM, Johnson AM. 2000. Effects of sequence alignment and structural domains of ribosomal DNA on phylogeny reconstruction for the protozoan family Sarcocystidae. Mol. Biol. Evol. 17:1842-1853. http://dx.doi.org/10.1093/ oxfordjournals.molbev.a026285.
27. Reid AJ, Vermont SJ, Cotton JA, Harris D, Hill-Cawthorne GA, Könen-Waisman S, Latham SM, Mourier T, Norton R, Quail MA, Sanders M, Shanmugam D, Sohal A, Wasmuth JD, Brunk B, Grigg ME, Howard JC, Parkinson J, Roos DS, Trees AJ, Berriman M, Pain A, Wastling JM. 2012. Comparative genomics of the apicomplexan parasites Toxoplasma gondii and Neospora caninum: coccidia differing in host range and transmission strategy. PLoS Pathog. 8:e1002567. http://dx.doi.org/10.1371/ journal.ppat.1002567.
28. Walzer KA, Adomako-Ankomah Y, Dam RA, Herrmann DC, Schares G, Dubey JP, Boyle JP. 2013. Hammondia hammondi, an avirulent relative of Toxoplasma gondii, has functional orthologs of known T. gondii virulence genes. Proc. Natl. Acad. Sci. U. S. A. 110:7446-7451. http:// dx.doi.org/10.1073/pnas.1304322110.
29. Frenkel JK, Dubey JP. 1975. Hammondia hammondi: a new coccidium of cats producing cysts in muscle of other mammals. Science 189:222-224. http://dx.doi.org/10.1126/science.806116.
30. Saeij JP, Boyle JP, Boothroyd JC. 2005. Differences among the three major strains of Toxoplasma gondii and their specific interactions with the infected host. Trends Parasitol. 21:476-481. http://dx.doi.org/10.1016/ j.pt.2005.08.001.
31. Collantes-Fernandez E, Arrighi RB, Alvarez-García G, Weidner JM, Regidor-Cerrillo J, Boothroyd JC, Ortega-Mora LM, Barragan A. 2012. Infected dendritic cells facilitate systemic dissemination and transplacental passage of the obligate intracellular parasite Neospora caninum in mice. PLoS One 7:e32123. http://dx.doi.org/10.1371/journal.pone.0032123.
32. Dubey JP, Sreekumar C. 2003. Redescription of Hammondia hammondi and its differentiation from Toxoplasma gondii. Int. J. Parasitol. 33: 1437-1453. http://dx.doi.org/10.1016/S0020-7519(03)00141-3.
33. Kent WJ. 2002. BLAT-the BLAST-like alignment tool. Genome Res. 12:656-664. http://dx.doi.org/10.1101/gr.229202.
34. Sudmant PH, Kitzman JO, Antonacci F, Alkan C, Malig M, Tsalenko A, Sampas N, Bruhn L, Shendure J, 1000 Genomes Project, Eichler EE. 2010. Diversity of human copy number variation and multicopy genes. Science 330:641-646. http://dx.doi.org/10.1126/science.1197005.
35. Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q, Wortman JR, Bidwell SL, Alsmark UC, Besteiro S, Sicheritz-Ponten T, Noel CJ, Dacks JB, Foster PG, Simillion C, Van de Peer Y, Miranda-Saavedra D, Barton GJ, Westrop GD, Müller S, Dessi D, Fiori PL, Ren Q, Paulsen I, Zhang H, Bastida-Corcuera FD, Simoes-Barbosa A, Brown MT, Hayes RD, Mukherjee M, Okumura CY, Schneider R, Smith AJ, Vanacova S, Villalvazo M, Haas BJ, Pertea M, Feldblyum TV, Utterback TR, Shu CL, Osoegawa K, de Jong PJ, Hrdy I, Horvathova L, Zubacova Z, Dolezal P, Malik SB, Logsdon JM, Henze K, Gupta A, Wang CC, Dunne RL, Upcroft JA, Upcroft P, White O, Salzberg SL, Tang P, Chiu CH, Lee YS, Embley TM, Coombs GH, Mottram JC, Tachezy J, Fraser-Liggett CM, Johnson PJ. 2007. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315:207-212. http:// dx.doi.org/10.1126/science.1132894.
36. Sokal RR, Rohlf FJ. 2012. Biometry: the principles and practice of statistics in biological research, 4th ed. WH Freeman & Co, New York, NY.
37. Wasmuth JD, Pszenny V, Haile S, Jansen EM, Gast AT, Sher A, Boyle JP, Boulanger MJ, Parkinson J, Grigg ME. 2012. Integrated bioinformatic and targeted deletion analyses of the SRS gene superfamily identify SRS29C as a negative regulator of Toxoplasma virulence. mBio 3(6): e00321-12. http://dx.doi.org/10.1128/mBio.00321-12.
38. Fritz HM, Buchholz KR, Chen X, Durbin-Johnson B, Rocke DM, Conrad PA, Boothroyd JC. 2012. Transcriptomic analysis of Toxoplasma development reveals many novel functions and structures specific to sporozoites and oocysts. PLoS One 7:e29998. http://dx.doi.org/10.1371/ journal.pone.0029998.
39. Huynh MH, Carruthers VB. 2009. Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot. Cell 8:530-539. http:// dx.doi.org/10.1128/EC.00358-08.
40. Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA. 2003. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41. http://dx.doi.org/10.1186/1471-2105-4-41.
41. Yang N, Farrell A, Niedelman W, Melo M, Lu D, Julien L, Marth GT, Gubbels MJ, Saeij JP. 2013. Genetic basis for phenotypic differences between different Toxoplasma gondii type I strains. BMC Genomics 14: 467. http://dx.doi.org/10.1186/1471-2164-14-467.
42. Boyle JP, Rajasekar B, Saeij JP, Ajioka JW, Berriman M, Paulsen I, Roos DS, Sibley LD, White MW, Boothroyd JC. 2006. Just one cross appears capable of dramatically altering the population biology of a eukaryotic pathogen like Toxoplasma gondii. Proc. Natl. Acad. Sci. U. S. A. 103: 10514-10519. http://dx.doi.org/10.1073/pnas.0510319103.
43. Frenkel JK, Dubey JP, Miller NL. 1970. Toxoplasma gondii in cats: fecal stages identified as coccidian oocysts. Science 167:893-896. http:// dx.doi.org/10.1126/science.167.3919.893.
44. Behnke MS, Khan A, Wootton JC, Dubey JP, Tang K, Sibley LD. 2011. Virulence differences in Toxoplasma mediated by amplification of a family of polymorphic pseudokinases. Proc. Natl. Acad. Sci. U. S. A. 108: 9631-9636. http://dx.doi.org/10.1073/pnas.1015338108.
45. Jackson AP, Gamble JA, Yeomans T, Moran GP, Saunders D, Harris D, Aslett M, Barrell JF, Butler G, Citiulo F, Coleman DC, de Groot PW, Goodwin TJ, Quail MA, McQuillan J, Munro CA, Pain A, Poulter RT, Rajandream MA, Renauld H, Spiering MJ, Tivey A, Gow NA, Barrell B, Sullivan DJ, Berriman M. 2009. Comparative genomics of the fungal pathogens Candida dubliniensis and Candida albicans. Genome Res. 19: 2231-2244. http://dx.doi.org/10.1101/gr.097501.109.
46. Saeij JP, Coller S, Boyle JP, Jerome ME, White MW, Boothroyd JC. 2007. Toxoplasma co-opts host gene expression by injection of a polymorphic kinase homologue. Nature 445:324-327. http://dx.doi.org/10.1038/ nature05395.
47. Rosowski EE, Lu D, Julien L, Rodda L, Gaiser RA, Jensen KD, Saeij JP. 2011. Strain-specific activation of the NF-kappaB pathway by GRA15, a novel Toxoplasma gondii dense granule protein. J. Exp. Med. 208:195-212. http://dx.doi.org/10.1084/jem.20100717.
48. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The Sequence Alignment/map format and SAMtools. Bioinformatics 25:2078-2079. http://dx.doi.org/10.1093/bioinformatics/ btp352.
49. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841-842. http:// dx.doi.org/10.1093/bioinformatics/btq033.
50. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9:357-359. http://dx.doi.org/10.1038/nmeth.1923.
51. Bahl A, Davis PH, Behnke M, Dzierszinski F, Jagalur M, Chen F, Shanmugam D, White MW, Kulp D, Roos DS. 2010. A novel multifunctional oligonucleotide microarray for Toxoplasma gondii. BMC Genomics 11:603. http://dx.doi.org/10.1186/1471-2164-11-603.
52. Dunn OJ. 1961. Multiple comparisons among means. J. Am. Stat. Assoc. 56:52-64. http://dx.doi.org/10.1080/01621459.1961.10482090.
53. Xie C, Tammi MT. 2009. CNV-seq, a new method to detect copy number variation using high-throughput sequencing. BMC Bioinformatics 10:80. http://dx.doi.org/10.1186/1471-2105-10-80.
54. Donald RG, Carter D, Ullman B, Roos DS. 1996. Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthinexanthine-guanine phosphoribosyltransferase gene. Use as a selectable marker for stable transformation. J. Biol. Chem. 271:14010-14019. http:// dx.doi.org/10.1074/jbc.271.24.14010.
55. Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR. 1989. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77:61-68. http://dx.doi.org/10.1016/0378-1119(89)90359-4.