Advertisement

Horizontal Gene Transfer in Obligate Parasites

  • J. M. AgeitosEmail author
  • M. Viñas
  • T. G. Villa
Chapter

Abstract

Parasitism entails a tight interaction between host, parasites, and the host’s commensal organisms; this derives into a coevolution process that in turn represents an extreme parasite specialization, associated with reductive evolution and streamlining. Horizontal gene transfer (HGT), as the asexual transfer of genetic material between or among distantly related species, may play an important role in host-parasite relations. HGT is especially important in the prokaryotic genome evolution; however, HGT is also present in eukaryotic genomes, for instance, the exchange of genetic sequences with organelles, endosymbiotic microorganisms, or even parasite genomes, and the host nucleus. Although parasitic symbiosis is classically defined as an arms race between host defenses and parasites, it has been identified the expression of exogenous parasitic genes in the host that provide selective advantages. Notwithstanding, the main part of HGT events in parasites takes place between them and commensal organisms, enabling selective advantages for the parasites. In this chapter, we will discuss some interesting cases of HGT in parasites that affect and belong to different kingdoms and the importance of this process in host-parasite coevolution.

Keywords

Horizontal gene transfer Obligate parasites Wolbachia Chlamydia Microsporidia Parasitic plants 

References

  1. Adato O, Ninyo N, Gophna U, Snir S (2015) Detecting horizontal gene transfer between closely related taxa. PLoS Comput Biol 11:1–23.  https://doi.org/10.1371/journal.pcbi.1004408 CrossRefGoogle Scholar
  2. Alam U, Medlock J, Brelsfoard C et al (2011) Wolbachia symbiont infections induce strong cytoplasmic incompatibility in the Tsetse fly glossina morsitans. PLoS Pathog 7.  https://doi.org/10.1371/journal.ppat.1002415 CrossRefGoogle Scholar
  3. Alexander WG, Wisecaver JH, Rokas A, Hittinger CT (2016) Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides. Proc Natl Acad Sci USA 113:4116–4121.  https://doi.org/10.1073/pnas.1517242113 CrossRefPubMedGoogle Scholar
  4. Alsmark C, Sicheritz-Ponten T, Foster PG et al (2009) Horizontal gene transfer in eukaryotic parasites: a case study of Entamoeba histolytica and Trichomonas vaginalis. In: Gogarten MB, Gogarten JP, Olendzenski L (eds) Horizontal gene transfer: genomes in flux. Humana, New York, pp 489–500CrossRefGoogle Scholar
  5. Alsmark C, Foster PG, Sicheritz-Ponten T et al (2013) Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes. Genome Biol 14:R19.  https://doi.org/10.1186/gb-2013-14-2-r19 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Ankarklev J, Jerlström-Hultqvist J, Ringqvist E et al (2010) Behind the smile: cell biology and disease mechanisms of Giardia species. Nat Rev Microbiol 8:413–422.  https://doi.org/10.1038/nrmicro2317 CrossRefPubMedGoogle Scholar
  7. Bar D (2011) Evidence of massive horizontal gene transfer between humans and Plasmodium vivax. Nat Preced 1–17.  https://doi.org/10.1038/npre.2011.5690.1
  8. Becq J, Churlaud C, Deschavanne P (2010) A benchmark of parametric methods for horizontal transfers detection. PLoS One 5:1–9.  https://doi.org/10.1371/journal.pone.0009989 CrossRefGoogle Scholar
  9. Beiko RG, Ragan MA (2009) Untangling hybrid phylogenetic signals: horizontal gene transfer and artifacts of phylogenetic reconstruction. In: Gogarten MB, Gogarten JP, Olendzenski LC (eds) Horizontal gene transfer: genomes in flux. Humana, Totowa, NJ, pp 241–256CrossRefGoogle Scholar
  10. Birschwilks M, Haupt S, Hofius D, Neumann S (2006) Transfer of phloem-mobile substances from the host plants to the holoparasite Cuscuta sp. J Exp Bot 57:911–921.  https://doi.org/10.1093/jxb/erj076 CrossRefPubMedGoogle Scholar
  11. Bohne W, Böttcher K, Groß U (2011) The parasitophorous vacuole of Encephalitozoon cuniculi: biogenesis and characteristics of the host cell-pathogen interface. Int J Med Microbiol 301:395–399.  https://doi.org/10.1016/j.ijmm.2011.04.006 CrossRefPubMedGoogle Scholar
  12. Bordenstein SR, Reznikoff WS (2005) Mobile DNA in obligate intracellular bacteria. Nat Rev Microbiol 3:688–699.  https://doi.org/10.1038/nrmicro1233 CrossRefPubMedGoogle Scholar
  13. Brelsfoard C, Tsiamis G, Falchetto M et al (2014) Presence of extensive Wolbachia symbiont insertions discovered in the genome of its host glossina morsitans morsitans. PLoS Negl Trop Dis 8:e2728.  https://doi.org/10.1371/journal.pntd.0002728 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Colwell AEL, Watson KC, Schneider AC (2017) A new species of Aphyllon (Orobanchaceae) parasitic on Galium in the Western USA. Madroño 64:99–107.  https://doi.org/10.3120/0024-9637-64.3.99 CrossRefGoogle Scholar
  15. Corradi N (2015) Microsporidia: eukaryotic intracellular parasites shaped by gene loss and horizontal gene transfers. Annu Rev Microbiol 69:167–183.  https://doi.org/10.1146/annurev-micro-091014-104136 CrossRefPubMedGoogle Scholar
  16. Cotton JA, Lilley CJ, Jones LM, et al (2014) The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. Genome Biol 15.  https://doi.org/10.1186/gb-2014-15-3-r43 CrossRefGoogle Scholar
  17. Danchin EGJ, Rosso M-N, Vieira P et al (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci USA 107:17651–17656.  https://doi.org/10.1073/pnas.1008486107 CrossRefPubMedGoogle Scholar
  18. Danchin EGJ, Guzeeva EA, Mantelin S et al (2016) Horizontal gene transfer from bacteria has enabled the plant-parasitic nematode Globodera pallida to feed on host-derived sucrose. Mol Biol Evol 33:1571–1579.  https://doi.org/10.1093/molbev/msw041 CrossRefPubMedGoogle Scholar
  19. Davis CC, Xi Z (2015) Horizontal gene transfer in parasitic plants. Curr Opin Plant Biol 26:14–19.  https://doi.org/10.1016/j.pbi.2015.05.008 CrossRefPubMedGoogle Scholar
  20. Davis CC, Anderson WR, Wurdack KJ (2005) Gene transfer from a parasitic flowering plant to a fern. Proc R Soc B Biol Sci 272:2237–2242.  https://doi.org/10.1098/rspb.2005.3226 CrossRefGoogle Scholar
  21. Deitsch KW, Carlton JM-R, Wootton JC, Wellems TE (2001) Host sequences in Plasmodium falciparum and Plasmodium vivax genomic DNA: horizontal transfer or contamination artifact? FEBS Lett 491:164–165.  https://doi.org/10.1016/S0014-5793(01)02154-8 CrossRefPubMedGoogle Scholar
  22. de Koning AP, Brinkman FSL, Jones SJM, Keeling PJ (2000) Lateral gene transfer and metabolic adaptation in the human parasite Trichomonas vaginalis. Mol Biol Evol 17:1769–1773.  https://doi.org/10.1093/oxfordjournals.molbev.a026275 CrossRefPubMedGoogle Scholar
  23. Delavault P, Montiel G, Brun G, et al (2017) Communication between host plants and parasitic plants. Elsevier, LondonCrossRefGoogle Scholar
  24. DeMarco R, Mathieson W, Dillon GP, Alan Wilson R (2007) Schistosome albumin is of host, not parasite, origin. Int J Parasitol 37:1201–1208.  https://doi.org/10.1016/j.ijpara.2007.03.004 CrossRefPubMedGoogle Scholar
  25. Djuika C, Huerta-Cepas J, Przyborski J et al (2015) Prokaryotic ancestry and gene fusion of a dual localized peroxiredoxin in malaria parasites. Microb Cell 2:5–13.  https://doi.org/10.15698/mic2015.01.182 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Dörr I, Kollmann R (1995) Symplasmic sieve element continuity between Orobanche and its host. Bot Acta 108:47–55.  https://doi.org/10.1111/j.1438-8677.1995.tb00830.x CrossRefGoogle Scholar
  27. Drezen JM, Gauthier J, Josse T et al (2017) Foreign DNA acquisition by invertebrate genomes. J Invertebr Pathol 147:157–168.  https://doi.org/10.1016/j.jip.2016.09.004 CrossRefPubMedGoogle Scholar
  28. Dunning Hotopp JC (2011) Horizontal gene transfer between bacteria and animals. Trends Genet 27:157–163.  https://doi.org/10.1016/j.tig.2011.01.005 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Elmer JJ, Christensen MD, Rege K (2013) Applying horizontal gene transfer phenomena to enhance non-viral gene therapy. J Control Release 172:246–257.  https://doi.org/10.1016/j.jconrel.2013.08.025 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Elwell C, Mirrashidi K, Engel J (2016) Chlamydia cell biology and pathogenesis. Nat Rev Microbiol 14:385–400.  https://doi.org/10.1038/nrmicro.2016.30 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Eme L, Gentekaki E, Curtis B et al (2017) Lateral gene transfer in the adaptation of the anaerobic parasite blastocystis to the gut. Curr Biol 27:807–820.  https://doi.org/10.1016/j.cub.2017.02.003 CrossRefPubMedGoogle Scholar
  32. Fast NM, Law JS, Williams BAP, Keeling PJ (2003) Bacterial catalase in the microsporidian Nosema locustae: implications for microsporidian metabolism and genome evolution. Eukaryot Cell 2:1069–1075.  https://doi.org/10.1128/EC.2.5.1069-1075.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Gandini CL, Sanchez-Puerta MV (2017) Foreign plastid sequences in plant mitochondria are frequently acquired via mitochondrion-to-mitochondrion horizontal transfer. Sci Rep 7:1–8.  https://doi.org/10.1038/srep43402 CrossRefGoogle Scholar
  34. Gasmi L, Boulain H, Gauthier J et al (2015) Recurrent domestication by Lepidoptera of genes from their parasites mediated by bracoviruses. PLoS Genet 11:1–32.  https://doi.org/10.1371/journal.pgen.1005470 CrossRefGoogle Scholar
  35. Gluck-Thaler E, Slot JC (2015) Dimensions of horizontal gene transfer in eukaryotic microbial pathogens. PLoS Pathog 11:1–7.  https://doi.org/10.1371/journal.ppat.1005156 CrossRefGoogle Scholar
  36. Grunau C, Boissier J (2010) No evidence for lateral gene transfer between salmonids and schistosomes. Nat Genet 42:918–919.  https://doi.org/10.1038/ng1110-918 CrossRefPubMedGoogle Scholar
  37. Hecht MM, Nitz N, Araujo PF et al (2010) Inheritance of DNA transferred from American trypanosomes to human hosts. PLoS One 5.  https://doi.org/10.1371/journal.pone.0009181 CrossRefGoogle Scholar
  38. Hotopp JCD, Clark ME, Oliveira DCSG et al (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317:1753–1756.  https://doi.org/10.1126/science.1142490 CrossRefGoogle Scholar
  39. Huang J (2013) Horizontal gene transfer in eukaryotes: the weak-link model. BioEssays 35:868–875.  https://doi.org/10.1002/bies.201300007 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Huang Q (2018) Evolution of Dicer and Argonaute orthologs in microsporidian parasites. Infect Genet Evol 65:329–332.  https://doi.org/10.1016/j.meegid.2018.08.011 CrossRefPubMedGoogle Scholar
  41. Huang J, Mullapudi N, Lancto CA et al (2004a) Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol 5:R88.  https://doi.org/10.1186/gb-2004-5-11-r88 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Huang J, Mullapudi N, Sicheritz-Ponten T, Kissinger JC (2004b) A first glimpse into the pattern and scale of gene transfer in the Apicomplexa. Int J Parasitol 34:265–274.  https://doi.org/10.1016/j.ijpara.2003.11.025 CrossRefPubMedGoogle Scholar
  43. Huang W, Tsai L, Li Y et al (2017) Widespread of horizontal gene transfer in the human genome. BMC Genomics 18:1–11.  https://doi.org/10.1186/s12864-017-3649-y CrossRefGoogle Scholar
  44. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267.  https://doi.org/10.1093/molbev/msj030 CrossRefPubMedGoogle Scholar
  45. Ioannidis P, Johnston KL, Riley DR et al (2013) Extensively duplicated and transcriptionally active recent lateral gene transfer from a bacterial Wolbachia endosymbiont to its host filarial nematode Brugia malayi. BMC Genomics 14:20–30.  https://doi.org/10.1186/1471-2164-14-639 CrossRefGoogle Scholar
  46. Iranzo J, Koonin EV (2018) How genetic parasites persist despite the purge of natural selection. EPL (Europhys Lett) 122:58001.  https://doi.org/10.1209/0295-5075/122/58001 CrossRefGoogle Scholar
  47. Iranzo J, Puigbo P, Lobkovsky AE et al (2016) Inevitability of genetic parasites. Genome Biol Evol 8:2856–2869.  https://doi.org/10.1093/gbe/evw193 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Johny S, Larson TM, Solter LF et al (2009) Phylogenetic characterization of Encephalitozoon romaleae (Microsporidia) from a grasshopper host: relationship to Encephalitozoon spp. infecting humans. Infect Genet Evol 9:189–195.  https://doi.org/10.1016/j.meegid.2008.10.010 CrossRefPubMedGoogle Scholar
  49. Kim H, Kwak W, Yoon SH et al (2018) Horizontal gene transfer of chlamydia: novel insights from tree reconciliation. PLoS One 13:1–14.  https://doi.org/10.1371/journal.pone.0195139 CrossRefGoogle Scholar
  50. Kishore SP, Stiller JW, Deitsch KW (2013) Horizontal gene transfer of epigenetic machinery and evolution of parasitism in the malaria parasite Plasmodium falciparum and other apicomplexans. BMC Evol Biol 13:37.  https://doi.org/10.1186/1471-2148-13-37 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Klasson L, Kambris Z, Cook PE et al (2009) Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti. BMC Genomics 10:1–9.  https://doi.org/10.1186/1471-2164-10-33 CrossRefGoogle Scholar
  52. Ku C, Nelson-Sathi S, Roettger M et al (2015) Endosymbiotic gene transfer from prokaryotic pangenomes: inherited chimerism in eukaryotes. Proc Natl Acad Sci USA 112:10139–10146.  https://doi.org/10.1073/pnas.1421385112 CrossRefPubMedGoogle Scholar
  53. Kwiatkowski DP (2005) How malaria has affected the human genome and what human genetics can teach us about malaria. Am J Hum Genet 77:171–192.  https://doi.org/10.1086/432519 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Kwolek D, Denysenko-Bennett M, Góralski G et al (2017) The first evidence of a host-to-parasite mitochondrial gene transfer in Orobanchaceae. Acta Biol Cracoviensia Ser Bot 59:13–22.  https://doi.org/10.1515/abcsb-2016-0021 CrossRefGoogle Scholar
  55. Laha T, Loukas A, Wattanasatitarpa S et al (2007) The bandit, a new DNA transposon from a hookworm—possible horizontal genetic transfer between host and parasite. PLoS Negl Trop Dis 1.  https://doi.org/10.1371/journal.pntd.0000035 CrossRefGoogle Scholar
  56. Lee SC, Weiss LM, Heitman J (2009) Generation of genetic diversity in microsporidia via sexual reproduction and horizontal gene transfer. Commun Integr Biol 2:414–417.  https://doi.org/10.4161/cib.2.5.8846 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Lena G, Walker JM (2009) Horizontal gene transfer: genomes in flux. Humana, Totowa, NJGoogle Scholar
  58. Ley RE, Lozupone CA, Hamady M et al (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nat Rev Microbiol 6:776–788.  https://doi.org/10.1038/nrmicro1978 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Li X, Zhang TC, Qiao Q et al (2013) Complete chloroplast genome sequence of holoparasite Cistanche deserticola (Orobanchaceae) reveals gene loss and horizontal gene transfer from its host Haloxylon ammodendron (Chenopodiaceae). PLoS One 8:e58747.  https://doi.org/10.1371/journal.pone.0058747 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Lukeš J, Husník F (2018) Microsporidia: a single horizontal gene transfer drives a great leap forward. Curr Biol 28:R712–R715.  https://doi.org/10.1016/j.cub.2018.05.031 CrossRefPubMedGoogle Scholar
  61. Margulis L (2009) Genome acquisition in horizontal gene transfer: symbiogenesis and macromolecular sequence analysis. In: Gogarten MB, Gogarten JP, Olendzenski LC (eds) Horizontal gene transfer: genomes in flux. Humana, Totowa, NJ, pp 181–191CrossRefGoogle Scholar
  62. Martincová E, Voleman L, Pyrih J et al (2015) Probing the biology of giardia intestinalis mitosomes using in vivo enzymatic tagging. Mol Cell Biol 35:2864–2874.  https://doi.org/10.1128/MCB.00448-15 CrossRefPubMedPubMedCentralGoogle Scholar
  63. McNulty SN, Foster JM, Mitreva M et al (2010) Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer. PLoS One 5:e11029.  https://doi.org/10.1371/journal.pone.0011029 CrossRefPubMedPubMedCentralGoogle Scholar
  64. McNulty SN, Abubucker S, Simon GM et al (2012) Transcriptomic and proteomic analyses of a Wolbachia-free filarial parasite provide evidence of trans-kingdom horizontal gene transfer. PLoS One 7:1–12.  https://doi.org/10.1371/journal.pone.0045777 CrossRefGoogle Scholar
  65. Mehrabi R, Bahkali AH, Abd-Elsalam KA et al (2011) Horizontal gene and chromosome transfer in plant pathogenic fungi affecting host range. FEMS Microbiol Rev 35:542–554.  https://doi.org/10.1111/j.1574-6976.2010.00263.x CrossRefPubMedGoogle Scholar
  66. Melamed P, Chong KL, Johansen MV (2004) Evidence for lateral gene transfer from salmonids to two Schistosome species. Nat Genet 36:786–787.  https://doi.org/10.1038/ng0804-786 CrossRefPubMedGoogle Scholar
  67. Mitsumasu K, Seto Y, Yoshida S (2015) Apoplastic interactions between plants and plant root intruders. Front Plant Sci 6:1–17.  https://doi.org/10.3389/fpls.2015.00617 CrossRefGoogle Scholar
  68. Moore ER, Ouellette SP (2014) Reconceptualizing the chlamydial inclusion as a pathogen-specified parasitic organelle: an expanded role for Inc proteins. Front Cell Infect Microbiol 4:1–10.  https://doi.org/10.3389/fcimb.2014.00157 CrossRefGoogle Scholar
  69. Mower JP, Stefanović S, Hao W et al (2010) Horizontal acquisition of multiple mitochondrial genes from a parasitic plant followed by gene conversion with host mitochondrial genes. BMC Biol 8.  https://doi.org/10.1186/1741-7007-8-150
  70. Nagayasu E, Ishikawa SA, Taketani S et al (2013) Identification of a bacteria-like ferrochelatase in Strongyloides venezuelensis, an animal parasitic nematode. PLoS One 8:1–11.  https://doi.org/10.1371/journal.pone.0058458 CrossRefGoogle Scholar
  71. Nixon JEJ, Wang A, Field J 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.  https://doi.org/10.1128/EC.1.2.181 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Pagnier I, Yutin N, Croce O et al (2015) Babela massiliensis, a representative of a widespread bacterial phylum with unusual adaptations to parasitism in amoebae. Biol Direct 10:1–17.  https://doi.org/10.1186/s13062-015-0043-z CrossRefGoogle Scholar
  73. Pan G, Xu J, Li T et al (2013) Comparative genomics of parasitic silkworm microsporidia reveal an association between genome expansion and host adaptation. BMC Genomics 14.  https://doi.org/10.1186/1471-2164-14-186 CrossRefGoogle Scholar
  74. Pombert J-F, Selman M, Burki F et al (2012) Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. Proc Natl Acad Sci USA 109:12638–12643.  https://doi.org/10.1073/pnas.1205020109 CrossRefPubMedGoogle Scholar
  75. Pombert JF, Haag KL, Beidas S et al (2015) The Ordospora colligata genome: evolution of extreme reduction in microsporidia and host-to-parasite horizontal gene transfer. MBio 6.  https://doi.org/10.1128/mBio.02400-14
  76. Qasem JR (2009) Parasitic weeds of the Orobanchaceae family and their natural hosts in Jordan. Weed Biol Manag 9:112–122.  https://doi.org/10.1111/j.1445-6664.2009.00328.x CrossRefGoogle Scholar
  77. Rancurel C, Legrand L, Danchin EGJ (2017) Alienness: rapid detection of candidate horizontal gene transfers across the tree of life. Genes (Basel) 8.  https://doi.org/10.3390/genes8100248 CrossRefGoogle Scholar
  78. Ravenhall M, Škunca N, Lassalle F, Dessimoz C (2015) Inferring horizontal gene transfer. PLoS Comput Biol 11:1–16.  https://doi.org/10.1371/journal.pcbi.1004095 CrossRefGoogle Scholar
  79. Renner SS, Bellot S (2012) Horizontal gene transfer in eukaryotes: fungi-to-plant and plant-to-plant transfers of organellar DNA. In: Bock R, Knoop V (eds) Genomics of chloroplasts and mitochondria, Advances in photosynthesis and respiration. Springer, Dordrecht, pp 223–235CrossRefGoogle Scholar
  80. Ricard G, McEwan NR, Dutilh BE et al (2006) Horizontal gene transfer from bacteria to rumen ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment. BMC Genomics 7:1–13.  https://doi.org/10.1186/1471-2164-7-22 CrossRefGoogle Scholar
  81. Richards TA, Hirt RP, Williams BAP, Embley TM (2003) Horizontal gene transfer and the evolution of parasitic protozoa. Protist 154:17–32.  https://doi.org/10.1078/143446103764928468 CrossRefPubMedGoogle Scholar
  82. Romero M, Cerritos R, Ximenez C (2016) Horizontal gene transfers from bacteria to entamoeba complex: a strategy for dating events along species divergence. J Parasitol Res 2016:1–10.  https://doi.org/10.1155/2016/3241027 CrossRefGoogle Scholar
  83. Sateriale A, Striepen B (2016) Beg, borrow and steal: three aspects of horizontal gene transfer in the protozoan parasite, Cryptosporidium parvum. PLoS Pathog 12:2–6.  https://doi.org/10.1371/journal.ppat.1005429 CrossRefGoogle Scholar
  84. Sayers EW, Barrett T, Benson DA et al (2012) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 40:5–16.  https://doi.org/10.1093/nar/gkr1184 CrossRefGoogle Scholar
  85. Schneider AC, Chun H, Tefanovic S, Baldwin BG (2018) Punctuated plastome reduction and host-parasite horizontal gene transfer in the holoparasitic plant genus Aphyllon. Proc R Soc B Biol Sci 285.  https://doi.org/10.1098/rspb.2018.1535 CrossRefGoogle Scholar
  86. Schönknecht G, Weber APM, Lercher MJ (2014) Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution. BioEssays 36:9–20.  https://doi.org/10.1002/bies.201300095 CrossRefGoogle Scholar
  87. Schwebke JR, Burgess D (2004) Trichomoniasis. Clin Microbiol Rev 17:794–803, Table of contents.  https://doi.org/10.1128/CMR.17.4.794-803.2004 CrossRefGoogle Scholar
  88. Selman M, Corradi N (2011) Microsporidia. Mob Genet Elem 1:251–292.  https://doi.org/10.4161/mge.18611 CrossRefGoogle Scholar
  89. Selman M, Pombert JF, Solter L et al (2011) Acquisition of an animal gene by microsporidian intracellular parasites. Curr Biol 21:R576–R577.  https://doi.org/10.1016/j.cub.2011.06.017 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Soucy SM, Huang J, Gogarten JP (2015) Horizontal gene transfer: building the web of life. Nat Rev Genet 16:472–482.  https://doi.org/10.1038/nrg3962 CrossRefPubMedGoogle Scholar
  91. Stanley SL (2003) Amoebiasis. Lancet (London, England) 361:1025–1034.  https://doi.org/10.1016/S0140-6736(03)12830-9 CrossRefGoogle Scholar
  92. Strese Å, Backlund A, Alsmark C (2014) A recently transferred cluster of bacterial genes in Trichomonas vaginalis—lateral gene transfer and the fate of acquired genes. BMC Evol Biol 14:1–13.  https://doi.org/10.1186/1471-2148-14-119 CrossRefGoogle Scholar
  93. Sun B-F, Xiao J-H, He S et al (2013) Multiple interkingdom horizontal gene transfers in Pyrenophora and closely related species and their contributions to phytopathogenic lifestyles. PLoS One 8:e60029.  https://doi.org/10.1371/journal.pone.0060029 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Sun B, Li T, Xiao J et al (2016a) Contribution of multiple inter-kingdom horizontal gene transfers to evolution and adaptation of amphibian-killing chytrid, Batrachochytrium dendrobatidis. Front Microbiol 7:1–10.  https://doi.org/10.3389/fmicb.2016.01360 CrossRefGoogle Scholar
  95. Sun T, Xu Y, Zhang D et al (2016b) An acyltransferase gene that putatively functions in anthocyanin modification was horizontally transferred from Fabaceae into the genus Cuscuta. Plant Divers 38:149–155.  https://doi.org/10.1016/j.pld.2016.04.002 CrossRefPubMedPubMedCentralGoogle Scholar
  96. Thomas CM, Nielsen KM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711–721.  https://doi.org/10.1038/nrmicro1234 CrossRefPubMedGoogle Scholar
  97. Tomilov AA, Tomilova NB, Wroblewski T et al (2008) Trans-specific gene silencing between host and parasitic plants. Plant J 56:389–397.  https://doi.org/10.1111/j.1365-313X.2008.03613.x CrossRefPubMedGoogle Scholar
  98. Tovar J, León-Avila G, Sánchez LB et al (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172–176.  https://doi.org/10.1038/nature01945 CrossRefPubMedGoogle Scholar
  99. Tsaousis AD, Kunji ERS, Goldberg AV et al (2008) A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453:553–556.  https://doi.org/10.1038/nature06903 CrossRefPubMedGoogle Scholar
  100. Van Der Giezen M, Cox S, Tovar J (2004) The iron-sulfur cluster assembly genes iscS and iscU of Entamoeba histolytica were acquired by horizontal gene transfer. BMC Evol Biol 4:1–9.  https://doi.org/10.1186/1471-2148-4-7 CrossRefGoogle Scholar
  101. Viney M, Kikuchi T (2017) Strongyloides ratti and S. venezuelensis—rodent models of Strongyloides infection. Parasitology 144:285–294.  https://doi.org/10.1017/S0031182016000020 CrossRefPubMedGoogle Scholar
  102. Wasson K, Peper RL (2000) Mammalian microsporidiosis. Vet Pathol 37:113–128.  https://doi.org/10.1354/vp.37-2-113 CrossRefPubMedGoogle Scholar
  103. Weeks AR, Turelli M, Harcombe WR et al (2007) From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5:0997–1005.  https://doi.org/10.1371/journal.pbio.0050114 CrossRefGoogle Scholar
  104. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751.  https://doi.org/10.1038/nrmicro1969 CrossRefPubMedGoogle Scholar
  105. Werren JH, Richards S, Desjardins CA et al (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327:343–348.  https://doi.org/10.1126/science.1178028 CrossRefPubMedGoogle Scholar
  106. WHO (2018) World malaria report 2018Google Scholar
  107. Wijayawardena BK, Minchella DJ, DeWoody JA (2013) Hosts, parasites, and horizontal gene transfer. Trends Parasitol 29:329–338.  https://doi.org/10.1016/j.pt.2013.05.001 CrossRefPubMedGoogle Scholar
  108. Wijayawardena BK, Minchella DJ, Dewoody JA (2015) Horizontal gene transfer in schistosomes: a critical assessment. Mol Biochem Parasitol 201:57–65.  https://doi.org/10.1016/j.molbiopara.2015.05.008 CrossRefPubMedGoogle Scholar
  109. Williams DL, Sayed AA, Ray D, McArthur AG (2006) Schistosoma mansoni albumin, a major defense against oxidative damage, was acquired by lateral gene transfer from a mammalian host. Mol Biochem Parasitol 150:359–363.  https://doi.org/10.1016/j.molbiopara.2006.07.009 CrossRefPubMedGoogle Scholar
  110. Wolf YI, Aravind L, Koonin EV (1999) Rickettsiae and Chlamydiae: evidence of horizontal gene transfer and gene exchange. Trends Genet 15:173–175.  https://doi.org/10.1016/S0168-9525(99)01704-7 CrossRefPubMedGoogle Scholar
  111. Woolfit M, Iturbe-Ormaetxe I, McGraw EA, O’Neill SL (2009) An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis. Mol Biol Evol 26:367–374.  https://doi.org/10.1093/molbev/msn253 CrossRefPubMedGoogle Scholar
  112. Wu M, Sun LV, Vamathevan J et al (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2:327–341.  https://doi.org/10.1371/journal.pbio.0020069 CrossRefGoogle Scholar
  113. Wu B, Novelli J, Jiang D (2013) Interdomain lateral gene transfer of an essential ferrochelatase gene in human parasitic nematodes. Proc Natl Acad Sci USA 110:7748–7753.  https://doi.org/10.1073/pnas.1304049110 CrossRefPubMedGoogle Scholar
  114. Xi Z, Bradley RK, Wurdack KJ et al (2012) Horizontal transfer of expressed genes in a parasitic flowering plant. BMC Genomics 13.  https://doi.org/10.1186/1471-2164-13-227 CrossRefGoogle Scholar
  115. Xi Z, Wang Y, Bradley RK et al (2013) Massive mitochondrial gene transfer in a parasitic flowering plant clade. PLoS Genet 9:1–10.  https://doi.org/10.1371/journal.pgen.1003265 CrossRefGoogle Scholar
  116. Yang Z, Zhang Y, Wafula EK et al (2016) Horizontal gene transfer is more frequent with increased heterotrophy and contributes to parasite adaptation. Proc Natl Acad Sci USA 113:E7010–E7019.  https://doi.org/10.1073/pnas.1608765113 CrossRefPubMedGoogle Scholar
  117. Yoshida S, Maruyama S, Nozaki H, Shirasu K (2010) Horizontal gene transfer by the parasitic plant Striga hermonthica. Science 80(328):1128.  https://doi.org/10.1126/science.1187145 CrossRefGoogle Scholar
  118. Yoshida S, Cui S, Ichihashi Y, Shirasu K (2016) The haustorium, a specialized invasive organ in parasitic plants. Annu Rev Plant Biol 67:643–667.  https://doi.org/10.1146/annurev-arplant-043015-111702 CrossRefPubMedGoogle Scholar
  119. Zamani-Dahaj SA, Okasha M, Kosakowski J, Higgs PG (2016) Estimating the frequency of horizontal gene transfer using phylogenetic models of gene gain and loss. Mol Biol Evol 33:1843–1857.  https://doi.org/10.1093/molbev/msw062 CrossRefPubMedGoogle Scholar
  120. Zhang D, Qi J, Yue J et al (2014a) Root parasitic plant Orobanche aegyptiaca and shoot parasitic plant Cuscuta australis obtained Brassicaceae-specific strictosidine synthase-like genes by horizontal gene transfer. BMC Plant Biol 14:19.  https://doi.org/10.1186/1471-2229-14-19 CrossRefPubMedPubMedCentralGoogle Scholar
  121. Zhang HH, Feschotte C, Han MJ, Zhang Z (2014b) Recurrent horizontal transfers of Chapaev transposons in diverse invertebrate and vertebrate animals. Genome Biol Evol 6:1375–1386.  https://doi.org/10.1093/gbe/evu112 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Microbiology, Faculty of PharmacyUniversity of Santiago de CompostelaSantiago de CompostelaSpain
  2. 2.Department of Pathology and Experimental Therapeutics, Faculty of MedicineUniversity of BarcelonaBarcelonaSpain
  3. 3.Faculty of Pharmacy, Department of MicrobiologyUniversity of Santiago de CompostelaSantiago de CompostelaSpain

Personalised recommendations