Abstract
Horizontal gene transfer (HGT) is now widely accepted as an indispensable mechanism in the evolution of microbes, but its contribution in metazoans still raises controversies. This is partly due to the methodologies used for the comprehensive prediction of HGT candidates from genomic information and also because the specific pathways that allow the incorporation of foreign DNA in the germline cells and subsequently to their chromosomes remain elusive. Here, we review the methods for HGT detection and examples of HGT events in two metazoan groups, bdelloid rotifers and tardigrades. Both groups are parthenogenetic and are capable of surviving desiccation (anhydrobiosis), and the roles of these features in promoting HGT, and of HGT loci to these phenomena, are discussed.
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Acuña R, Padilla BE, Flórez-Ramos CP et al (2012) Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee. Proc Natl Acad Sci U S A 109:4197–4202. https://doi.org/10.1073/pnas.1121190109
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
Ambrose KV, Koppenhöfer AM, Belanger FC (2014) Horizontal gene transfer of a bacterial insect toxin gene into the Epichloë fungal symbionts of grasses. Sci Rep 4:5562. https://doi.org/10.1038/srep05562
Arakawa K (2016) No evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. Proc Natl Acad Sci U S A 113:E3057. https://doi.org/10.1073/pnas.1602711113
Arakawa K, Yoshida Y, Tomita M (2016) Genome sequencing of a single tardigrade Hypsibius dujardini individual. Sci Data 3:160063. https://doi.org/10.1038/sdata.2016.63
Archibald JM (2015) Endosymbiosis and eukaryotic cell evolution. Curr Biol 25:R911–R921. https://doi.org/10.1016/j.cub.2015.07.055
Barraclough TG, Fontaneto D, Ricci C, Herniou EA (2007) Evidence for inefficient selection against deleterious mutations in cytochrome oxidase I of asexual bdelloid rotifers. Mol Biol Evol 24:1952–1962. https://doi.org/10.1093/molbev/msm123
Bast J, Parker DJ, Dumas Z et al (2018) Consequences of asexuality in natural populations: insights from stick insects. Mol Biol Evol 35:1668–1677. https://doi.org/10.1093/molbev/msy058
Bemm F, Weiß CL, Schultz J, Förster F (2016) Genome of a tardigrade: horizontal gene transfer or bacterial contamination? Proc Natl Acad Sci U S A 113:E3054–E3056. https://doi.org/10.1073/pnas.1525116113
Bemm FM, Burleigh L, Foerster F et al (2017) Draft genome of the Eutardigrade Milnesium tardigradum sheds light on ecdysozoan evolution. BioRxiv. https://doi.org/10.1101/122309
Blanc G, Agarkova I, Grimwood J et al (2012) The genome of the polar eukaryotic microalga Coccomyxa subellipsoidea reveals traits of cold adaptation. Genome Biol 13:R39. https://doi.org/10.1186/gb-2012-13-5-r39
Blaxter M (2007) Symbiont genes in host genomes: fragments with a future? Cell Host Microbe 2:211–213. https://doi.org/10.1016/j.chom.2007.09.008
Boothby TC, Goldstein B (2016) Reply to Bemm et al. and Arakawa: identifying foreign genes in independent Hypsibius dujardini genome assemblies. Proc Natl Acad Sci U S A 113:E3058–E3061. https://doi.org/10.1073/pnas.1601149113
Boothby TC, Tenlen JR, Smith FW et al (2015) Evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. Proc Natl Acad Sci U S A 112:15976–15981. https://doi.org/10.1073/pnas.1510461112
Boschetti C, Pouchkina-Stantcheva N, Hoffmann P, Tunnacliffe A (2011) Foreign genes and novel hydrophilic protein genes participate in the desiccation response of the bdelloid rotifer Adineta ricciae. J Exp Biol 214:59–68. https://doi.org/10.1242/jeb.050328
Boschetti C, Carr A, Crisp A et al (2012) Biochemical diversification through foreign gene expression in bdelloid rotifers. PLoS Genet 8:e1003035. https://doi.org/10.1371/journal.pgen.1003035
Clasen FJ, Pierneef RE, Slippers B, Reva O (2018) EuGI: a novel resource for studying genomic islands to facilitate horizontal gene transfer detection in eukaryotes. BMC Genomics 19:323. https://doi.org/10.1186/s12864-018-4724-8
Coghlan A, Fiedler TJ, McKay SJ et al (2008) nGASP–the nematode genome annotation assessment project. BMC Bioinf 9:549. https://doi.org/10.1186/1471-2105-9-549
Crisp A, Boschetti C, Perry M et al (2015) Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes. Genome Biol 16:50. https://doi.org/10.1186/s13059-015-0607-3
Crosbie EJ, Einstein MH, Franceschi S, Kitchener HC (2013) Human papillomavirus and cervical cancer. Lancet 382:889–899. https://doi.org/10.1016/S0140-6736(13)60022-7
Crowe JH (2014) Anhydrobiosis: an unsolved problem. Plant Cell Environ 37:1491–1493. https://doi.org/10.1111/pce.12304
Daborn PJ, Waterfield N, Silva CP et al (2002) A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc Natl Acad Sci U S A 99:10742–10747. https://doi.org/10.1073/pnas.102068099
Daimon T, Taguchi T, Meng Y et al (2008) Beta-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. https://doi.org/10.1074/jbc.M709350200
Danchin EGJ (2016) Lateral gene transfer in eukaryotes: tip of the iceberg or of the ice cube? BMC Biol 14:101. https://doi.org/10.1186/s12915-016-0330-x
Debortoli N, Li X, Eyres I et al (2016) Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex. Curr Biol 26:723–732. https://doi.org/10.1016/j.cub.2016.01.031
Delmont TO, Eren AM (2016) Identifying contamination with advanced visualization and analysis practices: metagenomic approaches for eukaryotic genome assemblies. PeerJ 4:e1839. https://doi.org/10.7717/peerj.1839
Dunning Hotopp JC, Estes AM (2014) Biology wars: the eukaryotes strike back. Cell Host Microbe 16:701–703. https://doi.org/10.1016/j.chom.2014.11.014
Dunning Hotopp JC, 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
Eren AM, Esen ÖC, Quince C et al (2015) Anvi’o: an advanced analysis and visualization platform for ‘omics data’. PeerJ 3:e1319. https://doi.org/10.7717/peerj.1319
Erkut C, Penkov S, Khesbak H et al (2011) Trehalose renders the dauer larva of Caenorhabditis elegans resistant to extreme desiccation. Curr Biol 21:1331–1336. https://doi.org/10.1016/j.cub.2011.06.064
Eyres I, Boschetti C, Crisp A et al (2015) Horizontal gene transfer in bdelloid rotifers is ancient, ongoing and more frequent in species from desiccating habitats. BMC Biol 13:90. https://doi.org/10.1186/s12915-015-0202-9
Flot J-F, Hespeels B, Li X et al (2013) Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500:453–457. https://doi.org/10.1038/nature12326
Gabriel WN, McNuff R, Patel SK et al (2007) The tardigrade Hypsibius dujardini, a new model for studying the evolution of development. Dev Biol 312:545–559. https://doi.org/10.1016/j.ydbio.2007.09.055
Gladyshev EA, Meselson M, Arkhipova IR (2008) Massive horizontal gene transfer in bdelloid rotifers. Science 320:1210–1213. https://doi.org/10.1126/science.1156407
Guidetti R, Altiero T, Rebecchi L (2011) On dormancy strategies in tardigrades. J Insect Physiol 57:567–576. https://doi.org/10.1016/j.jinsphys.2011.03.003
Gusev O, Nakahara Y, Vanyagina V et al (2010) Anhydrobiosis-associated nuclear DNA damage and repair in the sleeping chironomid: linkage with radioresistance. PLoS One 5:e14008. https://doi.org/10.1371/journal.pone.0014008
Gusev O, Suetsugu Y, Cornette R et al (2014) Comparative genome sequencing reveals genomic signature of extreme desiccation tolerance in the anhydrobiotic midge. Nat Commun 5:4784. https://doi.org/10.1038/ncomms5784
Harding T, Roger AJ, Simpson AGB (2017) Adaptations to high salt in a Halophilic Protist: differential expression and gene acquisitions through duplications and gene transfers. Front Microbiol 8:944. https://doi.org/10.3389/fmicb.2017.00944
Hashimoto T, Horikawa DD, Saito Y et al (2016) Extremotolerant tardigrade genome and improved radiotolerance of human cultured cells by tardigrade-unique protein. Nat Commun 7:12808. https://doi.org/10.1038/ncomms12808
Hengherr S, Heyer AG, Köhler H-R, Schill RO (2008) Trehalose and anhydrobiosis in tardigrades--evidence for divergence in responses to dehydration. FEBS J 275:281–288. https://doi.org/10.1111/j.1742-4658.2007.06198.x
Hespeels B, Knapen M, Hanot-Mambres D et al (2014) Gateway to genetic exchange? DNA double-strand breaks in the bdelloid rotifer Adineta vaga submitted to desiccation. J Evol Biol 27:1334–1345. https://doi.org/10.1111/jeb.12326
Husnik F, McCutcheon JP (2016) Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. Proc Natl Acad Sci U S A 113:E5416–E5424. https://doi.org/10.1073/pnas.1603910113
Husnik F, McCutcheon JP (2018) Functional horizontal gene transfer from bacteria to eukaryotes. Nat Rev Microbiol 16:67–79. https://doi.org/10.1038/nrmicro.2017.137
Husnik F, Nikoh N, Koga R et al (2013) Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell 153:1567–1578. https://doi.org/10.1016/j.cell.2013.05.040
Jönsson KI, Persson O (2010) Trehalose in three species of desiccation tolerant tardigrades. Open Zool J 3:1–5
Keilin D (1959) The Leeuwenhoek lecture the problem of anabiosis or latent life: history and current concept. Proc R Soc Lond B Biol Sci 150:149–191
Koonin EV (2015) Archaeal ancestors of eukaryotes: not so elusive any more. BMC Biol 13:84. https://doi.org/10.1186/s12915-015-0194-5
Koutsovoulos G, Kumar S, Laetsch DR et al (2016) No evidence for extensive horizontal gene transfer in the genome of the tardigrade Hypsibius dujardini. Proc Natl Acad Sci U S A 113:5053–5058. https://doi.org/10.1073/pnas.1600338113
Ku C, Nelson-Sathi S, Roettger M et al (2015a) Endosymbiotic origin and differential loss of eukaryotic genes. Nature 524:427–432. https://doi.org/10.1038/nature14963
Ku C, Nelson-Sathi S, Roettger M et al (2015b) Endosymbiotic gene transfer from prokaryotic pangenomes: inherited chimerism in eukaryotes. Proc Natl Acad Sci U S A 112:10139–10146. https://doi.org/10.1073/pnas.1421385112
Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921. https://doi.org/10.1038/35057062
Lee C-Y, Conrad MN, Dresser ME (2012) Meiotic chromosome pairing is promoted by telomere-led chromosome movements independent of bouquet formation. PLoS Genet 8:e1002730. https://doi.org/10.1371/journal.pgen.1002730
Mock T, Otillar RP, Strauss J et al (2017) Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus. Nature 541:536–540. https://doi.org/10.1038/nature20803
Nester EW, Gordon MP, Amasino RM, Yanofsky MF (1984) Crown gall: a molecular and physiological analysis. Annu Rev Plant Physiol 35:387–413. https://doi.org/10.1146/annurev.pp.35.060184.002131
Nikoh N, McCutcheon JP, Kudo T et al (2010) Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLoS Genet 6:e1000827. https://doi.org/10.1371/journal.pgen.1000827
Nowack ECM, Price DC, Bhattacharya D et al (2016) Gene transfers from diverse bacteria compensate for reductive genome evolution in the chromatophore of Paulinella chromatophora. Proc Natl Acad Sci U S A 113:12214–12219. https://doi.org/10.1073/pnas.1608016113
Nowell RW, Almeida P, Wilson CG et al (2018) Comparative genomics of bdelloid rotifers: insights from desiccating and nondesiccating species. PLoS Biol 16:e2004830. https://doi.org/10.1371/journal.pbio.2004830
Pett M, Coleman N (2007) Integration of high-risk human papillomavirus: a key event in cervical carcinogenesis? J Pathol 212:356–367. https://doi.org/10.1002/path.2192
Pittis AA, Gabaldón T (2016) Late acquisition of mitochondria by a host with chimeric prokaryotic ancestry. Nature 531:101–104. https://doi.org/10.1038/nature16941
Polz MF, Alm EJ, Hanage WP (2013) Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet 29:170–175. https://doi.org/10.1016/j.tig.2012.12.006
Rancurel C, Legrand L, Danchin EGJ (2017) Alienness: rapid detection of candidate horizontal gene transfers across the tree of life. Genes 8(10):248. https://doi.org/10.3390/genes8100248
Raymond JA, Kim HJ (2012) Possible role of horizontal gene transfer in the colonization of sea ice by algae. PLoS One 7:e35968. https://doi.org/10.1371/journal.pone.0035968
Regier JC, Shultz JW, Kambic RE, Nelson DR (2005) Robust support for tardigrade clades and their ages from three protein-coding nuclear genes. Invertebr Biol 123:93–100. https://doi.org/10.1111/j.1744-7410.2004.tb00145.x
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 7:22. https://doi.org/10.1186/1471-2164-7-22
Ricci C (1998) Anhydrobiotic capabilities of bdelloid rotifers. Hydrobiologia 387:321–326
Ricci C, Covino C (2005) Anhydrobiosis of Adineta ricciae: costs and benefits. Hydrobiologia 546:307–314. https://doi.org/10.1007/s10750-005-4238-7
Richards TA, Leonard G, Soanes DM, Talbot NJ (2011) Gene transfer into the fungi. Fungal Biol Rev 25:98–110. https://doi.org/10.1016/j.fbr.2011.04.003
Salzberg SL (2017) Horizontal gene transfer is not a hallmark of the human genome. Genome Biol 18:85. https://doi.org/10.1186/s13059-017-1214-2
Salzberg SL, White O, Peterson J, Eisen JA (2001) Microbial genes in the human genome: lateral transfer or gene loss? Science 292:1903–1906. https://doi.org/10.1126/science.1061036
Savory F, Leonard G, Richards TA (2015) The role of horizontal gene transfer in the evolution of the oomycetes. PLoS Pathog 11:e1004805. https://doi.org/10.1371/journal.ppat.1004805
Schönknecht G, Chen W-H, Ternes CM et al (2013) Gene transfer from bacteria and archaea facilitated evolution of an extremophilic eukaryote. Science 339:1207–1210. https://doi.org/10.1126/science.1231707
Schuster LN, Sommer RJ (2012) Expressional and functional variation of horizontally acquired cellulases in the nematode Pristionchus pacificus. Gene 506:274–282. https://doi.org/10.1016/j.gene.2012.07.013
Siderakis M, Tarsounas M (2007) Telomere regulation and function during meiosis. Chromosom Res 15:667–679. https://doi.org/10.1007/s10577-007-1149-7
Spang A, Saw JH, Jørgensen SL et al (2015) Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521:173–179. https://doi.org/10.1038/nature14447
Stanhope MJ, Lupas A, Italia MJ et al (2001) Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates. Nature 411:940–944. https://doi.org/10.1038/35082058
Sung W-K, Zheng H, Li S et al (2012) Genome-wide survey of recurrent HBV integration in hepatocellular carcinoma. Nat Genet 44:765–769. https://doi.org/10.1038/ng.2295
Switala J, O’Neil JO, Loewen PC (1999) Catalase HPII from Escherichia coli exhibits enhanced resistance to denaturation. Biochemistry 38:3895–3901. https://doi.org/10.1021/bi982863z
Tanaka S, Tanaka J, Miwa Y et al (2015) Novel mitochondria-targeted heat-soluble proteins identified in the anhydrobiotic tardigrade improve osmotic tolerance of human cells. PLoS One 10:e0118272. https://doi.org/10.1371/journal.pone.0118272
Vos M, Hesselman MC, Te Beek TA et al (2015) Rates of lateral gene transfer in prokaryotes: high but why? Trends Microbiol 23:598–605. https://doi.org/10.1016/j.tim.2015.07.006
Welch DBM, Ricci C, Meselson M (2009) Bdelloid rotifers: progress in understanding the success of an evolutionary scandal. In: Schön I, Martens K, Dijk P (eds) Lost sex. Springer, Dordrecht, pp 259–279
Wilson CG, Nowell RW, Barraclough TG (2018) Cross-contamination explains “inter and intraspecific horizontal genetic transfers” between asexual bdelloid rotifers. Curr biol 28:2436–2444.e14. https://doi.org/10.1016/j.cub.2018.05.070
Wybouw N, Dermauw W, Tirry L et al (2014) A gene horizontally transferred from bacteria protects arthropods from host plant cyanide poisoning. Elife 3:e02365. https://doi.org/10.7554/eLife.02365
Wybouw N, Pauchet Y, Heckel DG, Van Leeuwen T (2016) Horizontal gene transfer contributes to the evolution of arthropod herbivory. Genome Biol Evol 8:1785–1801. https://doi.org/10.1093/gbe/evw119
Yamaguchi A, Tanaka S, Yamaguchi S et al (2012) Two novel heat-soluble protein families abundantly expressed in an anhydrobiotic tardigrade. PLoS One 7:e44209. https://doi.org/10.1371/journal.pone.0044209
Yoshida Y, Koutsovoulos G, Laetsch DR et al (2017) Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus. PLoS Biol 15:e2002266. https://doi.org/10.1371/journal.pbio.2002266
Yoshida Y, Konno S, Nishino R et al (2018) Ultralow input genome sequencing library preparation from a single tardigrade specimen. J Vis Exp 137:e57615. https://doi.org/10.3791/57615
Zaneveld JR, Nemergut DR, Knight R (2008) Are all horizontal gene transfers created equal? Prospects for mechanism-based studies of HGT patterns. Microbiology 154:1–15. https://doi.org/10.1099/mic.0.2007/011833-0
Zaremba-Niedzwiedzka K, Caceres EF, Saw JH et al (2017) Asgard archaea illuminate the origin of eukaryotic cellular complexity. Nature 541:353–358. https://doi.org/10.1038/nature21031
Acknowledgements
We thank Michael Plewka (www.plingfactory.de) for the image of R. macrura.
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Yoshida, Y., Nowell, R.W., Arakawa, K., Blaxter, M. (2019). Horizontal Gene Transfer in Metazoa: Examples and Methods. In: Villa, T., Viñas, M. (eds) Horizontal Gene Transfer. Springer, Cham. https://doi.org/10.1007/978-3-030-21862-1_7
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