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Functional horizontal gene transfer from bacteria to eukaryotes

Nature Reviews Microbiology volume 16, pages 67–79 (2018)Cite this article

Subjects

Key Points

  • Genome fragments are sometimes transferred from bacteria to eukaryotes via horizontal gene transfer (HGT).

  • When these DNA fragments contain genes, these genes can retain their functionality in some cases.

  • If these bacterial sequences are maintained for long periods of time, they can acquire eukaryotic features such as introns.

  • If the eukaryotic recipient retains a stable bacterial endosymbiont, these HGT events can compensate for genome reduction in the endosymbiont.

  • These HGT events can also enable the eukaryotic recipient to protect itself from other organisms, survive in new environments or use new food sources.

  • Further study of neglected eukaryotic groups will help to clarify the frequency of bacteria–eukaryote HGT.

Abstract

Bacteria influence eukaryotic biology as parasitic, commensal or beneficial symbionts. Aside from these organismal interactions, bacteria have also been important sources of new genetic sequences through horizontal gene transfer (HGT) for eukaryotes. In this Review, we focus on gene transfers from bacteria to eukaryotes, discuss how horizontally transferred genes become functional and explore what functions are endowed upon a broad diversity of eukaryotes by genes derived from bacteria. We classify HGT events into two broad types: those that maintain pre-existing functions and those that provide the recipient with new functionality, including altered host nutrition, protection and adaptation to extreme environments.

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Figure 1: Functional horizontal gene transfer events in eukaryotes.
Figure 2: How foreign DNA gains functionality in eukaryotes.
Figure 3: Horizontal gene transfer events targeting peptidoglycan bonds are common across eukaryotes.
Figure 4: Schematic diagrams of maintenance transfers and innovation transfers.

References

  1. Koonin, E. V., Makarova, K. S. & Aravind, L. Horizontal gene transfer in prokaryotes: quantification and classification. Annu. Rev. Microbiol. 55, 709–742 (2001).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  2. Gogarten, J. P. & Townsend, J. P. Horizontal gene transfer, genome innovation and evolution. Nat. Rev. Microbiol. 3, 679–687 (2005).

    Article  CAS  PubMed  Google Scholar 

  3. Thomas, C. M. & Nielsen, K. M. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat. Rev. Microbiol. 3, 711–721 (2005).

    Article  CAS  PubMed  Google Scholar 

  4. Soucy, S. M., Huang, J. & Gogarten, J. P. Horizontal gene transfer: building the web of life. Nat. Rev. Genet. 16, 472–482 (2015).

    Article  CAS  PubMed  Google Scholar 

  5. Koonin, E. V. Horizontal gene transfer: essentiality and evolvability in prokaryotes, and roles in evolutionary transitions. F1000Res. 5, 1805 (2016).

    Article  CAS  Google Scholar 

  6. Wagner, A. et al. Mechanisms of gene flow in archaea. Nat. Rev. Microbiol. 15, 492–501 (2017).

    Article  CAS  PubMed  Google Scholar 

  7. Syvanen, M. Evolutionary implications of horizontal gene transfer. Annu. Rev. Genet. 46, 341–358 (2012).

    Article  CAS  PubMed  Google Scholar 

  8. Doolittle, W. F. et al. What is the tree of life? PLOS Genet. 12, e1005912 (2016).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  9. Philippe, H. & Douady, C. J. Horizontal gene transfer and phylogenetics. Curr. Opin. Microbiol. 6, 498–505 (2003).

    Article  CAS  PubMed  Google Scholar 

  10. Timmis, J. N., Ayliffe, M. A., Huang, C. Y. & Martin, W. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat. Rev. Genet. 5, 123–135 (2004).

    Article  CAS  PubMed  Google Scholar 

  11. Keeling, P. J. & Palmer, J. D. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9, 605–618 (2008).

    Article  CAS  PubMed  Google Scholar 

  12. Alsmark, C. et al. Patterns of prokaryotic lateral gene transfers affecting parasitic microbial eukaryotes. Genome Biol. 14, R19 (2013). This is a systematic reanalysis of 13 parasitic microbial eukaryotes that shows that the majority of HGT events in these species involve genes related to amino acid and sugar metabolism and that putative donors of these genes are significantly enriched in bacterial groups sharing the same habitats.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  13. Schönknecht, G., Weber, A. P. M. & Lercher, M. J. Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution. Bioessays 36, 9–20 (2014).

    Article  PubMed  CAS  Google Scholar 

  14. Lacroix, B. & Citovsky, V. Transfer of DNA from bacteria to eukaryotes. MBio 7, e00863–e00816 (2016).

    Article  PubMed Central  PubMed  Google Scholar 

  15. Robinson, K. M., Sieber, K. B. & Dunning Hotopp, J. C. A review of bacteria-animal lateral gene transfer may inform our understanding of diseases like cancer. PLoS Genet. 9, e1003877 (2013).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  16. Boto, L. Horizontal gene transfer in the acquisition of novel traits by metazoans. Proc. Biol. Sci. 281, 20132450 (2014).

    PubMed Central  PubMed  Google Scholar 

  17. Wybouw, N., Pauchet, Y., Heckel, D. G. & Van Leeuwen, T. Horizontal gene transfer contributes to the evolution of arthropod herbivory. Genome Biol. Evol. 8, 1785–1801 (2016).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Salzberg, S. L. et al. Microbial genes in the human genome: lateral transfer or gene loss? Science 292, 1903–1906 (2001).

    Article  CAS  PubMed  Google Scholar 

  19. Salzberg, S. L. Horizontal gene transfer is not a hallmark of the human genome. Genome Biol. 18, 85 (2017).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  20. Crisp, A. et al. Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes. Genome Biol. 16, 50 (2015).

    Article  PubMed Central  PubMed  Google Scholar 

  21. Lander, E. S. et al. Initial sequencing and analysis of the human genome. Nature 409, 860–921 (2001).

    Article  CAS  PubMed  Google Scholar 

  22. Stanhope, M. J. et al. Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates. Nature 411, 940–944 (2001).

    Article  CAS  PubMed  Google Scholar 

  23. Arakawa, K. No evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. Proc. Natl Acad. Sci. USA 113, E3057 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Koutsovoulos, G. et al. No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini. Proc. Natl Acad. Sci. USA 113, 5053–5058 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Nikoh, N. et al. Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. Plos Genet. 6, e1000827 (2010).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  26. Moran, Y., Fredman, D., Szczesny, P., Grynberg, M. & Technau, U. Recurrent horizontal transfer of bacterial toxin genes to eukaryotes. Mol. Biol. Evol. 29, 2223–2230 (2012). Bacteria use pore-forming toxins to lyse cellular membranes, but this article reveals several independent transfers of the genes for these toxins to eukaryotic genomes and discusses the possible role of those genes in defence and predation of multicellular eukaryotes.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Flot, J. et al. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500, 453–457 (2014).

    Article  CAS  Google Scholar 

  28. Husnik, F. et al. Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153, 1567–1578 (2013).

    Article  CAS  PubMed  Google Scholar 

  29. Wu, B. et al. Interdomain lateral gene transfer of an essential ferrochelatase gene in human parasitic nematodes. Proc. Natl Acad. Sci. USA 110, 7748–7753 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Chou, S. et al. Transferred interbacterial antagonism genes augment eukaryotic innate immune function. Nature 518, 98–101 (2014). This is an important study that shows multiple independent HGT events of genes encoding antibacterial amidases across the tree of life and experimentally verifies their function.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  31. Metcalf, J. A., Funkhouser-Jones, L. J., Brileya, K., Reysenbach, A.-L. & Bordenstein, S. R. Antibacterial gene transfer across the tree of life. eLife 3, e04266 (2014). This article shows and experimentally verifies HGT events for genes encoding bacterial cell wall degradation enzymes (lysozymes) occurring in parallel across the tree of life.

    Article  PubMed Central  Google Scholar 

  32. Sloan, D. B. et al. Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Mol. Biol. Evol. 31, 857–871 (2014).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Wybouw, N. et al. A gene horizontally transferred from bacteria protects arthropods from host plant cyanide poisoning. eLife 3, e02365 (2014). This is an elegant analysis of HGT events of a cysteine synthase family found in several lineages of herbivorous arthropods. Functional expression analysis suggests that the enzymes can be used for both cysteine biosynthesis and cyanide detoxification, but enzyme kinetics suggest their main function is cyanide detoxification.

    Article  PubMed Central  PubMed  Google Scholar 

  34. Luan, J.-B. et al. Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant sap-feeding insects. Genome Biol. Evol. 7, 2635–2647 (2015).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Baltrus, D. A. Exploring the costs of horizontal gene transfer. Trends Ecol. Evol. 28, 489–495 (2013).

    Article  PubMed  Google Scholar 

  36. Koutsovoulos, G. et al. Palaeosymbiosis revealed by genomic fossils of Wolbachia in a strongyloidean nematode. PLoS Genet. 10, e1004397 (2014).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  37. Choi, J. Y., Bubnell, J. E. & Aquadro, C. F. Population genomics of infectious and integrated Wolbachia pipientis genomes in Drosophila ananassae. Genome Biol. Evol. 7, 2362–2382 (2015).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Derelle, E. et al. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc. Natl Acad. Sci. USA 103, 11647–11652 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Eyres, I. et al. Horizontal gene transfer in bdelloid rotifers is ancient, ongoing and more frequent in species from desiccating habitats. BMC Biol. 13, 90 (2015).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  40. Ku, C. et al. Endosymbiotic gene transfer from prokaryotic pangenomes: inherited chimerism in eukaryotes. Proc. Natl Acad. Sci. USA 112, 10139–10146 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Ku, C. et al. Endosymbiotic origin and differential loss of eukaryotic genes. Nature 524, 427–432 (2015).

    Article  CAS  PubMed  Google Scholar 

  42. Katz, L. A. Recent events dominate interdomain lateral gene transfers between prokaryotes and eukaryotes and, with the exception of endosymbiotic gene transfers, few ancient transfer events persist. Phil. Trans. R. Soc. B Biol. Sci. 370, 20140324 (2015).

    Article  CAS  Google Scholar 

  43. Brown, J. R. Ancient horizontal gene transfer. Nat. Rev. Genet. 4, 121–132 (2003).

    Article  CAS  PubMed  Google Scholar 

  44. Nowack, E. C. M. et al. Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of Paulinella chromatophora. Proc. Natl Acad. Sci. USA 113, 12214–12219 (2016). Paulinella chromatophora is an amoeba that contains a photosynthetic symbiont. Genomic and transcriptomic data enabled the authors to untangle how many bacterial genes in the genome of P. chromatophora came from phylogenetic sources other than the current symbiont and suggest that HGT from diverse bacteria compensates for gene loss in the symbiont.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Xu, F. et al. On the reversibility of parasitism: adaptation to a free-living lifestyle via gene acquisitions in the diplomonad Trepomonas sp. PC1. BMC Biol. 14, 62 (2016).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  46. Paganini, J. et al. Contribution of lateral gene transfers to the genome composition and parasitic ability of root-knot nematodes. PLoS ONE 7, e50875 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Schönknecht, G. et al. Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339, 1207–1210 (2013). This study describes the important role that HGT from bacteria has had in enabling the red alga Galdieria to adapt to hot, toxic and acidic environments.

    Article  PubMed  CAS  Google Scholar 

  48. Qiu, H. et al. Adaptation through horizontal gene transfer in the cryptoendolithic red alga Galdieria phlegrea. Curr. Biol. 23, R865–R866 (2013).

    Article  CAS  PubMed  Google Scholar 

  49. Savory, F., Leonard, G. & Richards, T. A. The role of horizontal gene transfer in the evolution of the oomycetes. PLoS Pathog. 11, e1004805 (2015). This study evaluates extensive HGT from bacteria and fungi that assisted oomycetes in becoming successful plant parasites.

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  50. Eme, L., Gentekaki, E., Curtis, B., Archibald, J. M. & Roger, A. J. Lateral gene transfer in the adaptation of the anaerobic parasite Blastocystis to the gut. Curr. Biol. 27, 807–820 (2017). This rigorous phylogeny-based analysis of HGT in Blastocystis spp. shows that 2.5% of their genes have been fairly recently acquired from bacteria, archaea and eukaryotes. In particular, the authors report genes involved in carbohydrate scavenging and metabolism, anaerobic amino acid and nitrogen metabolism, oxygen-stress resistance and pH homeostasis. These HGT events are hypothesized to assist Blastocystis spp. in adaptation to the gut environment they inhabit.

    Article  CAS  PubMed  Google Scholar 

  51. Husnik, F. & McCutcheon, J. P. Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. Proc. Natl Acad. Sci. USA 113, E5416–E5424 (2016). One common argument against the idea of HGT from diverse bacteria compensating for symbiont or organelle gene loss is that complex pathways are impossible to build in a gene-by-gene fashion. This study shows how complex and mosaic pathways can be built sequentially with HGT events from diverse bacteria and that pre-existing HGT events can remain stable in genomes in the face of extensive symbiont turnover.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Boschetti, C. et al. Biochemical diversification through foreign gene expression in bdelloid rotifers. PLoS Genet. 8, e1003035 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  53. Marcet-Houben, M. & Gabaldón, T. Acquisition of prokaryotic genes by fungal genomes. Trends Genet. 26, 5–8 (2010).

    Article  CAS  PubMed  Google Scholar 

  54. Ford Doolittle, W. You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 14, 307–311 (1998).

    Article  Google Scholar 

  55. Gluck-Thaler, E. & Slot, J. C. Dimensions of horizontal gene transfer in eukaryotic microbial pathogens. PLoS Pathog. 11, e1005156 (2015).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  56. Huang, J. Horizontal gene transfer in eukaryotes: the weak-link model. Bioessays 35, 868–875 (2013). This study presents the weak-link model, which posits that foreign genes enter eukaryotic genomes at unprotected stages of their development; the model thus expands previous models for multicellular sexual eukaryotes.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Dunning Hotopp, J. C. Horizontal gene transfer between bacteria and animals. Trends Genet. 27, 157–163 (2011).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  58. Brelsfoard, C. et al. Presence of extensive Wolbachia symbiont insertions discovered in the genome of its host Glossina morsitans morsitans. PLoS Negl. Trop. Dis. 8, e2728 (2014).

    Article  PubMed Central  PubMed  Google Scholar 

  59. Klasson, L. et al. Extensive duplication of the Wolbachia DNA in chromosome four of Drosophila ananassae. BMC Genomics 15, 1097 (2014).

    Article  PubMed Central  PubMed  Google Scholar 

  60. Lieber, M. R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79, 181–211 (2010).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Hao, W., Richardson, A. O., Zheng, Y. & Palmer, J. D. Gorgeous mosaic of mitochondrial genes created by horizontal transfer and gene conversion. Proc. Natl Acad. Sci. USA 107, 21576–21581 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Dunning Hotopp, J. C. et al. Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317, 1753–1756 (2007).

    Article  CAS  PubMed  Google Scholar 

  63. Funkhouser-Jones, L. J. et al. Wolbachia co-infection in a hybrid zone: discovery of horizontal gene transfers from two Wolbachia supergroups into an animal genome. PeerJ 3, e1479 (2015).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  64. Leclercq, S. et al. Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome. Proc. Natl Acad. Sci. USA 113, 15036–15041 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Kumar, N. et al. Efficient subtraction of insect rRNA prior to transcriptome analysis of Wolbachia-Drosophila lateral gene transfer. BMC Res. Notes 5, 230 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  66. Ricchetti, M., Tekaia, F. & Dujon, B. Continued colonization of the human genome by mitochondrial DNA. PLoS Biol. 2, E273 (2004).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  67. Ricchetti, M., Fairhead, C. & Dujon, B. Mitochondrial DNA repairs double-strand breaks in yeast chromosomes. Nature 402, 96–100 (1999).

    Article  CAS  PubMed  Google Scholar 

  68. Tsuji, J., Frith, M. C., Tomii, K. & Horton, P. Mammalian NUMT insertion is non-random. Nucleic Acids Res. 40, 9073–9088 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  69. McNulty, S. N. et al. Endosymbiont DNA in endobacteria-free filarial nematodes indicates ancient horizontal genetic transfer. PLoS ONE 5, e11029 (2010).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  70. Acuna, R. et al. Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc. Natl Acad. Sci. USA 109, 4197–4202 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Pauchet, Y. & Heckel, D. G. The genome of the mustard leaf beetle encodes two active xylanases originally acquired from bacteria through horizontal gene transfer. Proc. Biol. Sci. 280, 20131021 (2013).

    PubMed Central  PubMed  Google Scholar 

  72. Gladyshev, E. A., Meselson, M. & Arkhipova, I. R. Massive horizontal gene transfer in bdelloid rotifers. Science 320, 1210–1213 (2008). This is one of the first studies to describe massive HGT to an animal genome with details on gene localization, structure and function.

    Article  CAS  PubMed  Google Scholar 

  73. Sun, B. F. et al. Multiple ancient horizontal gene transfers and duplications in lepidopteran species. Insect Mol. Biol. 22, 72–87 (2013).

    Article  CAS  PubMed  Google Scholar 

  74. Le Hir, H., Nott, A. & Moore, M. J. How introns influence and enhance eukaryotic gene expression. Trends Biochem. Sci. 28, 215–220 (2003).

    Article  CAS  PubMed  Google Scholar 

  75. Craig, J. P., Bekal, S., Niblack, T., Domier, L. & Lambert, K. N. Evidence for horizontally transferred genes involved in the biosynthesis of vitamin B1, B5, and B7 in Heterodera glycines. J. Nematol. 41, 281–290 (2009).

    CAS  PubMed Central  PubMed  Google Scholar 

  76. Bowler, C. et al. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456, 239–244 (2008).

    Article  CAS  PubMed  Google Scholar 

  77. Danchin, E. G. J. et al. Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc. Natl Acad. Sci. USA 107, 17651–17656 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Andersson, J. O. et al. Lateral gene transfer in eukaryotes. Cell. Mol. Life Sci. 62, 1182–1197 (2005).

    Article  CAS  PubMed  Google Scholar 

  79. Archibald, J. M. Endosymbiosis and eukaryotic cell evolution. Curr. Biol. 25, R911–R921 (2015).

    Article  CAS  PubMed  Google Scholar 

  80. Gray, M. W. Mitochondrial evolution. Cold Spring Harb. Perspect. Biol. 4, a011403 (2012).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  81. Koonin, E. V. & Yutin, N. The dispersed archaeal eukaryome and the complex archaeal ancestor of eukaryotes. Cold Spring Harb. Perspect. Biol. 6, a016188 (2014).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  82. Ponce-Toledo, R. I. et al. An early-branching freshwater cyanobacterium at the origin of plastids. Curr. Biol. 27, 386–391 (2017).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  83. Wang, Z. & Wu, M. An integrated phylogenomic approach toward pinpointing the origin of mitochondria. Sci. Rep. 5, 7949 (2015).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  84. Gray, M. W. Mosaic nature of the mitochondrial proteome: implications for the origin and evolution of mitochondria. Proc. Natl Acad. Sci. USA 112, 10133–10138 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Huynen, M. A., Duarte, I. & Szklarczyk, R. Loss, replacement and gain of proteins at the origin of the mitochondria. Biochim. Biophys. Acta 1827, 224–231 (2013).

    Article  CAS  PubMed  Google Scholar 

  86. Gabaldón, T. & Huynen, M. A. From endosymbiont to host-controlled organelle: the hijacking of mitochondrial protein synthesis and metabolism. PLoS Comput. Biol. 3, e219 (2007).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  87. Esser, C. et al. A genome phylogeny for mitochondria among α-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol. Biol. Evol. 21, 1643–1660 (2004).

    Article  CAS  PubMed  Google Scholar 

  88. Thiergart, T., Landan, G., Schenk, M., Dagan, T. & Martin, W. F. An evolutionary network of genes present in the eukaryote common ancestor polls genomes on eukaryotic and mitochondrial origin. Genome Biol. Evol. 4, 466–485 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  89. Kurland, C. G. & Andersson, S. G. Origin and evolution of the mitochondrial proteome. Microbiol. Mol. Biol. Rev. 64, 786–820 (2000).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  90. Suzuki, K. & Miyagishima, S. Eukaryotic and eubacterial contributions to the establishment of plastid proteome estimated by large-scale phylogenetic analyses. Mol. Biol. Evol. 27, 581–590 (2010).

    Article  CAS  PubMed  Google Scholar 

  91. Zaremba-Niedzwiedzka, K. et al. Asgard arcahea illuminates the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017).

    Article  CAS  PubMed  Google Scholar 

  92. Pittis, A. A. & Gabaldón, T. Late acquisition of mitochondria by a host with chimaeric prokaryotic ancestry. Nature 531, 101–104 (2016).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  93. Koonin, E. V. Archaeal ancestors of eukaryotes: not so elusive any more. BMC Biol. 13, 84 (2015).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  94. Spang, A. et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  95. Delaye, L., Valadez-Cano, C. & Pérez-Zamorano, B. How really ancient is Paulinella chromatophora? PLoS Curr. http://dx.doi.org/10.1371/currents.tol.e68a099364bb1a1e129a17b4e06b0c6b (2016).

  96. Klein, C. C. et al. Biosynthesis of vitamins and cofactors in bacterium-harbouring trypanosomatids depends on the symbiotic association as revealed by genomic analyses. PLoS ONE 8, e79786 (2013).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  97. Alves, J. M. P. et al. Endosymbiosis in trypanosomatids: the genomic cooperation between bacterium and host in the synthesis of essential amino acids is heavily influenced by multiple horizontal gene transfers. BMC Evol. Biol. 13, 190 (2013).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  98. Larkum, A. W. D., Lockhart, P. J. & Howe, C. J. Shopping for plastids. Trends Plant Sci. 12, 189–195 (2007).

    Article  CAS  PubMed  Google Scholar 

  99. Gray, M. W. The pre-endosymbiont hypothesis: a new perspective on the origin and evolution of mitochondria. Cold Spring Harb. Perspect. Biol. 6, a016097 (2014).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  100. Qiu, H. et al. Assessing the bacterial contribution to the plastid proteome. Trends Plant Sci. 18, 680–687 (2013).

    Article  CAS  PubMed  Google Scholar 

  101. Karnkowska, A. et al. A eukaryote without a mitochondrial organelle. Curr. Biol. 26, 1274–1284 (2016).

    Article  CAS  PubMed  Google Scholar 

  102. Embley, T. M. & Martin, W. Eukaryotic evolution, changes and challenges. Nature 440, 623–630 (2006).

    Article  CAS  PubMed  Google Scholar 

  103. Daimon, T. et al. β-fructofuranosidase genes of the silkworm, Bombyx mori: insights into enzymatic adaptation of B. mori to toxic alkaloids in mulberry latex. J. Biol. Chem. 283, 15271–15279 (2008).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  104. Ambrose, K. V., Koppenhöfer, A. M. & Belanger, F. C. Horizontal gene transfer of a bacterial insect toxin gene into the Epichloë fungal symbionts of grasses. Sci. Rep. 4, 5562 (2014).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  105. Daborn, P. J. et al. A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc. Natl Acad. Sci. USA 99, 10742–10747 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Ricard, G. et al. Horizontal gene transfer from bacteria to rumen ciliates indicates adaptation to their anaerobic, carbohydrates-rich environment. BMC Genomics 7, 22 (2006).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  107. Richards, T. A., Leonard, G., Soanes, D. M. & Talbot, N. J. Gene transfer into the fungi. Fungal Biol. Rev. 25, 98–110 (2011).

    Article  Google Scholar 

  108. Danchin, E. G. J. & Rosso, M.-N. Lateral gene transfers have polished animal genomes: lessons from nematodes. Front. Cell. Infect. Microbiol. 2, 27 (2012).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  109. Schuster, L. N. & Sommer, R. J. Expressional and functional variation of horizontally acquired cellulases in the nematode Pristionchus pacificus. Gene 506, 274–282 (2012).

    Article  CAS  PubMed  Google Scholar 

  110. Sasakura, Y. et al. Transcriptional regulation of a horizontally transferred gene from bacterium to chordate. Proc. Biol. Sci. 283, 20161712 (2016).

    PubMed Central  PubMed  Google Scholar 

  111. Huang, J. et al. Phylogenomic evidence supports past endosymbiosis, intracellular and horizontal gene transfer in Cryptosporidium parvum. Genome Biol. 5, R88 (2004).

    Article  PubMed Central  PubMed  Google Scholar 

  112. Marchetti, A. et al. Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 457, 467–470 (2009).

    Article  CAS  PubMed  Google Scholar 

  113. Allen, A. E. et al. Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc. Natl Acad. Sci. USA 105, 10438–10443 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Eichinger, L. et al. The genome of the social amoeba Dictyostelium discoideum. Nature 435, 43–57 (2005).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  115. Andersson, J. O. Evolution of patchily distributed proteins shared between eukaryotes and prokaryotes: Dictyostelium as a case study. J. Mol. Microbiol. Biotechnol. 20, 83–95 (2011).

    Article  CAS  PubMed  Google Scholar 

  116. Worden, A. Z. et al. Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 375, 268–272 (2009).

    Article  CAS  Google Scholar 

  117. de Koning, A. P., Brinkman, F. S. L., Jones, S. J. M. & Keeling, P. J. Lateral gene transfer and metabolic adaptation in the human parasite Trichomonas vaginalis. Mol. Biol. Evol. 17, 1769–1773 (2000).

    Article  CAS  PubMed  Google Scholar 

  118. Sun, G. & Huang, J. Horizontally acquired DAP pathway as a unit of self-regulation. J. Evol. Biol. 24, 587–595 (2011).

    Article  CAS  PubMed  Google Scholar 

  119. Craig, J. P. et al. Analysis of a horizontally transferred pathway involved in vitamin B6 biosynthesis from the soybean cyst nematode Heterodera glycines. Mol. Biol. Evol. 25, 2085–2098 (2008).

    Article  CAS  PubMed  Google Scholar 

  120. Mock, T. et al. Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. Nature 541, 536–540 (2017).

    Article  CAS  PubMed  Google Scholar 

  121. Raymond, J. A. et al. Possible role of horizontal gene transfer in the colonization of sea ice by algae. PLoS ONE 7, e35968 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  122. Blanc, G. et al. The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol. 13, R39 (2012).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  123. Harding, T., Roger, A. J. & Simpson, A. G. B. Adaptations to high salt in a halophilic protist: differential expression and gene acquisitions through duplications and gene transfers. Front. Microbiol. 8, 944 (2017).

    Article  PubMed Central  PubMed  Google Scholar 

  124. Slamovits, C. H. & Keeling, P. J. Class II photolyase in a microsporidian intracellular parasite. J. Mol. Biol. 341, 713–721 (2004).

    Article  CAS  PubMed  Google Scholar 

  125. Fast, N. M., Law, J. S., Williams, B. A. P. & Keeling, P. J. Bacterial catalase in the microsporidian Nosema locustae: implications for microsporidian metabolism and genome evolution. Eukaryot. Cell 2, 1069–1075 (2003).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  126. Dunning Hotopp, J. C. et al. Biology wars: the eukaryotes strike back. Cell Host Microbe 16, 701–703 (2014).

    Article  CAS  PubMed  Google Scholar 

  127. Ioannidis, P. et al. Rapid transcriptome sequencing of an invasive pest, the brown marmorated stink bug Halyomorpha halys. BMC Genomics 15, 738 (2014).

    Article  PubMed Central  PubMed  Google Scholar 

  128. Yue, J., Hu, X., Sun, H., Yang, Y. & Huang, J. Widespread impact of horizontal gene transfer on plant colonization of land. Nat. Commun. 3, 1152 (2012).

    Article  PubMed  CAS  Google Scholar 

  129. Hirano, T. et al. Moss chloroplasts are surrounded by a peptidoglycan wall containing D-amino acids. Plant Cell 28, 1521–1532 (2016).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  130. Machida, M. et al. Genes for the peptidoglycan synthesis pathway are essential for chloroplast division in moss. Proc. Natl Acad. Sci. USA 103, 6753–6758 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Garcia, M. et al. An Arabidopsis homolog of the bacterial peptidoglycan synthesis enzyme MurE has an essential role in chloroplast development. Plant J. 53, 924–934 (2008).

    Article  CAS  PubMed  Google Scholar 

  132. Royet, J., Gupta, D. & Dziarski, R. Peptidoglycan recognition proteins: modulators of the microbiome and inflammation. Nat. Rev. Immunol. 11, 837–851 (2011).

    Article  CAS  PubMed  Google Scholar 

  133. Nyholm, S. V. & Graf, J. Knowing your friends: invertebrate innate immunity fosters beneficial bacterial symbioses. Nat. Rev. Microbiol. 10, 815–827 (2012).

    Article  CAS  PubMed  Google Scholar 

  134. Wang, J. W., Wu, Y. N., Yang, G. X. & Aksoy, S. Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proc. Natl Acad. Sci. USA 106, 12133–12138 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. DiSalvo, S. et al. Burkholderia bacteria infectiously induce the proto-farming symbiosis of Dictyostelium amoebae and food bacteria. Proc. Natl Acad. Sci. USA 112, E5029–E5037 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Salter, S. J. et al. Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. BMC Biol. 12, 87 (2014).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  137. Boschetti, C. et al. Foreign genes and novel hydrophilic protein genes participate in the desiccation response of the bdelloid rotifer Adineta ricciae. J. Exp. Biol. 214, 59–68 (2011).

    Article  CAS  PubMed  Google Scholar 

  138. Wheeler, D., Redding, A. J. & Werren, J. H. Characterization of an ancient lepidopteran lateral gene transfer. PLoS ONE 8, e59262 (2013).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  139. Philippe, H. et al. Pitfalls in supermatrix phylogenomics. Eur. J. Taxon. 283, 1–25 (2017).

    Google Scholar 

  140. Shimodaira, H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51, 492–508 (2002).

    Article  PubMed  Google Scholar 

  141. Richards, T. A. et al. Horizontal gene transfer facilitated the evolution of plant parasitic mechanisms in the oomycetes. Proc. Natl Acad. Sci. USA 108, 15258–15263 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Stairs, C. W., Roger, A. J. & Hampl, V. Eukaryotic pyruvate formate lyase and its activating enzyme were acquired laterally from a firmicute. Mol. Biol. Evol. 28, 2087–2099 (2011).

    Article  CAS  PubMed  Google Scholar 

  143. Stechmann, A. et al. The glycolytic pathway of Trimastix pyriformis is an evolutionary mosaic. BMC Evol. Biol. 6, 101 (2006).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  144. Boxma, B. et al. The [FeFe] hydrogenase of Nyctotherus ovalis has a chimeric origin. BMC Evol. Biol. 7, 230 (2007).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  145. Müller, M., Lee, J. A., Gordon, P., Gaasterland, T. & Sensen, C. W. Presence of prokaryotic and eukaryotic species in all subgroups of the PPi-dependent group II phosphofructokinase protein family. J. Bacteriol. 183, 6714–6716 (2001).

    Article  PubMed Central  PubMed  Google Scholar 

  146. Nixon, J. E. J. et al. 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 (2002).

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  147. Sateriale, A. & Striepen, B. Beg, borrow and steal: three aspects of horizontal gene transfer in the protozoan parasite, Cryptosporidium parvum. PLoS Pathog. 12, e1005429 (2016).

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  148. Gojkovic, Z. et al. Horizontal gene transfer promoted evolution of the ability to propagate under anaerobic conditions in yeasts. Mol. Genet. Genomics 271, 387–393 (2004).

    Article  CAS  PubMed  Google Scholar 

  149. Tsaousis, A. D. et al. A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453, 553–556 (2008).

    Article  CAS  PubMed  Google Scholar 

  150. Alexander, W. G., Wisecaver, J. H., Rokas, A. & Hittinger, C. T. Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides. Proc. Natl Acad. Sci. USA 113, 4116–4121 (2016). This comprehensive analysis of HGT events in Microsporidia and Cryptomycota fungi detects dozens of novel HGT candidates, including parallel acquisitions that enable these pathogenic fungi to scavenge nucleosides and nucleotides from their hosts.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

F.H. was supported by the Fulbright Commission and a fellowship from the European Molecular Biology Organization (EMBO; ALTF 1260–2016) while writing this Review. J.P.M. was supported by grants from the US National Science Foundation (IOS-1256680 and IOS-1553529), the US National Aeronautics and Space Administration (NASA) Astrobiology Institute (NNA15BB04A) and the Gordon and Betty Moore Foundation (GBMF5602).

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  1. Filip Husnik

    Present address: Present address: Department of Botany, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada.,

Authors and Affiliations

  1. Faculty of Science, University of South Bohemia and Institute of Parasitology, Biology Centre Academy of Sciences of the Czech Republic (ASCR), 370 05, Ceske Budejovice, Czech Republic

    Filip Husnik

  2. Division of Biological Sciences, University of Montana, Missoula, 59812, Montana, USA

    Filip Husnik & John P. McCutcheon

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F.H. and J.P.M. researched data for the article, made substantial contributions to discussions of the content, wrote the article and reviewed and/or edited the manuscript before submission.

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FURTHER INFORMATION

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Supplementary information

Supplementary information S1 (table)

HGT events from bacteria to eukaryotes. (XLSX 33 kb)

Glossary

Horizontal gene transfer

(HGT). Movement of genetic material between organisms (also called lateral gene transfer) via non-vertical (not parent-to-offspring) transmission.

Germ line

The specialized cellular lineage in multicellular sexual organisms that is used to pass on genetic material to the progeny.

Endosymbionts

Organisms living within the body or cells of another organism.

Long-branch attraction

A phylogenetic artefact that causes distantly related lineages (often on long branches) to be incorrectly inferred as closely related in phylogenetic trees.

Conjugation

Gene transfer from a donor to a recipient by direct cell-to-cell contact, such as plasmid transfer between two bacterial cells.

Transduction

Gene transfer carried out by a virus, such as a bacteriophage, transferring DNA from one bacterium to another.

Transformation

Direct acquisition of DNA from the environment through the cell membrane.

Gene transfer agents

Bacteriophage-like elements that package random DNA regions from a host cell and transfer them to a recipient cell.

Non-homologous end joining

(NHEJ). A pathway for the direct repair of double-strand DNA breaks without a homologous template.

Nuclear mitochondrial transfers

(numts). Transfers of mitochondrial DNA into the nuclear genome of a eukaryotic host; the encoded genes often become non-functional.

Nuclear plastid transfers

(nupts). Transfers of plastid DNA into the nuclear genome of a eukaryotic host; the encoded genes often become non-functional.

Transposable elements

DNA sequences (also known as jumping genes) that can move within a genome (and sometimes also between genomes) by a 'cut and paste' (DNA transposons) or a 'copy and paste' (retrotransposons) mechanism.

Organellogenesis

The process by which an endosymbiont becomes an organelle, in part by becoming (nearly) irreversibly integrated with its host cell at both a genetic and cell biological level.

Reproductive manipulators

Bacteria, such as Wolbachia spp., that are transmitted in the egg cytoplasm of arthropods and nematodes and shift the sex ratio of the host population.

Peptidoglycan

A structural matrix in bacterial cell walls formed by alternating N-acetylglucosamine (NAG) and N-acetylmuramic acid (NAM) residues, where peptide chains of up to five amino acids link NAM to other NAM-connected peptides.

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Husnik, F., McCutcheon, J. Functional horizontal gene transfer from bacteria to eukaryotes. Nat Rev Microbiol 16, 67–79 (2018). https://doi.org/10.1038/nrmicro.2017.137

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