, Volume 142, Issue 2, pp 149–160 | Cite as

A novel cluster of mariner-like elements belonging to mellifera subfamily from spiders and insects: implications of recent horizontal transfer on the South-West Islands of Japan

  • Kaori Yamada
  • Yuichi Kawanishi
  • Akinori Yamada
  • Gaku Tokuda
  • Raj Deep Gurung
  • Takeshi Sasaki
  • Yumiko Nakajima
  • Hideaki MaekawaEmail author


Mariner-like elements (MLEs) have been isolated from various eukaryotic genomes and they are divided into 15 subfamilies, including main five subfamilies: mauritiana, cecropia, mellifera/capitata, irritans, and elegans/briggsae. In the present study, MLEs belonging to mellifera subfamily were isolated from various spiders and insects (Hymenoptera and Lepidoptera) inhabiting the South-West Islands of Japan and neighboring regions. MLEs isolated from 15 different species formed a distinct novel cluster in mellifera subfamily. MLEs obtained from three different species [i.e., the bee Amegilla senahai subflavescens (Amsmar1), the wasp Campsomeris sp. (Casmar1), and the swallowtail butterfly Pachliopta aristolochiae (Paamar1)] contained an intact open reading frame that encoded a putative transposase. These transposases exhibited high similarity of 97.9 % among themselves. In case of Casmar1, the presence of an intact ORF was found in high frequencies (i.e., 11 out of 12 clones). In addition, these transposases also showed the presence of a terminal inverted repeat-binding motif, DD(34)D and two highly conserved amino acid motifs, (W/L)(I/L)PHQL and YSP(D/N)L(A/S)P. These two motifs differed from previously known motifs, WVPHEL and YSPDLAP. MLEs isolated from these three different species may have been inserted into their genomes by horizontal transfer. Furthermore, the presence of an intact ORF suggests that they are still active in habitats along these isolated islands.


Mariner-like elements Mellifera subfamily Transposable elements Horizontal transfer 



This work was supported by the project “Analysis for invasion mechanism into genome of movable element and its novel application for gene introduction.” funded by Ministry of Education, Culture, Sports and Science in Japan and sponsored by foundation of the University of the Ryukyus. We thank the members of Center of Molecular Biosciences, Tropical Biosphere Research Center, University of the Ryukyus specially Mr. S. Okuma, Ms. H. Iwasaki, Ms. H. Nakahara, and Ms. S. Gurung for their great help.

Supplementary material

10709_2014_9762_MOESM1_ESM.eps (1.8 mb)
Supplementary material Supplementary figure 1 Comparative analysis of MLE clones classified into cluster B. The phylogenetic tree was constructed by the Neighbor-Joining (NJ) method, rooted with MLEs in mellifera subfamily: Ccmar1 (Ceratitis capitata; U40493), Tcmar1 (Trirhithrum coffeae; U88164) and Crmar1 (Ceratitis rosa; U88162). For comparison, following MLEs of cluster A were included from the GenBank/EMBL/DDBJ database: Epicauta funebris, AY154756 (Efmar1.1); Apis mellifera, AY155490 (Ammar1); Chymomyza amoena, AY155491 (Camar1); Forfícula auricularia, AY155492 (Famar1); and Ceratitis capitata, AY155493 (Ccmar2). Bootstrap values (1,000 replications) at the nodes supporting these groupings are indicated for ML and MP in addition to NJ analyses (NJ/ML/MP). A scale bar represents the number of substitutions per nucleotide position. MLE clones that were indicated by black triangles in Fig. 2 are each described by their sample names and clone numbers in this figure. (EPS 1826 kb)
10709_2014_9762_MOESM2_ESM.docx (23 kb)
Supplementary material 2 (DOCX 23 kb)


  1. Acinas SG, Sarma-Rupavtarm R, Klepac-Ceraj V, Polz MF (2005) PCR-induced sequence artifacts and bias: insights from comparison of two 16S rRNA clone libraries constructed from the same sample. Appl Environ Microbiol 71:8966–8969. doi: 10.1128/AEM.71.12.8966-8969.2005 PubMedCentralPubMedCrossRefGoogle Scholar
  2. Auge-Gouillou C, Bigot Y, Pollet N, Hamelin MH, Meunier-Rotival M, Periquet G (1995) Human and other mammalian genomes contain transposons of the mariner family. FEBS Lett 368:541–546. doi: 10.1016/0014-5793(95)00735-R PubMedCrossRefGoogle Scholar
  3. Auge-Gouillou C, Brillet B, Germon S, Hamelin MH, Bigot Y (2005) Mariner Mos1 transposase dimerizes prior to ITR binding. J Mol Biol 351:117–130. doi: 10.1016/j.jmb.2005.05.019 PubMedCrossRefGoogle Scholar
  4. Blanchetot A, Gooding RH (1995) Identification of a mariner element from the tsetse fly, Glossina palpalis palpalis. Insect Mol Biol 4:89–96. doi: 10.1111/j.1365-2583.1995.tb00012.x PubMedCrossRefGoogle Scholar
  5. Bracho MA, Moya A, Barrio E (1998) Contribution of Taq polymerase-induced errors to the estimation of RNA virus diversity. J Gen Virol 79:2921–2928PubMedGoogle Scholar
  6. Bucher P (1990) Weight matrix descriptions of four eukaryotic RNA polymerase II promoter elements derived from 502 unrelated promoter sequences. J Mol Biol 212:563–578. doi: 10.1016/0022-2836(90)90223-9 PubMedCrossRefGoogle Scholar
  7. Bui QT, Casse N, Leignel V, Nicolas V, Chénais B (2008) Widespread occurrence of mariner transposons in coastal crabs. Mol Phylogenet Evol 47:1181–1189. doi: 10.1016/j.ympev.2008.03.029 PubMedCrossRefGoogle Scholar
  8. Carr M (2008) Multiple subfamilies of mariner transposable elements are present in stalk-eyed flies (Diptera: Diopsidae). Genetica 132:113–122. doi: 10.1007/s10709-007-9157-2 PubMedCrossRefGoogle Scholar
  9. Casse N, Bui QT, Nicolas V, Renault S, Bigot Y, Laulier M (2006) Species sympatry and horizontal transfers of Mariner transposons in marine crustacean genomes. Mol Phylogenet Evol 40:609–619. doi: 10.1016/j.ympev.2006.02.005 PubMedCrossRefGoogle Scholar
  10. Cummings SM, McMullan M, Joyce DA, van Oosterhout C (2010) Solutions for PCR, cloning and sequencing errors in population genetic analysis. Conserv Genet 11:1095–1097. doi: 10.1007/s10592-009-9864-6 CrossRefGoogle Scholar
  11. Doak TG, Doerder FP, Jahn CL, Herrick G (1994) A proposed superfamily of transposase genes: transposon-like elements in ciliated protozoa and a common “D35E” motif. Proc Natl Acad Sci USA 91:942–946. doi: 10.1073/pnas.91.3.942 PubMedCentralPubMedCrossRefGoogle Scholar
  12. Folmer O, Black M, Hoeh R, Lutz RA, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  13. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709Google Scholar
  14. Gomulski LM, Torti C, Malacrida AR, Gasperi G (1997) Ccmar1, a full-length mariner element from the Mediterranean fruit fly, Ceratitis capitata. Insect Mol Biol 6:241–253. doi: 10.1046/j.1365-2583.1997.00179.x PubMedCrossRefGoogle Scholar
  15. Halaimia-Toumi N, Casse N, Demattei MV, Renault S, Pradier E, Bigot Y, Laulier M (2004) The GC-rich transposon Bytmar1 from the deep-sea hydrothermal crab, Bythograea thermydron, may encode three transposase isoforms from a single ORF. J Mol Evol 59:747–760. doi: 10.1007/s00239-004-2665-0 PubMedCrossRefGoogle Scholar
  16. Hartl DL (1989) Transposable element mariner in Drosophila species. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington, pp 531–536Google Scholar
  17. Hartl DL, Lohe AR, Lozovskaya ER (1997) Modern thoughts on an ancyent marinere: function, evolution, regulation. Annu Rev Genet 31:337–358. doi: 10.1146/annurev.genet.31.1.337 PubMedCrossRefGoogle Scholar
  18. Jacobson JW, Medhora MM, Hartl DL (1986) Molecular structure of somatically unstable transposable element in Drosophila. Proc Natl Acad Sci USA 83:8684–8688. doi: 10.1073/pnas.83.22.8684 PubMedCentralPubMedCrossRefGoogle Scholar
  19. Jarvik T, Lark KG (1998) Characterization of Soymar1, a mariner element in soybean. Genetics 149:1569–1574PubMedCentralPubMedGoogle Scholar
  20. Jursch T, Miskey C, Izsvák Z, Ivics Z (2013) Regulation of DNA transposition by CpG methylation and chromatin structure in human cells. Mob DNA 4:15. doi: 10.1186/1759-8753-4-15 PubMedCentralPubMedCrossRefGoogle Scholar
  21. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. doi: 10.1093/molbev/mst010 PubMedCentralPubMedCrossRefGoogle Scholar
  22. Kondrakhin YuV, Shamin VV, Kolchanov NA (1994) Construction of a generalized consensus matrix for recognition of vertebrate pre-mRNA 3′-terminal processing sites. Comput Appl Biosci 10:597–603. doi: 10.1093/bioinformatics/10.6.597 PubMedGoogle Scholar
  23. Laha T, Loukas A, Wattanasatitarpa S, Somprakhon J, Kewgrai N, Sithithaworn P, Kaewkes S, Mitreva M, Brindley PJ (2007) The bandit, a new transposon from hookworm-possible horizontal genetic transfer between host and parasite. PLoS Negl Trop Dis 1:1–11. doi: 10.1371/journal.pntd.0000035 CrossRefGoogle Scholar
  24. Lampe DJ, Witherspoon DJ, Soto-Adames FN, Robertson HM (2003) Recent horizontal transfer of mellifera subfamily mariner transposons into insect lineages representing four different orders shows that selection acts only during horizontal transfer. Mol Biol Evol 20:554–562. doi: 10.1093/molbev/msg069 PubMedCrossRefGoogle Scholar
  25. Langin T, Capy P, Daboussi MJ (1995) The transposable element impala, a fungal member of the Tc1-mariner superfamily. Mol Gen Genet 246:19–28. doi: 10.1007/BF00290129 PubMedCrossRefGoogle Scholar
  26. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi: 10.1093/bioinformatics/btm404 PubMedCrossRefGoogle Scholar
  27. Lidholm DA, Gudmundsson GH, Boman HG (1991) A highly repetitive, mariner-like element in the genome of Hyalophora cecropia. J Biol Chem 266:11518–11521PubMedGoogle Scholar
  28. Liu D, Chalmers R (2013) Hyperactive mariner transposons are created by mutations that disrupt allosterism and increase the rate of transposon end synapsis. Nucleic Acids Res 13:1–9. doi: 10.1093/nar/gkt1218 Google Scholar
  29. Lohe AR, Moriyama EN, Lidholm DA, Hartl DL (1995) Horizontal transmission, vertical inactivation, and stochastic loss of mariner-like transposable elements. Mol Biol Evol 12:62–72. doi: 10.1093/oxfordjournals.molbev.a040191 PubMedCrossRefGoogle Scholar
  30. López-García P, Philippe H, Gail F, Moreira D (2003) Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge. Proc Natl Acad Sci USA 100:697–702. doi: 10.1073/pnas.0235779100 PubMedCentralPubMedCrossRefGoogle Scholar
  31. Lorite P, Maside X, Sanllorente O, Torres MI, Periquet G, Palomeque T (2012) The ant genomes have been invaded by several types of mariner transposable elements. Naturwissenschaften 99:1007–1020. doi: 10.1007/s00114-012-0982-5 PubMedCrossRefGoogle Scholar
  32. Marcon HS, Domingues DS, Coscrato VE, Selivon D, Perondini AL, Marion CL (2011) New mariner elements in Anastrepha species (Diptera: Tephritidae). Neotrop Entomol 40:568–574PubMedGoogle Scholar
  33. Medhora M, Maruyama K, Hartl DL (1991) Molecular and functional analysis of the mariner mutator element Mos1 in Drosophila. Genetics 128:311–318PubMedCentralPubMedGoogle Scholar
  34. Mittapalli O, Rivera-Vega L, Bhandary B, Bautista MA, Mamidala P, Michel AP, Shukle RH, Mian MA (2011) Cloning and characterization of mariner-like elements in the soybean aphid, Aphis glycines Matsumura. Bull Entomol Res 101:697–704. doi: 10.1017/s0007485311000253 PubMedCrossRefGoogle Scholar
  35. Nakajima Y, Hashido K, Shiino T, Hayashi T, Tsuchida K, Nagamine M, Maekawa H (1998) Isolation of mariner-like sequence containing a complete open reading frame for transposase from Attacus atlas and its phylogenetic relationships within the Ditrysia of Lepidoptera. J Seric Sci Jpn 67:271–278Google Scholar
  36. Okuma S, Kawanishi Y, Sasaki K, Hidaka M, Maekawa H, Nakajima Y (2010) Analysis for horizontal transmittance mechanism of mariner-like elements of insects and spiders inhabiting sub-tropical area. Entomotech 34:47–52 (in Japanese)Google Scholar
  37. Petit A, Rouleux-Bonnin F, Lambelé M, Pollet N, Bigot Y (2007) Properties of the various Botmar1 transcripts in imagoes of the bumble bee, Bombus terrestris (Hymenoptera: Apidae). Gene 390:52–66. doi: 10.1016/j.gene.2006.07.025 PubMedCrossRefGoogle Scholar
  38. Plasterk RHA, van Luenen HGAM (2002) The Tc1/mariner family of transposable elements. In: Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) Mobile DNA II. American Society for Microbiology, Washington, pp 519–532Google Scholar
  39. Plasterk RHA, Izsvák Z, Ivics Z (1999) Resident aliens: the Tc1/mariner superfamily of transposable elements. Trends Genet 15:326–332. doi: 10.1016/S0168-9525(99)01777-1 PubMedCrossRefGoogle Scholar
  40. Rezende-Teixeira P, do Amaral JB, Siviero F, Machado-Santelli GM (2012) Molecular characterization of a mariner-like element in the Atta sexdens rubropilosa genome. Genet Mol Res 11:1475–1485. doi: 10.4238/2012.May.21.4 PubMedCrossRefGoogle Scholar
  41. Robertson HM (1993) The mariner transposable element is widespread in insects. Nature 362:241–245. doi: 10.1038/362241a0 PubMedCrossRefGoogle Scholar
  42. Robertson HM, Asplund ML (1996) Bmmar1: a basal lineage of the mariner family of transposable elements in the Bombyx mori. Insect Biochem Mol Biol 26:945–954. doi: 10.1016/s0965-1748(96)00061-6 PubMedCrossRefGoogle Scholar
  43. Robertson HM, Lampe DJ (1995) Recent horizontal transfer of a mariner transposable element among and between Diptera and Neuroptera. Mol Biol Evol 12:850–862PubMedGoogle Scholar
  44. Robertson HM, MacLeod EG (1993) Five major subfamilies of mariner transposable elements in insects, including the Mediterranean fruit fly, and related arthropods. Insect Mol Biol 2:125–139. doi: 10.1111/j.1365-2583.1993.tb00132.x PubMedCrossRefGoogle Scholar
  45. Robertson HM, Soto-Adames FN, Walden KKO, Avancini RMP, Lampe DJ (1998) The mariner transposons of animals: horizontally jumping genes. In: Syvanen M, Kado C (eds) Horizontal gene transfer. Chapman and Hall, London, pp 268–284Google Scholar
  46. Rouault JD, Casse N, Chénais B, Hua-Van A, Filée J, Capy P (2009) Automatic classification within families of transposable elements: application to the mariner family. Gene 448:227–232. doi: 10.1016/j.gene.2009.08.009 PubMedCrossRefGoogle Scholar
  47. Rouleux-Bonnin F, Petit A, Demattei M-V, Bigot Y (2005) Evolution of full-length and deleted forms of the mariner-like element, Botmar1, in the genome of the bumble bee, Bombus terrestris (Hymenoptera: Apidae). J Mol Biol 59:736–747. doi: 10.1007/s00239-004-0195-4
  48. Shao H, Tu Z (2001) Expanding the diversity of the IS630-Tc1-mariner superfamily: discovery of a unique DD37E transposon and reclassification of the DD37D and DD39D transposons. Genetics 159:1103–1115PubMedCentralPubMedGoogle Scholar
  49. Silva JC, Bastida F, Bidwell SL, Johnson PJ, Carlton JM (2005) A potentially functional mariner transposable element in the protist Trichomonas vaginalis. Mol Biol Evol 22:126–134. doi: 10.1093/molbev/msh260 PubMedCentralPubMedCrossRefGoogle Scholar
  50. Speksnijder AG, Kowalchuk GA, De Jong S, Kline E, Stephen JR, Laanbroek HJ (2001) Microvariation artifacts introduced by PCR and cloning of closely related 16S rRNA gene sequences. Appl Environ Microbiol 67:469–472. doi: 10.1128/AEM.67.1.469-472.2001 PubMedCentralPubMedCrossRefGoogle Scholar
  51. Sumitani M, Lee JM, Hatakeyama M, Oishi K (2002) Cloning and characterization of Acmar1, a mariner-like element in the Asiatic honey bee, Apis cerana japonica (Hymenoptera, Apocrita). Arch Insect Biochem Physiol 50:183–190. doi: 10.1002/arch.10043 PubMedCrossRefGoogle Scholar
  52. Tajima F (1989) Statistical methods to test for nucleotide mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedCentralPubMedGoogle Scholar
  53. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi: 10.1093/molbev/msr121 PubMedCentralPubMedCrossRefGoogle Scholar
  54. Torti C, Gomulski LM, Malacrida AR, Capy P, Gasperi G (1998) Characterization and evolution of mariner elements from closely related species of fruit flies (Diptera: Tephritidae). J Mol Evol 46:288–298. doi: 10.1007/pl00006305 PubMedCrossRefGoogle Scholar
  55. Wallau GL, Hua-Van A, Capy P, Loreto EL (2011) The evolutionary history of mariner-like elements in Neotropical drosophilids. Genetica 139:327–338. doi: 10.1007/s10709-011-9552-6 PubMedCrossRefGoogle Scholar
  56. Yamada K, Kawanishi Y, Okuma S, Iwasaki H, Yamada A, Sasaki K, Nakajima Y, Maekawa H (2011) Comparative phylogenetic analysis of movable element, mariner-like element (MLE), among insects and spiders inhabiting South-West Islands in Japan. Entomotech 35:13–19 (in Japanese)Google Scholar
  57. Yoshiyama M, Tu Z, Kainoh Y, Honda H, Shono T, Kimura K (2001) Possible horizontal transfer of a transposable element from host to parasitoid. Mol Biol Evol 18:1952–1958. doi: 10.1093/oxfordjournals.molbev.a003735 PubMedCrossRefGoogle Scholar
  58. Zhou MB, Zhong H, Tang DQ (2011) Isolation and characterization of seventy-nine full-length mariner-like transposase genes in the Bambusoideae subfamily. J Plant Res 124:607–617Google Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Kaori Yamada
    • 1
  • Yuichi Kawanishi
    • 2
  • Akinori Yamada
    • 2
    • 3
  • Gaku Tokuda
    • 1
    • 2
  • Raj Deep Gurung
    • 1
  • Takeshi Sasaki
    • 4
  • Yumiko Nakajima
    • 1
    • 2
  • Hideaki Maekawa
    • 2
    Email author
  1. 1.Graduate School of Science and EngineeringUniversity of the RyukyusNishiharaJapan
  2. 2.Center of Molecular Biosciences, Tropical Biosphere Research CenterUniversity of the RyukyusNishiharaJapan
  3. 3.Faculty of FisheriesNagasaki UniversityNagasakiJapan
  4. 4.University MuseumUniversity of the RyukyusNishiharaJapan

Personalised recommendations