Genomic changes during evolution of animal parasitism in eukaryotes

Current Opinion in Genetics and Development

Volumn 35, Issue , 2015, Pages 86-92

  Leckenby, Amber ^a   Hall, Neil ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BRUGIA MALAYI; COMPARATIVE GENOMICS; CRYPTOSPORIDIUM; ENTAMOEBA HISTOLYTICA; EUKARYOTE; EVOLUTION; GENE LOSS; GENE REARRANGEMENT; GENE SEQUENCE; GENOMICS; GIARDIA; GIARDIA INTESTINALIS; HAEMONCHUS CONTORTUS; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; MULTIGENE FAMILY; NONHUMAN; PARASITISM; PATHOGENESIS; PATHOGENICITY; PHYLOGENY; PLASMODIUM; PRIORITY JOURNAL; REVIEW; SPECIES DIFFERENCE; STRAIN DIFFERENCE; TOXOPLASMA; TRICHOMONAS; TRYPANOSOMA; TRYPANOSOMATIDAE; ANIMAL; GENETICS; GENOME; MOLECULAR EVOLUTION; PARASITE;

ANIMALS; BIOLOGICAL EVOLUTION; EVOLUTION, MOLECULAR; GENOME, PROTOZOAN; GENOMICS; HOST-PATHOGEN INTERACTIONS; PARASITES;

EID: 84948139134     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2015.11.001     Document Type: Review

References (103)

1. Wei L., Liu Y., Dubchak I., Shon J., Park J. Comparative genomics approaches to study organism similarities and differences. J Biomed Inform 2002, 35:142-150.
2. Parkhill J., Dougan G., James K.D., Thomson N.R., Pickard D., Wain J., Churcher C., Mungall K.L., Bentley S.D., Holden M.T.G., et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 2001, 413:848-852.
3. Parkhill J., Wren B.W., Thomson N.R., Titball R.W., Holden M.T., Prentice M.B., Sebaihia M., James K.D., Churcher C., Mungall K.L., et al. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 2001, 413:523-527.
4. Waterman S.R., Holden D.W. Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol 2003, 5:501-511.
5. Juhas M., Crook D.W., Hood D.W. Type IV secretion systems: tools of bacterial horizontal gene transfer and virulence. Cell Microbiol 2008, 10:2377-2386.
6. Loftus B., Anderson I., Davies R., Alsmark U.C.M., Samuelson J., Amedeo P., Roncaglia P., Berriman M., Hirt R.P., Mann B.J., et al. The genome of the protist parasite Entamoeba histolytica. Nature 2005, 433:865-868.
7. Lorenzi H.A., Puiu D., Miller J.R., Brinkac L.M., Amedeo P., Hall N., Caler E.V. New assembly, reannotation and analysis of the Entamoeba histolytica genome reveal new genomic features and protein content information. PLoS Negl Trop Dis 2010, 4:e716.
8. Carlton J.M., Hirt R.P., Silva J.C., Delcher A.L., Schatz M., Zhao Q., Wortman J.R., Bidwell S.L., Alsmark U.C.M., Besteiro S., et al. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 2007, 315:207-212.
9. Keeling P.J., Palmer J.D. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 2008, 9:605-618.
10. Andersson J.O. Gene transfer and diversification of microbial eukaryotes. Annu Rev Microbiol 2009, 63:177-193.
11. Ohno S. Evolution by Gene Duplication 2013, Springer.
12. Force A., Lynch M., Pickett F.B., Amores A., Yan Y., Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 1999, 151:1531-1545.
13. Stoltzfus A. On the possibility of constructive neutral evolution. J Mol Evol 1999, 49:169-181.
14. He X., Zhang J. Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 2005, 169:1157-1164.
15. Shapiro J.A., Huang W., Zhang C., Hubisz M.J., Lu J., Turissini D.A., Fang S., Wang H.-Y., Hudson R.R., Nielsen R., et al. Adaptive genic evolution in the Drosophila genomes. Proc Natl Acad Sci U S A 2007, 104:2271-2276.
16. Sackton T.B., Lazzaro B.P., Schlenke T.A., Evans J.D., Hultmark D., Clark A.G. Dynamic evolution of the innate immune system in Drosophila. Nat Genet 2007, 39:1461-1468.
17. Escriva H., Bertrand S., Germain P., Robinson-Rechavi M., Umbhauer M., Cartry J., Duffraisse M., Holland L., Gronemeyer H., Laudet V. Neofunctionalization in vertebrates: the example of retinoic acid receptors. PLoS Genet 2006, 2:e102.
18. Duarte J.M., Cui L., Wall P.K., Zhang Q., Zhang X., Leebens-Mack J., Ma H., Altman N., dePamphilis C.W. Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol 2006, 23:469-478.
19. Assis R., Bachtrog D. Neofunctionalization of young duplicate genes in Drosophila. Proc Natl Acad Sci U S A 2013, 110:17409-17414.
20. Rastogi S., Liberles D.A. Subfunctionalization of duplicated genes as a transition state to neofunctionalization. BMC Evol Biol 2005, 5:28.
21. Poulin R., Morand S. The diversity of parasites. Q Rev Biol 2000, 75:277-293.
22. Blaxter M.L., De Ley P., Garey J.R., Liu L.X., Scheldeman P., Vierstraete A., Vanfleteren J.R., Mackey L.Y., Dorris M., Frisse L.M., et al. A molecular evolutionary framework for the phylum Nematoda. Nature 1998, 392:71-75.
23. Clark W.C. Origins of the parasitic habit in the nematoda. Int J Parasitol 1994, 24:1117-1129.
24. Hall N. Advanced sequencing technologies and their wider impact in microbiology. J Exp Biol 2007, 210:1518-1525.
25. Forrester S.J., Hall N. The revolution of whole genome sequencing to study parasites. Mol Biochem Parasitol 2014, 195:77-81.
26. Cameron S.L. Insect mitochondrial genomics: implications for evolution and phylogeny. Annu Rev Entomol 2014, 59:95-117.
27. Gibson A., Gowri-Shankar V., Higgs P.G., Rattray M. A comprehensive analysis of mammalian mitochondrial genome base composition and improved phylogenetic methods. Mol Biol Evol 2005, 22:251-264.
28. Li H., Shao R., Song N., Song F., Jiang P., Li Z., Cai W. Higher-level phylogeny of paraneopteran insects inferred from mitochondrial genome sequences. Sci Rep 2015, 5:8527.
29. Liu G.-H., Shao R., Li J.-Y., Zhou D.-H., Li H., Zhu X.-Q. The complete mitochondrial genomes of three parasitic nematodes of birds: a unique gene order and insights into nematode phylogeny. BMC Genomics 2013, 14:414.
30. Sultana T., Kim J., Lee S.-H., Han H., Kim S., Min G.-S., Nadler S.A., Park J.-K. Comparative analysis of complete mitochondrial genome sequences confirms independent origins of plant-parasitic nematodes. BMC Evol Biol 2013, 13:12.
31. Ogedengbe J.D., Hanner R.H., Barta J.R. DNA barcoding identifies Eimeria species and contributes to the phylogenetics of coccidian parasites (Eimeriorina, Apicomplexa, Alveolata). Int J Parasitol 2011, 41:843-850.
32. Huang H., Wang T., Yang G., Zhang Z., Wang C., Yang Z., Luo L., Liu L., Lan J., Huang X. Molecular characterization and phylogenetic analysis of Dirofilaria immitis of China based on COI and 12S rDNA genes. Vet Parasitol 2009, 160:175-179.
33. Janouskovec J., Horák A., Oborník M., Lukes J., Keeling P.J. A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci U S A 2010, 107:10949-10954.
34. Moore R.B., Oborník M., Janouskovec J., Chrudimský T., Vancová M., Green D.H., Wright S.W., Davies N.W., Bolch C.J.S., Heimann K., et al. A photosynthetic alveolate closely related to apicomplexan parasites. Nature 2008, 451:959-963.
35. Janouškovec J., Tikhonenkov D.V., Burki F., Howe A.T., Kolísko M., Mylnikov A.P., Keeling P.J. Factors mediating plastid dependency and the origins of parasitism in apicomplexans and their close relatives. Proc Natl Acad Sci U S A 2015, 112:10200-10207.
36. Anantharaman V., Iyer L.M., Balaji S., Aravind L. Adhesion molecules and other secreted host-interaction determinants in Apicomplexa: insights from comparative genomics. Int Rev Cytol 2007, 262:1-74.
37. Wasmuth J., Daub J., Peregrín-Alvarez J.M., Finney C.A.M., Parkinson J. The origins of apicomplexan sequence innovation. Genome Res 2009, 19:1202-1213.
38. Ghedin E., Wang S., Spiro D., Caler E., Zhao Q., Crabtree J., Allen J.E., Delcher A.L., Guiliano D.B., Miranda-Saavedra D., et al. Draft genome of the filarial nematode parasite Brugia malayi. Science 2007, 317:1756-1760.
39. Laing R., Kikuchi T., Martinelli A., Tsai I.J., Beech R.N., Redman E., Holroyd N., Bartley D.J., Beasley H., Britton C., et al. The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome Biol 2013, 14:R88.
40. Nash T.E., Banks S.M., Alling D.W., Merritt J.W., Conrad J.T. Frequency of variant antigens in Giardia lamblia. Exp Parasitol 1990, 71:415-421.
41. Nash T.E., Mowatt M.R. Variant-specific surface proteins of Giardia lamblia are zinc-binding proteins. Proc Natl Acad Sci U S A 1993, 90:5489-5493.
42. Sun J., Jiang H., Flores R., Wen J. Gene duplication in the genome of parasitic Giardia lamblia. BMC Evol Biol 2010, 10:49.
43. Berriman M., Ghedin E., Hertz-Fowler C., Blandin G., Renauld H., Bartholomeu D., Lennard N., Caler E., Hamlin N., Haas B., et al. The genome of the African trypanosome Trypanosoma brucei. Science 2005, 309:416-422.
44. Ivens A.C., Peacock C.S., Worthey E.A., Murphy L., Aggarwal G., Berriman M., Sisk E., Rajandream M.-A., Adlem E., Aert R., et al. The genome of the kinetoplastid parasite, Leishmania major. Science 2005, 309:436-442.
45. El-Sayed N.M., Myler P.J., Bartholomeu D.C., Nilsson D., Aggarwal G., Tran A.-N., Ghedin E., Worthey E.A., Delcher A.L., Blandin G., et al. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 2005, 309:409-415.
46. Barry J.D., Ginger M.L., Burton P., McCulloch R. Why are parasite contingency genes often associated with telomeres?. Int J Parasitol 2003, 33:29-45.
47. Lemieux J.E., Kyes S.A., Otto T.D., Feller A.I., Eastman R.T., Pinches R.A., Berriman M., Su X.-Z., Newbold C.I. Genome-wide profiling of chromosome interactions in Plasmodium falciparum characterizes nuclear architecture and reconfigurations associated with antigenic variation. Mol Microbiol 2013, 90:519-537.
48. El-Sayed N.M., Myler P.J., Blandin G., Berriman M., Crabtree J., Aggarwal G., Caler E., Renauld H., Worthey E.a., Hertz-Fowler C., et al. Comparative genomics of trypanosomatid parasitic protozoa. Science 2005, 309:404-409.
49. Rovira-Graells N., Gupta A.P., Planet E., Crowley V.M., Mok S., Ribas de Pouplana L., Preiser P.R., Bozdech Z., Cortés A. Transcriptional variation in the malaria parasite Plasmodium falciparum. Genome Res 2012, 22:925-938.
50. Flueck C., Bartfai R., Niederwieser I., Witmer K., Alako B.T.F., Moes S., Bozdech Z., Jenoe P., Stunnenberg H.G., Voss T.S. A major role for the Plasmodium falciparum ApiAP2 Protein PfSIP2 in chromosome end biology. PLoS Pathog 2010, 6:e1000784.
51. Campbell T.L., De Silva E.K., Olszewski K.L., Elemento O., Llinás M. Identification and genome-wide prediction of DNA binding specificities for the ApiAP2 family of regulators from the malaria parasite. PLoS Pathog 2010, 6:e1001165.
52. Tsai I.J., Zarowiecki M., Holroyd N., Garciarrubio A., Sanchez-Flores A., Brooks K., Tracey A., Bobes R.J., Fragoso G., Sciutto E., et al. The genomes of four tapeworm species reveal adaptations to parasitism. Nature 2013, 496:57-63.
53. Jex A.R., Nejsum P., Schwarz E.M., Hu L., Young N.D., Hall R.S., Korhonen P.K., Liao S., Thamsborg S., Xia J., et al. Genome and transcriptome of the porcine whipworm Trichuris suis. Nat Genet 2014, 46:701-706.
54. Gomez-Escobar N., Bennett C., Prieto-Lafuente L., Aebischer T., Blackburn C.C., Maizels R.M. Heterologous expression of the filarial nematode alt gene products reveals their potential to inhibit immune function. BMC Biol 2005, 3:8.
55. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., Carlton J.M., Pain A., Nelson K.E., Bowman S., et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419:498-511.
56. Carlton J.M., Adams J.H., Silva J.C., Bidwell S.L., Lorenzi H., Caler E., Crabtree J., Angiuoli S.V., Merino E.F., Amedeo P., et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 2008, 455:757-763.
57. Winter G., Kawai S., Haeggström M., Kaneko O., von Euler A., Kawazu S., Palm D., Fernandez V., Wahlgren M. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J Exp Med 2005, 201:1853-1863.
58. Sam-Yellowe T.Y., Florens L., Johnson J.R., Wang T., Drazba J.A., Le Roch K.G., Zhou Y., Batalov S., Carucci D.J., Winzeler E.A., et al. A Plasmodium gene family encoding Maurer's cleft membrane proteins: structural properties and expression profiling. Genome Res 2004, 14:1052-1059.
59. Del Portillo H.A., Fernandez-Becerra C., Bowman S., Oliver K., Preuss M., Sanchez C.P., Schneider N.K., Villalobos J.M., Rajandream M.A., Harris D., et al. A superfamily of variant genes encoded in the subtelomeric region of Plasmodium vivax. Nature 2001, 410:839-842.
60. Nash T.E. Surface antigenic variation in Giardia lamblia. Mol Microbiol 2002, 45:585-590.
61. Baida R.C.P., Santos M.R.M., Carmo M.S., Yoshida N., Ferreira D., Ferreira A.T., El Sayed N.M., Andersson B., da Silveira J.F. Molecular characterization of serine-, alanine-, and proline-rich proteins of Trypanosoma cruzi and their possible role in host cell infection. Infect Immun 2006, 74:1537-1546.
62. Nakjang S., Williams T.A., Heinz E., Watson A.K., Foster P.G., Sendra K.M., Heaps S.E., Hirt R.P., Martin Embley T. Reduction and expansion in microsporidian genome evolution: new insights from comparative genomics. Genome Biol Evol 2013, 5:2285-2303.
63. Gupta A., Thiruvengadam G., Desai S.A. The conserved clag multigene family of malaria parasites: essential roles in host-pathogen interaction. Drug Resist Updat 2015, 18:47-54.
64. Brown C.A., Murray A.W., Verstrepen K.J. Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Curr Biol 2010, 20:895-903.
65. Lafay B., Sharp P.M. Synonymous codon usage variation among Giardia lamblia genes and isolates. Mol Biol Evol 1999, 16:1484-1495.
66. Prucca C.G., Slavin I., Quiroga R., Elías E.V., Rivero F.D., Saura A., Carranza P.G., Luján H.D. Antigenic variation in Giardia lamblia is regulated by RNA interference. Nature 2008, 456:750-754.
67. Dujon B., Sherman D., Fischer G., Durrens P., Casaregola S., Lafontaine I., De Montigny J., Marck C., Neuvéglise C., Talla E., et al. Genome evolution in yeasts. Nature 2004, 430:35-44.
68. Mogi T., Kita K. Diversity in mitochondrial metabolic pathways in parasitic protists Plasmodium and Cryptosporidium. Parasitol Int 2010, 59:305-312.
69. Seeber F., Limenitakis J., Soldati-Favre D. Apicomplexan mitochondrial metabolism: a story of gains, losses and retentions. Trends Parasitol 2008, 24:468-478.
70. Keithly J.S., Langreth S.G., Buttle K.F., Mannella C.A. Electron tomographic and ultrastructural analysis of the Cryptosporidium parvum relict mitochondrion, its associated membranes, and organelles. J Eukaryot Microbiol 2005, 52:132-140.
71. Smíd O., Matusková A., Harris S.R., Kucera T., Novotný M., Horváthová L., Hrdý I., Kutejová E., Hirt R.P., Embley T.M., et al. Reductive evolution of the mitochondrial processing peptidases of the unicellular parasites Trichomonas vaginalis and Giardia intestinalis. PLoS Pathog 2008, 4:e1000243.
72. Dolezal P., Dagley M.J., Kono M., Wolynec P., Likić V.A., Foo J.H., Sedinová M., Tachezy J., Bachmann A., Bruchhaus I., et al. The essentials of protein import in the degenerate mitochondrion of Entamoeba histolytica. PLoS Pathog 2010, 6:e1000812.
73. Jackson A.P., Quail M.A., Berriman M. Insights into the genome sequence of a free-living Kinetoplastid: Bodo saltans (Kinetoplastida: Euglenozoa). BMC Genomics 2008, 9:594.
74. Mitreva M., Jasmer D.P., Zarlenga D.S., Wang Z., Abubucker S., Martin J., Taylor C.M., Yin Y., Fulton L., Minx P., et al. The draft genome of the parasitic nematode Trichinella spiralis. Nat Genet 2011, 43:228-235.
75. Hjort K., Goldberg A.V., Tsaousis A.D., Hirt R.P., Embley T.M. Diversity and reductive evolution of mitochondria among microbial eukaryotes. Philos Trans R Soc Lond B Biol Sci 2010, 365:713-727.
76. Muller H.J. The relation of recombination to mutational advance. Mutat Res 1964, 106:2-9.
77. Mira A., Ochman H., Moran N.A. Deletional bias and the evolution of bacterial genomes. Trends Genet 2001, 17:589-596.
78. Williams B.A.P., Hirt R.P., Lucocq J.M., Embley T.M. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 2002, 418:865-869.
79. Tovar J., Fischer A., Clark C.G. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol Microbiol 1999, 32:1013-1021.
80. Tovar J., León-Avila G., Sánchez L.B., Sutak R., Tachezy J., van der Giezen M., Hernández M., Müller M., Lucocq J.M. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 2003, 426:172-176.
81. Clark C.G., Roger A.J. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc Natl Acad Sci U S A 1995, 92:6518-6521.
82. Aguilera P., Barry T., Tovar J. Entamoeba histolytica mitosomes: organelles in search of a function. Exp Parasitol 2008, 118:10-16.
83. Van der Giezen M. Hydrogenosomes and mitosomes: conservation and evolution of functions. J Eukaryot Microbiol 2009, 56:221-231.
84. Léon-Avila G., Tovar J. Mitosomes of Entamoeba histolytica are abundant mitochondrion-related remnant organelles that lack a detectable organellar genome. Microbiology 2004, 150:1245-1250.
85. Anderson I.J., Loftus B.J. Entamoeba histolytica: observations on metabolism based on the genome sequence. Exp Parasitol 2005, 110:173-177.
86. Cavalier-Smith T., Chao E.E. Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.). Eur J Protistol 2004, 40:185-212.
87. Seeber F., Soldati-Favre D. Metabolic pathways in the apicoplast of apicomplexa. Int Rev Cell Mol Biol 2010, 281:161-228.
88. Ralph S.A., van Dooren G.G., Waller R.F., Crawford M.J., Fraunholz M.J., Foth B.J., Tonkin C.J., Roos D.S., McFadden G.I. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2004, 2:203-216.
89. Abrahamsen M.S., Templeton T.J., Enomoto S., Abrahante J.E., Zhu G., Lancto C.A., Deng M., Liu C., Widmer G., Tzipori S., et al. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 2004, 304:441-445.
90. Andersson S.G., Kurland C.G. Reductive evolution of resident genomes. Trends Microbiol 1998, 6:263-268.
91. Bromham L., Cowman P.F., Lanfear R. Parasitic plants have increased rates of molecular evolution across all three genomes. BMC Evol Biol 2013, 13:126.
92. Gregory T.R. The bigger the C-value, the larger the cell: genome size and red blood cell size in vertebrates. Blood Cells Mol Dis 2001, 27:830-843.
93. Gregory T.R. Genome size and developmental complexity. Genetica 2002, 115:131-146.
94. Gilleard J.S. The use of Caenorhabditis elegans in parasitic nematode research. Parasitology 2004, 128(Suppl 1):S49-S70.
95. Dieterich C., Clifton S.W., Schuster L.N., Chinwalla A., Delehaunty K., Dinkelacker I., Fulton L., Fulton R., Godfrey J., Minx P., et al. The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nat Genet 2008, 40:1193-1198.
96. Guiliano D., Hall N., Jones S., Clark L., Corton C., Barrell B., Blaxter M. Conservation of long-range synteny and microsynteny between the genomes of two distantly related nematodes. Genome Biol 2002, 3. RESEARCH0057.
97. Kutisova K., Kulda J., Cepicka I., Flegr J., Koudela B., Teras J., Tachezy J. Tetratrichomonads from the oral cavity and respiratory tract of humans. Parasitology 2005, 131:309-319.
98. Deceliere G., Charles S., Biémont C. The dynamics of transposable elements in structured populations. Genetics 2005, 169:467-474.
99. Felsenstein J. The evolutionary advantage of recombination. Genetics 1974, 78:737-756.
100. Hertz-Fowler C., Figueiredo L.M., Quail M.A., Becker M., Jackson A., Bason N., Brooks K., Churcher C., Fahkro S., Goodhead I., et al. Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS One 2008, 3:e3527.
101. Sundberg L.-R., Pulkkinen K. Genome size evolution in macroparasites. Int J Parasitol 2015, 45:285-288.
102. Koonin E.V., Wolf Y.I. Constraints and plasticity in genome and molecular-phenome evolution. Nat Rev Genet 2010, 11:487-498.
103. Pan G., Xu J., Li T., Xia Q., Liu S.-L., Zhang G., Li S., Li C., Liu H., Yang L., et al. Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation. BMC Genomics 2013, 14:186.