Comparative genomic analysis of human infective Trypanosoma cruzi lineages with the bat-restricted subspecies T. cruzi marinkellei

BMC Genomics

Volumn 13, Issue 1, 2012, Pages

  Franzén, Oscar ^a   Talavera López, Carlos ^a   Ochaya, Stephen ^a   Butler, Claire E ^b   Messenger, Louisa A ^c   Lewis, Michael D ^c   Llewellyn, Martin S ^c   Marinkelle, Cornelis J ^d   Tyler, Kevin M ^b   Miles, Michael A ^c   Andersson, Björn ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^d UNIVERSIDAD DE LOS ANDES   (Colombia)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; PROTOZOAL DNA; RETROPOSON;

ARTICLE; BAT; CELL DIVISION; CELL LINEAGE; CHAGAS DISEASE; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; COPY NUMBER VARIATION; GENE SEQUENCE; GENETIC VARIABILITY; GENOME SIZE; HETEROZYGOSITY; HORIZONTAL GENE TRANSFER; HUMAN; KINETOPLASTIDA; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; RETROPOSON; SEQUENCE HOMOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM; SYNTENY; TRYPANOSOMA CRUZI; TRYPANOSOMA CRUZI MAINKELLEI; TRYPANOSOMIASIS; ANIMAL; BIOLOGY; CLASSIFICATION; COMPARATIVE STUDY; GENETIC LINKAGE; GENETICS; PARASITOLOGY; TRYPANOSOMA;

EUKARYOTA; MAMMALIA; SCHIZOTRYPANUM; TRYPANOSOMA CRUZI; TRYPANOSOMA CRUZI MARINKELLEI;

ACETYLTRANSFERASES; ANIMALS; CHAGAS DISEASE; CHIROPTERA; COMPUTATIONAL BIOLOGY; DNA COPY NUMBER VARIATIONS; DNA, PROTOZOAN; GENETIC LINKAGE; HUMANS; RETROELEMENTS; TRYPANOSOMA; TRYPANOSOMA CRUZI;

EID: 84867024945     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-13-531     Document Type: Article

References (72)

1. Baker JR, Miles MA, Godfrey DG, Barrett TV. Biochemical characterization of some species of Trypansoma (Schizotrypanum) from bats (Microchiroptera). AmJTrop Med Hyg 1978, 27(3):483-491.
2. Gaunt M, Miles M. The ecotopes and evolution of triatomine bugs (triatominae) and their associated trypanosomes. Mem Inst Oswaldo Cruz 2000, 95(4):557-565.
3. Stevens J, Noyes H, Gibson W. The evolution of trypanosomes infecting humans and primates. Mem Inst Oswaldo Cruz 1998, 93(5):669-676. 10.1590/S0074-02761998000500019, 9830536.
4. Marinkelle CJ. Prevalence of Trypanosoma cruzi-like infection of Colombian bats. Ann Trop Med Parasitol 1982, 76(2):125-134.
5. Cavazzana M, Marcili A, Lima L, da Silva FM, Junqueira AC, Veludo HH, Viola LB, Campaner M, Nunes VL, Paiva F, et al. Phylogeographical, ecological and biological patterns shown by nuclear (ssrRNA and gGAPDH) and mitochondrial (Cyt b) genes of trypanosomes of the subgenus Schizotrypanum parasitic in Brazilian bats. Int J Parasitol 2010, 40(3):345-355. 10.1016/j.ijpara.2009.08.015, 19766649.
6. Thomas ME, Rasweiler Iv JJ, D'Alessandro A. Experimental transmission of the parasitic flagellates Trypanosoma cruzi and Trypanosoma rangeli between triatomine bugs or mice and captive neotropical bats. Mem Inst Oswaldo Cruz 2007, 102(5):559-565. 10.1590/S0074-02762007005000068, 17710299.
7. Stevens JR, Noyes HA, Dover GA, Gibson WC. The ancient and divergent origins of the human pathogenic trypanosomes. Trypanosoma brucei and T. cruzi. Parasitology 1999, 118(Pt 1):107-116.
8. Hamilton PB, Stevens JR, Gaunt MW, Gidley J, Gibson WC. Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. Int J Parasitol 2004, 34(12):1393-1404. 10.1016/j.ijpara.2004.08.011, 15542100.
9. Hamilton PB, Gibson WC, Stevens JR. Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Mol Phylogenet Evol 2007, 44(1):15-25. 10.1016/j.ympev.2007.03.023, 17513135.
10. Machado CA, Ayala FJ. Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proc Natl Acad Sci U S A 2001, 98(13):7396-7401. 10.1073/pnas.121187198, 34680, 11416213.
11. Lewis MD, Llewellyn MS, Yeo M, Acosta N, Gaunt MW, Miles MA. Recent, Independent and Anthropogenic Origins of Trypanosoma cruzi Hybrids. PLoS Negl Trop Dis 2011, 5(10):e1363. 10.1371/journal.pntd.0001363, 3191134, 22022633.
12. Flores-Lopez CA, Machado CA. Analyses of 32 loci clarify phylogenetic relationships among Trypanosoma cruzi lineages and support a single hybridization prior to human contact. PLoS Negl Trop Dis 2011, 5(8):e1272. 10.1371/journal.pntd.0001272, 3149036, 21829751.
13. Marinkelle CJ. Developmental stages of Trypanosoma cruzi-like flagellates in Cavernicola pilosa. Rev Biol Trop 1982, 30(2):107-111.
14. Barnabe C, Brisse S, Tibayrenc M. Phylogenetic diversity of bat trypanosomes of subgenus Schizotrypanum based on multilocus enzyme electrophoresis, random amplified polymorphic DNA, and cytochrome b nucleotide sequence analyses. Infect Genet Evol 2003, 2(3):201-208. 10.1016/S1567-1348(02)00130-2, 12797982.
15. Hamilton PB, Teixeira MM, Stevens JR. The evolution of Trypanosoma cruzi: the 'bat seeding' hypothesis. Trends Parasitol 2012, 28(4):136-141. 10.1016/j.pt.2012.01.006, 22365905.
16. Hoffecker JF, Powers WR, Goebel T. The colonization of beringia and the peopling of the new world. Science 1993, 259(5091):46-53. 10.1126/science.259.5091.46, 17757472.
17. Zingales B, Miles MA, Campbell DA, Tibayrenc M, Macedo AM, Teixeira MM, Schijman AG, Llewellyn MS, Lages-Silva E, Machado CR, Andrade SG, Sturm NR. The revised Trypanosoma cruzi subspecific nomenclature: rationale, epidemiological relevance and research applications. Infect Genet Evol 2012, 12(2):240-53. 10.1016/j.meegid.2011.12.009, 22226704.
18. El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran AN, Ghedin E, Worthey EA, Delcher AL, Blandin G, et al. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 2005, 309(5733):409-415. 10.1126/science.1112631, 16020725.
19. Weatherly DB, Boehlke C, Tarleton RL. Chromosome level assembly of the hybrid Trypanosoma cruzi genome. BMC Genomics 2009, 10:255. 10.1186/1471-2164-10-255, 2698008, 19486522.
20. Franzén O, Ochaya S, Sherwood E, Lewis MD, Llewellyn MS, Miles MA, Andersson B. Shotgun Sequencing Analysis of Trypanosoma cruzi I Sylvio X10/1 and Comparison with T. cruzi VI CL Brener. PLoS Negl Trop Dis 2011, 5(3):e984. 10.1371/journal.pntd.0000984, 3050914, 21408126.
21. Zingales B, Andrade SG, Briones MR, Campbell DA, Chiari E, Fernandes O, Guhl F, Lages-Silva E, Macedo AM, Machado CR, et al. A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem Inst Oswaldo Cruz 2009, 104(7):1051-1054. 10.1590/S0074-02762009000700021, 20027478.
22. Van Nieuwerburgh F, Thompson RC, Ledesma J, Deforce D, Gaasterland T, Ordoukhanian P, Head SR. Illumina mate-paired DNA sequencing-library preparation using Cre-Lox recombination. Nucleic Acids Res 2012, 40(3):e24. 10.1093/nar/gkr1000, 3273786, 22127871.
23. Tsai IJ, Otto TD, Berriman M. Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps. Genome Biol 2010, 11(4):R41. 10.1186/gb-2010-11-4-r41, 2884544, 20388197.
24. Lewis MD, Llewellyn MS, Gaunt MW, Yeo M, Carrasco HJ, Miles MA. Flow cytometric analysis and microsatellite genotyping reveal extensive DNA content variation in Trypanosoma cruzi populations and expose contrasts between natural and experimental hybrids. Int J Parasitol 2009, 39(12):1305-1317. 10.1016/j.ijpara.2009.04.001, 2731025, 19393242.
25. Rogers MB, Hilley JD, Dickens NJ, Wilkes J, Bates PA, Depledge DP, Harris D, Her Y, Herzyk P, Imamura H, et al. Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. Genome Res 2011, 21(12):2129-2142. 10.1101/gr.122945.111, 3227102, 22038252.
26. Gladyshev EA, Arkhipova IR. Genome structure of bdelloid rotifers: shaped by asexuality or desiccation?. J Hered 2010, 101(Suppl 1):S85-93.
27. Franzen O, Jerlstrom-Hultqvist J, Castro E, Sherwood E, Ankarklev J, Reiner DS, Palm D, Andersson JO, Andersson B, Svard SG. Draft genome sequencing of giardia intestinalis assemblage B isolate GS: is human giardiasis caused by two different species?. PLoS Pathog 2009, 5(8):e1000560. 10.1371/journal.ppat.1000560, 2723961, 19696920.
28. Jerlstrom-Hultqvist J, Franzen O, Ankarklev J, Xu F, Nohynkova E, Andersson JO, Svard SG, Andersson B. Genome analysis and comparative genomics of a Giardia intestinalis assemblage E isolate. BMC Genomics 2010, 11:543. 10.1186/1471-2164-11-543, 3091692, 20929575.
29. Fritz-Laylin LK, Prochnik SE, Ginger ML, Dacks JB, Carpenter ML, Field MC, Kuo A, Paredez A, Chapman J, Pham J, et al. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 2010, 140(5):631-642. 10.1016/j.cell.2010.01.032, 20211133.
30. Omilian AR, Cristescu ME, Dudycha JL, Lynch M. Ameiotic recombination in asexual lineages of Daphnia. Proc Natl Acad Sci U S A 2006, 103(49):18638-18643. 10.1073/pnas.0606435103, 1693715, 17121990.
31. Bartholomeu DC, Cerqueira GC, Leao AC, daRocha WD, Pais FS, Macedo C, Djikeng A, Teixeira SM, El-Sayed NM. Genomic organization and expression profile of the mucin-associated surface protein (masp) family of the human pathogen Trypanosoma cruzi. Nucleic Acids Res 2009, 37(10):3407-3417. 10.1093/nar/gkp172, 2691823, 19336417.
32. Buscaglia CA, Campo VA, Di Noia JM, Torrecilhas AC, De Marchi CR, Ferguson MA, Frasch AC, Almeida IC. The surface coat of the mammal-dwelling infective trypomastigote stage of Trypanosoma cruzi is formed by highly diverse immunogenic mucins. J Biol Chem 2004, 279(16):15860-15869. 10.1074/jbc.M314051200, 14749325.
33. Minning TA, Weatherly DB, Flibotte S, Tarleton RL. Widespread, focal copy number variations (CNV) and whole chromosome aneuploidies in Trypanosoma cruzi strains revealed by array comparative genomic hybridization. BMC Genomics 2011, 12:139. 10.1186/1471-2164-12-139, 3060142, 21385342.
34. Arner E, Kindlund E, Nilsson D, Farzana F, Ferella M, Tammi MT, Andersson B. Database of Trypanosoma cruzi repeated genes: 20,000 additional gene variants. BMC Genomics 2007, 8:391. 10.1186/1471-2164-8-391, 2204015, 17963481.
35. Souza RT, Lima FM, Barros RM, Cortez DR, Santos MF, Cordero EM, Ruiz JC, Goldenberg S, Teixeira MM, da Silveira JF. Genome size, karyotype polymorphism and chromosomal evolution in Trypanosoma cruzi. PLoS One 2011, 6(8):e23042. 10.1371/journal.pone.0023042, 3155523, 21857989.
36. Ruvalcaba-Trejo LI, Sturm NR. The Trypanosoma cruzi Sylvio X10 strain maxicircle sequence: the third musketeer. BMC Genomics 2011, 12:58. 10.1186/1471-2164-12-58, 3040149, 21261994.
37. Messenger LA, Llewellyn MS, Bhattacharyya T, Franzen O, Lewis MD, Ramirez JD, Carrasco HJ, Andersson B, Miles MA. Multiple Mitochondrial Introgression Events and Heteroplasmy inTrypanosoma cruziRevealed by Maxicircle MLST and Next Generation Sequencing. PLoS Negl Trop Dis 2012, 6(4):e1584. 10.1371/journal.pntd.0001584, 3323513, 22506081.
38. Carver TJ, Rutherford KM, Berriman M, Rajandream MA, Barrell BG, Parkhill J. ACT: the Artemis Comparison Tool. Bioinformatics 2005, 21(16):3422-3423. 10.1093/bioinformatics/bti553, 15976072.
39. Jackson AP, Sanders M, Berry A, McQuillan J, Aslett MA, Quail MA, Chukualim B, Capewell P, MacLeod A, Melville SE, et al. The genome sequence of Trypanosoma brucei gambiense, causative agent of chronic human african trypanosomiasis. PLoS Negl Trop Dis 2010, 4(4):e658. 10.1371/journal.pntd.0000658, 2854126, 20404998.
40. Sharp PM, Li WH. The codon Adaptation Index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 1987, 15(3):1281-1295. 10.1093/nar/15.3.1281, 340524, 3547335.
41. Engman DM, Reddy LV, Donelson JE, Kirchhoff LV. Trypanosoma cruzi exhibits inter- and intra-strain heterogeneity in molecular karyotype and chromosomal gene location. Mol Biochem Parasitol 1987, 22(2-3):115-123.
42. Henriksson J, Aslund L, Macina RA, de Cazzulo BM F, Cazzulo JJ, Frasch AC, Pettersson U. Chromosomal localization of seven cloned antigen genes provides evidence of diploidy and further demonstration of karyotype variability in Trypanosoma cruzi. Mol Biochem Parasitol 1990, 42(2):213-223. 10.1016/0166-6851(90)90164-H, 2270104.
43. Branche C, Ochaya S, Aslund L, Andersson B. Comparative karyotyping as a tool for genome structure analysis of Trypanosoma cruzi. Mol Biochem Parasitol 2006, 147(1):30-38. 10.1016/j.molbiopara.2006.01.005, 16481054.
44. Kurtz S, Phillippy A, Delcher AL, Smoot M, Shumway M, Antonescu C, Salzberg SL. Versatile and open software for comparing large genomes. Genome Biol 2004, 5(2):R12. 10.1186/gb-2004-5-2-r12, 395750, 14759262.
45. Obado SO, Taylor MC, Wilkinson SR, Bromley EV, Kelly JM. Functional mapping of a trypanosome centromere by chromosome fragmentation identifies a 16-kb GC-rich transcriptional " strand-switch" domain as a major feature. Genome Res 2005, 15(1):36-43. 10.1101/gr.2895105, 540271, 15632088.
46. Maser P, Sutterlin C, Kralli A, Kaminsky R. A nucleoside transporter from Trypanosoma brucei involved in drug resistance. Science 1999, 285(5425):242-244. 10.1126/science.285.5425.242, 10398598.
47. Kazazian HH. Mobile elements: drivers of genome evolution. Science 2004, 303(5664):1626-1632. 10.1126/science.1089670, 15016989.
48. Bringaud F, Ghedin E, El-Sayed NM, Papadopoulou B. Role of transposable elements in trypanosomatids. Microbes Infect 2008, 10(6):575-581. 10.1016/j.micinf.2008.02.009, 18467144.
49. Lorenzi HA, Robledo G, Levin MJ. The VIPER elements of trypanosomes constitute a novel group of tyrosine recombinase-enconding retrotransposons. Mol Biochem Parasitol 2006, 145(2):184-194. 10.1016/j.molbiopara.2005.10.002, 16297462.
50. Thomas MC, Macias F, Alonso C, Lopez MC. The biology and evolution of transposable elements in parasites. Trends Parasitol 2010, 26(7):350-362. 10.1016/j.pt.2010.04.001, 20444649.
51. Price AL, Jones NC, Pevzner PA. De novo identification of repeat families in large genomes. Bioinformatics 2005, 21(Suppl 1):i351-358. 10.1093/bioinformatics/bti1018, 15961478.
52. Smit AFA, Hubley R, Green P. RepeatMasker Open-3.0 2010,
53. Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008, 18(5):821-829. 10.1101/gr.074492.107, 2336801, 18349386.
54. Miller JR, Delcher AL, Koren S, Venter E, Walenz BP, Brownley A, Johnson J, Li K, Mobarry C, Sutton G. Aggressive assembly of pyrosequencing reads with mates. Bioinformatics 2008, 24(24):2818-2824. 10.1093/bioinformatics/btn548, 2639302, 18952627.
55. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25(14):1754-1760. 10.1093/bioinformatics/btp324, 2705234, 19451168.
56. Lacerda G, Vidal R, Zorro, Carazzole M. 2011, http://www.lge.ibi.unicamp.br/zorro/.
57. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011, 27(4):578-579. 10.1093/bioinformatics/btq683, 21149342.
58. Besemer J, Lomsadze A, Borodovsky M. GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 2001, 29(12):2607-2618.
59. Hurst LD. The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends Genet 2002, 18(9):486. 10.1016/S0168-9525(02)02722-1, 12175810.
60. Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 1997, 13(5):555-556.
61. Jurka J, Kapitonov VV, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res 2005, 110(1-4):462-467.
62. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 1999, 27(2):573-580. 10.1093/nar/27.2.573, 148217, 9862982.
63. Dereeper A, Audic S, Claverie JM, Blanc G. BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evol Biol 2010, 10:8. 10.1186/1471-2148-10-8, 2821324, 20067610.
64. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 2003, 31(13):3497-3500. 10.1093/nar/gkg500, 168907, 12824352.
65. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007, 56(4):564-577. 10.1080/10635150701472164, 17654362.
66. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 2009, 25(9):1189-1191. 10.1093/bioinformatics/btp033, 2672624, 19151095.
67. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006, 22(21):2688-2690. 10.1093/bioinformatics/btl446, 16928733.
68. Grant BJ, Rodrigues AP, ElSawy KM, McCammon JA, Caves LS. Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics 2006, 22(21):2695-2696. 10.1093/bioinformatics/btl461, 16940322.
69. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25(16):2078-2079. 10.1093/bioinformatics/btp352, 2723002, 19505943.
70. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1999, 41:95-98.
71. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.
72. Woods A, Baines AJ, Gull K. A high molecular mass phosphoprotein defined by a novel monoclonal antibody is closely associated with the intermicrotubule cross bridges in the Trypanosoma brucei cytoskeleton. J Cell Sci 1992, 103(Pt 3):665-675.