Skip to main content

Evidence for Ancient Horizontal Gene Acquisitions in Bdelloid Rotifers of the Genus Adineta

  • Chapter
  • First Online:
Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life

Abstract

Until recently, obligate asexuality was often considered an evolutionary dead end. However, recent advances suggest that conventional sexual reproduction, defined as the alternation of meiosis and fertilization, is not the only sustainable eukaryotic lifestyle. Moreover, different modes of asexual reproduction are observed in nature, raising the question of the diverse mechanisms responsible for the long-term survival and adaptation of strict asexuals. One possible way to study the molecular-genetic consequences of the loss of meiotic recombination is to scrutinize the genomes of asexuals of ancient and more recent origins. The first genome draft of an ancient asexual species, the bdelloid rotifer Adineta vaga, was recently made available, revealing a peculiar genomic structure in which allelic regions were massively rearranged and sometimes found on the same chromosome. Such genome organization devoid of homologous chromosomes appears incompatible with meiotic pairing and segregation, and represents therefore a compelling genomic signature of asexuality. Besides, the genome of A. vaga contains around 8 % of genes of apparent nonmetazoan origin, a percentage much higher than observed in most eukaryotes. Interestingly, a similar percentage of genes of nonmetazoan origin was independently inferred from a large-scale transcriptome analysis of the bdelloid rotifer Adineta ricciae. In this chapter, we conducted a comparative study between these two closely related species using reciprocal best blast hits, followed by functional annotation using the GOANNA pipeline. Around 10 % of all the orthologs identified between the two species were putatively acquired by horizontal gene transfer and lots of them were associated to hydrolases (18 %) and oxidoreductases (16 %) functions. We hypothesize that these acquisitions may have helped bdelloids to adapt to multiple food sources and to develop enhanced resistance to desiccation. Furthermore, comparisons with sequences available for the monogonont rotifer Brachionus plicatilis suggest that some nonmetazoan genes were acquired by rotifers before the separation of bdelloids and monogononts.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abad P et al (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26(8):909–915

    Article  CAS  PubMed  Google Scholar 

  • Altenhoff AM, Dessimoz C (2009) Phylogenetic and functional assessment of orthologs inference projects and methods. PLoS Comput Biol 5(1):e1000262

    Article  PubMed Central  PubMed  Google Scholar 

  • Arkhipova IR, Meselson M (2005) Deleterious transposable elements and the extinction of asexuals. BioEssays 27(1):76–85

    Article  CAS  PubMed  Google Scholar 

  • Arkhipova IR, Yushenova IA, Rodriguez F (2013) Endonuclease−containing Penelope retrotransposons in the bdelloid rotifer Adineta vaga exhibit unusual structural features and play a role in expansion of host gene families. Mob DNA 4(1):19

    Google Scholar 

  • Birky CW Jr, (1996). Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144(1):427–437

    Google Scholar 

  • Boschetti C et al (2012) Biochemical diversification through foreign gene expression in bdelloid rotifers PLoS Genet 8(11):e1003035

    Google Scholar 

  • Castagnone-Sereno P, Danchin EGJ (2014) Parasitic success without sex—the nematode experience. J Evol Biol (in press)

    Google Scholar 

  • Chapman JA et al (2010) The dynamic genome of Hydra. Nature 464(7288):592–596

    Article  CAS  PubMed  Google Scholar 

  • Colbourne JK et al (2011) The ecoresponsive genome of Daphnia pulex. Science 331(6017):555–561

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Connallon T, Clark AG (2010) Gene duplication, gene conversion and the evolution of the Y chromosome. Genetics 186(1):277–286

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Crombach A, Hogeweg P (2007) Chromosome rearrangements and the evolution of genome structuring and adaptability. Mol Biol Evol 24(5):1130–1139

    Article  CAS  PubMed  Google Scholar 

  • Danchin EGJ et al (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Natl Acad Sci USA 107(41):17651–17656

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Danchin EGJ et al (2011) Genomic perspectives on the long-term absence of sexual reproduction in animals. In: Pontarotti P (ed) Evolutionary biology—concepts, biodiversity, macroevolution and genome evolution. Springer, Heidelberg, pp 223–242

    Chapter  Google Scholar 

  • de Jonge R et al (2013) Extensive chromosomal reshuffling drives evolution of virulence in an asexual pathogen. Genome Res 23(8):1271–1282

    Article  PubMed Central  PubMed  Google Scholar 

  • Denekamp N et al (2009) Discovering genes associated with dormancy in the monogonont rotifer Brachionus plicatilis. BMC Genom 10(1):108

    Article  Google Scholar 

  • Doolittle FW (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet 14(8):307–311

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1974) The evolutionary advantage of recombination. Genetics 78(2):737–756

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fitch WM (1970) Distinguishing homologous from analogous proteins. Syst Biol 19(2):99–113

    CAS  Google Scholar 

  • Flot, JF et al (2013). Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500(7463):453–457

    Google Scholar 

  • Fontaneto D et al (2010) Cryptic diversity in the genus Adineta Hudson & Gosse, 1886 (Rotifera: Bdelloidea: Adinetidae): a DNA taxonomy approach. Hydrobiologia 662(1):27–33

    Article  Google Scholar 

  • Fontaneto D et al (2009) Extreme levels of hidden diversity in microscopic animals (Rotifera) revealed by DNA taxonomy. Mol Phylogenet Evol 53(1):182–189

    Article  CAS  PubMed  Google Scholar 

  • Gladyshev EA, Arkhipova IR (2010) Genome structure of bdelloid rotifers: shaped by asexuality or desiccation? J Hered 101(Supplement 1):S85–S93

    Article  Google Scholar 

  • Gladyshev EA, Meselson M, Arkhipova IR (2008) Massive horizontal gene transfer in bdelloid rotifers. Science 320(5880):1210–1213

    Google Scholar 

  • Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19(12):2226–2238

    Article  CAS  PubMed  Google Scholar 

  • Gross SM, Williamson VM (2011) Tm1: a Mutator/Foldback transposable element family in root-knot nematodes. PLoS ONE 6(9):e24534

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Haegeman A, Jones JT, Danchin EGJ (2011) Horizontal gene transfer in nematodes: a catalyst for plant parasitism? Molecular Plant-Microbe Interactions 24(8):879–887

    Article  CAS  PubMed  Google Scholar 

  • Hehemann J-H et al (2012) Bacteria of the human gut microbiome catabolize red seaweed glycans with carbohydrate-active enzyme updates from extrinsic microbes. Proc Natl Acad Sci USA 109(48):19786–19791

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Henry L, Schwander T, Crespi BJ (2012) Deleterious mutation accumulation in asexual Timema stick insects. Mol Biol Evol 29(1):401–408

    Article  CAS  PubMed  Google Scholar 

  • Hespeels B et al (2014) Gateway to genetic exchange? DNA double-strand breaks in the bdelloid rotifer Adineta vaga submitted to desiccation. J Evol Biol (in press)

    Google Scholar 

  • Hotopp JCD et al (2007) Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science 317(5845):1753–1756

    Article  Google Scholar 

  • Hsu WS (1956a) Oogenesis in Habrotrocha tridens (Milne). Biol Bull 111(3):364

    Article  Google Scholar 

  • Hsu WS (1956b) Oogenesis in the Bdelloidea rotifer Philodina roseola Ehrenberg. La Cellule 57:283–296

    Google Scholar 

  • Hulsen T et al (2006) Benchmarking ortholog identification methods using functional genomics data. Genome Biol 7(4):R31

    Article  PubMed Central  PubMed  Google Scholar 

  • Hur JH et al (2009) Degenerate tetraploidy was established before bdelloid rotifer families diverged. Mol Biol Evol 26(2):375–383

    Article  CAS  PubMed  Google Scholar 

  • International Aphid Genomics Consortium (2010) Genome sequence of the pea aphid Acyrthosiphon pisum. PLoS Biol 8(2):e1000313

    Article  Google Scholar 

  • Jain R, Rivera MC, Lake JA (1999) Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci USA 96(7):3801–3806

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Judson O, Normark B (1996) Ancient asexual scandals. Trends Ecol Evol 11(2):41–46

    Google Scholar 

  • Khakhlova O, Bock R (2006) Elimination of deleterious mutations in plastid genomes by gene conversion. Plant J 46(1):85–94

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi T et al (2011) Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathog 7(9):e1002219

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309–338

    Article  CAS  PubMed  Google Scholar 

  • Kraaijeveld K et al (2012) Transposon proliferation in an asexual parasitoid. Mol Ecol 21(16):3898–3906

    Article  CAS  PubMed  Google Scholar 

  • Leffler EM et al (2012) Revisiting an old riddle: what determines genetic diversity levels within species? PLoS Biol 10(9):e1001388

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lesbarrères D (2011) Sex or no sex, reproduction is not the question. BioEssays 33(11):818

    Article  Google Scholar 

  • Lipinski KJ et al (2014) High spontaneous rate of gene duplication in Caenorhabditis elegans. Curr Biol 21(4):306–310

    Article  Google Scholar 

  • Lodé T (2011) Sex is not a solution for reproduction: the libertine bubble theory. BioEssays 33(6):419–422

    Article  Google Scholar 

  • Lunt DH (2008) Genetic tests of ancient asexuality in root knot nematodes reveal recent hybrid origins. BMC Evol Biol 8:194

    Article  PubMed Central  PubMed  Google Scholar 

  • Lynch M et al (2008) Localization of the genetic determinants of meiosis suppression in Daphnia pulex. Genetics 180(1):317–327

    Article  PubMed Central  PubMed  Google Scholar 

  • Maynard Smith J (1986) Evolution: contemplating life without sex. Nature 324(6095):300–301

    Article  Google Scholar 

  • Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge

    Google Scholar 

  • McCarthy FM et al (2006) AgBase: a functional genomics resource for agriculture. BMC Genom 7:229

    Article  Google Scholar 

  • Moran NA, Jarvik T (2010). Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science 328(5978):624–627

    Google Scholar 

  • Moreno-Hagelsieb G, Latimer K (2008) Choosing BLAST options for better detection of orthologs as reciprocal best hits. Bioinformatics 24(3):319–324

    Article  CAS  Google Scholar 

  • Muller HJ (1932) Some genetic aspects of sex. Am Nat 66(703):118–138

    Google Scholar 

  • Ni T, Yue J, Sun G, Zou Y, Wen J, Huang J. (2012). Ancient gene transfer from algae to animals: Mechanisms and evolutionary significance. BMC Evol. Biol 12(1):83

    Google Scholar 

  • Nikoh N et al (2010) Bacterial genes in the aphid genome: absence of functional gene transfer from Buchnera to its host. PLoS Genet 6(2):e1000827

    Article  PubMed Central  PubMed  Google Scholar 

  • Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405(6784):299–304

    Article  CAS  PubMed  Google Scholar 

  • Overballe-Petersen S et al (2013) Bacterial natural transformation by highly fragmented and damaged DNA. Proc Natl Acad Sci USA 110(49):19860–19865

    Google Scholar 

  • Paganini J et al (2012) Contribution of lateral gene transfers to the genome composition and parasitic ability of root-knot nematodes. PLoS ONE 7(11):e50875

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rödelsperger C, Sommer RJ (2011) Computational archaeology of the Pristionchus pacificus genome reveals evidence of horizontal gene transfers from insects. BMC Evol Biol 11(1):239

    Article  PubMed Central  PubMed  Google Scholar 

  • Schwander T, Crespi BJ (2009) Multiple direct transitions from sexual reproduction to apomictic parthenogenesis in Timema stick insects. Evolution 63(1):84–103

    Article  Google Scholar 

  • Schwander T, Henry L, Crespi BJ (2011) Molecular evidence for ancient asexuality in Timema stick insects. Current Biol 21(13):1129–1134

    Article  CAS  Google Scholar 

  • Segers H et al (2007) Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 1564:1–104

    Google Scholar 

  • Segers H, Shiel RJ (2005) Tale of a sleeping beauty: a new and easily cultured model organism for experimental studies on bdelloid rotifers. Hydrobiologia 546(1):141–145

    Article  Google Scholar 

  • Seidl MF, Thomma BPHJ (2014) Sex or no sex: evolutionary adaptation occurs regardless. BioEssays 36(4):335–345

    Article  PubMed  Google Scholar 

  • Stephens PJ et al (2011) Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144(1):27–40

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Suga K et al (2007) Analysis of expressed sequence tags of the cyclically parthenogenetic rotifer Brachionus plicatilis. PLoS ONE 2(8):e671

    Article  PubMed Central  PubMed  Google Scholar 

  • Takeuchi N, Kaneko K, Koonin EV (2014) Horizontal gene transfer can rescue prokaryotes from Muller’s ratchet: benefit of DNA from dead cells and population subdivision. G3 4(2):325–339

    Google Scholar 

  • Tekaia F, Yeramian E (2012) SuperPartitions: detection and classification of orthologs. Gene 492(1):199–211

    Article  CAS  PubMed  Google Scholar 

  • Triantaphyllou AC (1981) Oogenesis and the chromosomes of the parthenogenic root-knot nematode Meloidogyne incognita. J Nematol 13(2):95–104

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tucker AE et al (2013) Population-genomic insights into the evolutionary origin and fate of obligately asexual Daphnia pulex. Proc Natl Acad Sci USA 110(39):15740–15745

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Whitaker JW, McConkey GA, Westhead DR (2009) The transferome of metabolic genes explored: analysis of the horizontal transfer of enzyme encoding genes in unicellular eukaryotes. Genome Biol 10(4):R36

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang J et al (2011) Transposable elements as catalysts for chromosome rearrangements. In Birchler JA (ed) Plant chromosome engineering. Methods in molecular biology. Humana Press, pp 315–326

    Google Scholar 

  • Zhu B, Lou MM, Xie GL, Zhang GQ, Zhou XP, Li B, Jin GL (2011). Horizontal gene transfer in silkworm, Bombyx mori. BMC Genom 12(1):248

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Karine Van Doninck .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Hespeels, B., Flot, JF., Derzelle, A., Van Doninck, K. (2014). Evidence for Ancient Horizontal Gene Acquisitions in Bdelloid Rotifers of the Genus Adineta . In: Pontarotti, P. (eds) Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life. Springer, Cham. https://doi.org/10.1007/978-3-319-07623-2_10

Download citation

Publish with us

Policies and ethics