Phylogenomic study indicates widespread lateral gene transfer in Entamoeba and suggests a past intimate relationship with parabasalids

Genome Biology and Evolution

Volumn 6, Issue 9, 2014, Pages 2350-2360

  Grant, Jessica R ^a   Katz, Laura A ^a,b  

^a SMITH COLLEGE   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

HGT; Horizontal gene transfer; LGT; Microbial eukaryotes; Parasites; Trichomonas vaginalis

Indexed keywords

ARCHAEON; BACTERIUM; CLASSIFICATION; ENTAMOEBA; GENETICS; GENOME; HORIZONTAL GENE TRANSFER; MOLECULAR EVOLUTION; PARABASALIA; PHYLOGENY;

ARCHAEA; BACTERIA; ENTAMOEBA; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENOME; PARABASALIDEA; PHYLOGENY;

EID: 84916932905     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu179     Document Type: Article

References (65)

1. Ali V, Hashimoto T, Shigeta Y, Nozaki T. 2004. Molecular and biochemical characterization of D-phosphoglycerate dehydrogenase from Entamoeba histolytica. A unique enteric protozoan parasite that possesses both phosphorylated and nonphosphorylated serine metabolic pathways. Eur J Biochem. 271:2670-2681.
2. Ali V, Shigeta Y, Tokumoto U, Takahashi Y, Nozaki T. 2004. An intestinal parasitic protist, Entamoeba histolytica, possesses a non-redundant nitrogen fixation-like system for iron-sulfur cluster assembly under anaerobic conditions. J Biol Chem. 279:16863-16874.
3. Alsmark C, et al. 2013. Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes. Genome Biol. 14:R19.
4. Alsmark UC, et al. 2009. Horizontal gene transfer in eukaryotic parasites: a case study of Entamoeba histolytica and Trichomonas vaginalis. Methods Mol Biol. 532:489-500.
5. Anderson IJ, Loftus BJ. 2005. Entamoeba histolytica: observations on metabolism based on the genome sequence. Exp Parasitol. 110:173-177.
6. Andersson JO. 2005. Lateral gene transfer in eukaryotes. Cell Mol Life Sci. 62:1182-1197.
7. Andersson JO, Sjogren AM, Davis LAM, Embley TM, Roger AJ. 2003. Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr Biol. 13:94-104.
8. Baltrus DA. 2013. Exploring the costs of horizontal gene transfer. Trends Ecol Evol. 28:489-495.
9. Beiko RG, Ragan MA. 2009. Untangling hybrid phylogenetic signals: horizontal gene transfer and artifacts of phylogenetic reconstruction. Methods Mol Biol. 532:241-256.
10. Bork PD, Doolittle RF. 1992. Proposed acquisition of an animal protein domain by bacteria. Proc Natl Acad Sci USA. 89:8990-8994.
11. Cavalier-Smith T. 1998. A revised six-kingdom system of life. Biol Rev Camb Philos Soc. 73:203-266.
12. Chen F, Mackey AJ, Stoeckert CJ, Roos DS. 2006. OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res. 34:D363-D368.
13. Clark CG, et al. 2007. Structure and content of the Entamoeba histolytica genome. Adv Parasitol. 65:51-190.
14. Clarke M, et al. 2013. Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling. Genome Biol. 14:R11.
15. Cohen O, Gophna U, Pupko T. 2011. The complexity hypothesis revisited: connectivity rather than function constitutes a barrier to horizontal gene Transfer. Mol Biol Evol. 28:1481-1489.
16. Cohen O, Pupko T. 2010. Inference and characterization of horizontally transferred gene families using stochastic mapping. Mol Biol Evol. 27:703-713.
17. Conesa A, et al. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674-3676.
18. Doolittle RF. 1994. Convergent evolution: the need to be explicit. Trends Biochem Sci. 19:15-18.
19. Embley TM. 2006. Multiple secondary origins of the anaerobic lifestyle in eukaryotes. Philos Trans R Soc B Biol Sci. 361:1055-1067.
20. Fokin SI, Di Giuseppe G, Erra F, Dini F. 2008. Euplotespora binucleata n. Gen., n. Sp (protozoa: microsporidia), a parasite infecting the hypotrichous ciliate Euplotes woodruffi, with observations on microsporidian infections in Ciliophora. J Eukaryot Microbiol. 55:214-228.
21. Fokin SI, Schrallhammer M, Chiellini C, Verni F, Petroni G. 2014. Free-living ciliates as potential reservoirs for eukaryotic parasites: occurrence of a trypanosomatid in the macronucleus of Euplotes encysticus. Parasit Vectors. 7:203.
22. Foster PG. 2004. Modeling compositional heterogeneity. Syst Biol. 53:485-495.
23. Gandbhir M, Rasched I, Marliere P, Mutzel R. 1995. Convergent evolution of amino-acid usage in archaebacterial and eubacterial lineages adapted to high-salt. Res Microbiol. 146:113-120.
24. Ginger ML. 2006. Niche metabolism in parasitic protozoa. Philos Trans R Soc B Biol Sci. 361:101-118.
25. Ginger ML, Fritz-Laylin LK, Fulton C, Cande WZ, Dawson SC. 2010. Intermediary metabolism in protists: a sequence-based view of facultative anaerobic metabolism in evolutionarily diverse eukaryotes. Protist 161:642-671.
26. Gogarten JP, Olendzenski L. 1999. Orthologs, paralogs and genome comparisons. Curr Opin Genet Dev. 9:630-636.
27. Gomaa F, et al. 2014. One alga to rule them all: unrelated mixotrophic testate amoebae (amoebozoa, rhizaria and stramenopiles) share the same symbiont (trebouxiophyceae). Protist 165:161-176.
28. Grant JR, Katz LA. 2014. Building a phylogenomic pipeline for the eukaryotic tree of life-addressing deep phylogenies with genomescale data. PLoS Curr., Advance Access published April 2, 2014, doi: 10.1371/currents.tol.c24b6054aebf3602748ac042ccc8f2e9.
29. Hug LA, Stechmann A, Roger AJ. 2010. Phylogenetic distributions and histories of proteins involved in anaerobic pyruvate metabolism in eukaryotes. Mol Biol Evol. 27:311-324.
30. Imanian B, Keeling PJ. 2014. Horizontal gene transfer and redundancy of tryptophan biosynthetic enzymes in dinotoms. Genome Biol Evol. 6:333-343.
31. Katz LA. 2002. Lateral gene transfers and the evolution of eukaryotes: theories and data. Int J Syst Evol Microbiol. 52:1893-1900.
32. Keeling PJ. 2009. Functional and ecological impacts of horizontal gene transfer in eukaryotes. Curr Opin Genet Dev. 19:613-619.
33. Keeling PJ, Palmer JD. 2008. Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet. 9:605-618.
34. Kurland CG, Canback B, Berg OG. 2003. Horizontal gene transfer: a critical view. Proc Natl Acad Sci USA. 100:9658-9662.
35. Lake JA, Rivera MC. 2004. Deriving the genomic tree of life in the presence of horizontal gene transfer: conditioned reconstruction. Mol Biol Evol. 21:681-690.
36. Le PT, et al. 2012. An automated approach for the identification of horizontal gene transfers from complete genomes reveals the rhizome of Rickettsiales. BMC Evol Biol. 12:243.
37. Li L, Stoeckert CJ, Roos DS. 2003. OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178-2189.
38. Liu K, Linder CR, Warnow T. 2011. RAxML and FastTree: comparing two methods for large-scale maximum likelihood phylogeny estimation. PLoS One 6:e27731.
39. Loftus B, et al. 2005. The genome of the protist parasite Entamoeba histolytica. Nature 433:865-868.
40. Loftus BJ, Hall N. 2005. Entamoeba: still more to be learned from the genome. Trends Parasitol. 21:453-453.
41. Lorenzi HA, et al. 2010. New assembly, reannotation and analysis of the Entamoeba histolytica genome reveal new genomic features and protein content information. PLoS Neglect Trop Dis. 4:e716.
42. Lühe M. 1913. Erstes urreich der tiere. In: Lang A, editor. Handbuch der Morphologie der Wirbellosen Tiere. Jena: G. Fischer.
43. Martin W. 2005. Molecular evolution-lateral gene transfer and other possibilities. Heredity 94:565-566.
44. Nixon JEJ, 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.
45. Oren A. 1995. Convergent evolution of amino acid usage in archaebacterial and eubacterial lineages adapted to high salt-comment. Res Microbiol. 146:805-806.
46. Penn O, et al. 2010. GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res. 38:W23-W28.
47. Price MN, Dehal PS, Arkin AP. 2009. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol. 26:1641-1650.
48. Price MN, Dehal PS, Arkin AP. 2010. FastTree 2-approximately maximumlikelihood trees for large alignments. PLoS One 5:e9490.
49. Ragan MA. 2001. On surrogate methods for detecting lateral gene transfer. FEMS Microbiol Lett. 201:187-191.
50. Ricard G, et al. 2006. Horizontal gene transfer from bacteria to rumen ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment. BMC Genomics 7:22.
51. Richards TA, Hirt RP, Williams BAP, Embley TM. 2003. Horizontal gene transfer and the evolution of parasitic protozoa. Protist 154:17-32.
52. Rosenthal B, et al. 1997. Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica. J Bacteriol. 179:3736-3745.
53. Shimodaira H, Hasegawa M. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246-1247.
54. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
55. Stamatakis A, Hoover P, Rougemont J. 2008. A rapid bootstrap algorithm for the RAxML web servers. Syst Biol. 57:758-771.
56. Stamatakis A, Ludwig T, Meier H. 2005. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456-463.
57. Stanley SL. 2003. Amoebiasis. Lancet 361:1025-1034.
58. Stanley SL Jr. 2005. The Entamoeba histolytica genome: something old, something new, something borrowed and sex too? Trends Parasitol. 21:451-453.
59. Tanifuji G, et al. 2011. Genomic characterization of Neoparamoeba pemaquidensis (amoebozoa) and its kinetoplastid endosymbiont. Eukaryot Cell. 10:1143-1146.
60. Tomii K, Sawada Y, Honda S. 2012. Convergent evolution in structural elements of proteins investigated using cross profile analysis. BMC Bioinformatics 13:11.
61. Tsaousis AD, et al. 2012. Evolution of Fe/S cluster biogenesis in the anaerobic parasite Blastocystis. Proc Natl Acad Sci USA. 109:10426-10431.
62. Umejiego NN, et al. 2008. Targeting a prokaryotic protein in a eukaryotic pathogen: identification of lead compounds against cryptosporidiosis (vol 15, pg 70, 2008). Chem Biol. 15:200-200.
63. Wolf YI, Koonin EV. 2013. Genome reduction as the dominant mode of evolution. Bioessays 35:829-837.
64. Yang W, Li E, Kairong T, Stanley SL Jr. 1994. Entamoeba histolytica has an alcohol dehydrogenase homologous to the multifunctional adhE gene product of Escherichia coli. Mol Biochem Parasitol. 64:253-260.
65. Zmasek CM, Godzik A. 2011. Strong functional patterns in the evolution of eukaryotic genomes revealed by the reconstruction of ancestral protein domain repertoires. Genome Biol. 12:13.