Skip to main content

Advertisement

SpringerLink
Log in

Phylogenetic characterization of a microsporidium (Nosema sp. MPr) isolated from the Pieris rapae

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Cabbage butterfly (Pieris rapae), included in the Lepidoptera genus, Pieris family, is the main pest that damages Cruciferae. In this paper, we reported a microsporidian isolate of Nosema species which was isolated from P. rapae in Zhenjiang City, Jiangsu Province, China. The mature spore of this microsporidium is long oval in shape and 3.8 ± 0.3 × 2.0 ± 0.2 μm in size. Research results showed that the novel microsporidium cannot infect the BmN cell in vitro and silkworm larvae. The organization of rRNA gene was 5′-SSU rRNA-ITS-LSU rRNA-3′. Phylogenetic trees based on SSU rRNA and LSU rRNA gene sequences were constructed by MEGA 4.0 software. The topology showed that this microsporidium was on the same second branch of Nosema clade, and had close relationships to other Nosema species. Consequently, this microsporidium was confirmed to be a member of Nosema genus, and named as Nosema sp. MPr.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adl SM, Simpson AG, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup O, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MF (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol 52:399–451

    Article  PubMed  Google Scholar 

  • Baker MD, Vossbrinck CR, Didier ES, Maddox JV, Shadduck JA (1995) Small subunit ribosomal DNA phylogeny of various microsporidia with emphasis on AIDS related forms. J Eukaryot Microbiol 42:564–570

    Article  PubMed  CAS  Google Scholar 

  • Bhat SA, Bashir I, Kamili AS (2009) Microsporidiosis of silkworm, Bombyx mori L. (Lepidoptera-Bombycidae): a review. Afr J Agric Res 4:1519–1523

    Google Scholar 

  • Corradi N, Keeling PJ (2009) Microsporidia: a journey through radical taxonomical revisions. Fungal Biol Rev 23:1–8

    Article  Google Scholar 

  • Desser SS, Hong H et al (1992) Ultrastructure of the development of a species of Encephalitozoon cultured from the eye of an AIDS patient. Parasitol Res 78(8):677–683

    Article  PubMed  CAS  Google Scholar 

  • Dong SN, Shen ZY, Xu L, Zhu F (2010) Sequence and phylogenetic analysis of SSU rRNA gene of five microsporidia. Curr Microbiol 60:30–37

    Article  PubMed  CAS  Google Scholar 

  • Franzen C, Müller A (1999) Molecular techniques for detection, species differentiation, and phylogenetic analysis of microsporidia. Clin Microbiol Rev 12:243–285

    PubMed  CAS  Google Scholar 

  • Franzen C, Müller P, Hartmann P, Hegener M, Schrappe V (1998) Polymerase chain reaction for diagnosis and species differentiation of microsporidia. Folia Parasitol (Prague) 45:140–148

    CAS  Google Scholar 

  • Fries I, Ekbohm G, Villumstad E (1984) Nosema apis, sampling techniques and honey yield. J Apicult Res 23:102–105

    Google Scholar 

  • Fries I, Feng F, Silva AD, Slemenda SB, Pieniazek NJ (1996) Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur J Protistol 32:356–365

    Article  Google Scholar 

  • Gatehouse HS, Malone LA (1998) The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size. J Invertebr Pathol 71:97–105

    Article  PubMed  CAS  Google Scholar 

  • Gresoviac JS, Khattra SJ, Nadler AS, Kent LM, Devlin HR, Vivares PC, Fuente DLE, Hedrick PR (2000) Comparison of small subunit ribosomal RNA gene and internal transcribed spacer sequences among isolates of the intranuclear microsporidian Nucleospora salmonis. J Eukaryot Microbiol 47:379–387

    Article  PubMed  CAS  Google Scholar 

  • Hatakeyama Y, Kawakami Y, Iwano H, Inoue T, Ishihara R (1997) Analysis and taxonomic inference of small subunit ribosomal RNA sequences of five microsporidia pathogenic to the silkworm, Bombyx mori. J Seric Sci Jpn 66:242–252

    CAS  Google Scholar 

  • Hayasaka S, Sato T, Inoue H (1993) Infection and proliferation of microsporidians pathogenic to the silkworm, Bombyx mori L. and Chinese oak silkworm, Antheraea pernyi in Lepidopteran cell line. J Bull Natl Inst Seric Entomol Sci 7:47–63

    Google Scholar 

  • Hibbett DS, Binder M, Bischoff JF, Blackwell M, Cannon PF, Eriksson OE, Huhndorf S, James T, Kirk PM, Lücking R, Thorsten Lumbsch H, Lutzoni F, Matheny PB, McLaughlin DJ, Powell MJ, Redhead S, Schoch CL, Spatafora JW, Stalpers JA, Vilgalys R, Aime MC, Aptroot A, Bauer R, Begerow D, Benny GL, Castlebury LA, CrousPW DYC, Gams W, Geiser DM, Griffith GW, Gueidan C, Hawksworth DL, Hestmark G, Hosaka K, Humber RA, Hyde KD, Ironside JE, Kõljalg U, Kurtzman CP, Larsson KH, Lichtwardt R, Longcore J, Miadlikowska J, Miller A, Moncalvo JM, MozleyStandridge S, Oberwinkler F, Parmasto E, Reeb V, Rogers JD, Roux C, Ryvarden L, Sampaio JP, Schüssler A, Sugiyama J, Thorn RG, Tibell L, Untereiner WA, Walker C, Wang Z, Weir A, Weiss M, White MM, Winka K, Yao YJ, Zhang N (2007) A higher-level phylogenetic classification of the fungi. Mycol Res 111:509–547

    Article  PubMed  Google Scholar 

  • Huang WF, Jiang JH, Chen YW, Wang CH (2007) A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38:30–37

    Article  Google Scholar 

  • Huang WF, Bocquet M, Lee KC et al (2008) The comparison of rDNA spacer regions of Nosema ceranae isolates from different hosts and locations. J Invertebr Pathol 97:9–13

    Article  PubMed  CAS  Google Scholar 

  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J, Lumbsch HT, Rauhut A, Reeb V, Arnold AE, Amtoft A, Stajich JE, Hosaka K, Sung GH, Johnson D, O'Rourke B, Crockett M, Binder M, Curtis JM, Slot JC, Wang Z, Wilson AW, Schüssler A, Longcore JE, O'Donnell K, Mozley-Standridge S, Porter D, Letcher PM, Powell MJ, Taylor JW, White MM, Griffith GW, Davies DR, Humber RA, Morton JB, Sugiyama J, Rossman AY, Rogers JD, Pfister DH, Hewitt D, Hansen K, Hambleton S, Shoemaker RA, Kohlmeyer J, Volkmann-Kohlmeyer B, Spotts RA, Serdani M, Crous PW, Hughes KW, Matsuura K, Langer E, Langer G, Untereiner WA, Lücking R, Büdel B, Geiser DM, Aptroot A, Diederich P, Schmitt I, Schultz M, Yah R, Hibbett DS, Lutzoni F, McLaughlin DJ, Spatafora JW, Vilgalys R (2006) Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 443:818–822

    Article  PubMed  CAS  Google Scholar 

  • Johny S, Kanginakudru S, Muralirangan MC, Nagaraju J (2006) Morphological and molecular characterization of a new microsporidian (Protozoa: Microsporidia) isolated from Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae). Parasitology 132:803–814

    Article  PubMed  CAS  Google Scholar 

  • Kahler A, Thurston-Enriquez J (2007) Human pathogenic microsporidia detection in agricultural samples: method development and assessment. Parasitol Res 100(3):529–538

    Article  PubMed  Google Scholar 

  • Keeling PJ, Luker MA, Palmer JD (2000) Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol Biol Evol 17:23–31

    Article  PubMed  CAS  Google Scholar 

  • Kishore S, Baig M, Nataraju B, Balavenkatasubbaiah M, Sivaprasad V, Iyengar MNS, Datta RK (1994) Cross infectivity microsporidians isolated from wild Lepidopterous insects to silkworm, Bombyx mori L. Indian J Seric 33:126–130

    Google Scholar 

  • Ku CT, Wang CY, Tsai YC, Tzeng CC, Wang CH (2007) Phylogenetic analysis of two putative Nosema isolates from cruciferous lepidopteran pests in Taiwan. J Invertebr Pathol 95:71–76

    Article  PubMed  CAS  Google Scholar 

  • Müller A, Trammer T, Ghioralia G, Seitz HM, Diehl V, Franzen E (2000) Ribosomal RNA of Nosema algerae and phylogenetic relationship to other microsporidia. Parasitol Res 86:18–23

    Article  PubMed  Google Scholar 

  • Nilsen F, Endresen C, Hordvik I (1998) Molecular phylogeny of microsporidians with particular reference to species that infect the muscle of fish. J Eukaryot Microbiol 45:535–543

    Article  PubMed  CAS  Google Scholar 

  • Peyretaillade E, Biderre P, Peyret F, Duffieux G, Metenier M (1998) Microsporidian Encephalitozoon cuniculi, a unicellular eukaryote, with an unusual chromosomal dispersion of ribosomal genes and a LSU rRNA reduced to the universal core. Nucleic Acids Res 26:3513–3520

    Article  PubMed  CAS  Google Scholar 

  • Rao SN, Muthulakshmi M, Kanginakudru S, Nagaraju J (2004) Phylogenetic relationships of three new microsporidian isolates from the silkworm, Bombyx mori. J Invertebr Pathol 86:87–95

    Article  Google Scholar 

  • Rao SN, Nath BS, Saratchandra B (2005) Characterization and phylogenetic relationships among microsporidia infecting silkworm, Bombyx mori, using inter simple sequence repeat (ISSR) and small subunit rRNA (SSU-rRNA) sequence analysis. Genome 48:355–366

    Article  PubMed  CAS  Google Scholar 

  • Saková K, Sak B et al (2006) Humoral response of chicken infected with the microsporidium Encephalitozoon hellem. Parasitol Res 98(5):488–492

    Article  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tanada Y, Kaya HK (1993) Protozoan infections: Apicomplexa, microspora. In: Insect pathology. Academic Press, San Diego, pp 414–458

    Google Scholar 

  • Terry RS, MacNeil C, Dick JTA, Smith JE, Dunn AM (2003) Resolution of a taxonomic conundrum: an ultrastructural and molecular description of the life cycle of Pleistophora mulleri (Pfeiffer 1895; Georgevitch 1929). J Eukaryot Microbiol 50:266–273

    Article  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interference: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Tsai SJ, Kou GH, Lo CF, Wang CH (2002) Complete sequence and structure of ribosomal RNA gene of Heterosporis anguillarum. Dis Aquat Org 49:199–206

    Article  PubMed  CAS  Google Scholar 

  • Tsai SJ, Yamane S, Lo CF, Wang CH (2003) The characterization of microsporidian isolates (Nosematidae: Nosema) from five important lepidopteran pests in Taiwan. J Invertebr Pathol 83:51–59

    Article  PubMed  CAS  Google Scholar 

  • Undeen AH, Vavra J (1997) Research methods for entomopathogenic protozoa. In: Lacey LA (ed) Manual of techniques in insect pathology. Academic Press, San Diego, pp 117–151

    Google Scholar 

  • Vávra J, Kamler M et al (2011) Opportunistic nature of the mammalian microsporidia: experimental transmission of Trachipleistophora extenrec (Fungi: Microsporidia) between mammalian and insect hosts. Parasitol Res 108(6):1565–1573

    Article  PubMed  Google Scholar 

  • Waters PF, Snowden KF et al (2004) A comparison of homologous genes encoding aminopeptidases among bird and human Encephalitozoon hellem isolates and a rabbit E. cuniculi isolate. Parasitol Res 93(5):410–418

    Article  PubMed  Google Scholar 

  • Weiss LM, Vossbrinck CR (1999) Molecular biology, molecular phylogeny, and molecular diagnostic approaches to the Microsporidia. In: Wittner M, Weiss LM (eds.) The microsporidia and microsporidiosis. ASM Press, Washington, DC, 4:129–171

  • Xu XF, Shen ZY et al (2011) Phylogenetic characterization of a microsporidium (Endoreticulatus sp. Zhenjiang) isolated from the silkworm, Bombyx mori. Parasitol Res. doi:10.1007/s00436-011-2560-8

  • Zhu X, Wittner M, Tanowitz HB, Cali A, Weiss LM (1994) Ribosomal RNA sequences of Enterocytozoon bieneusi, Septata intestinalis and Ameson michaelis: phylogenetic construction and structural correspondence. J Eukaryot Microbiol 41:204–209

    Article  PubMed  CAS  Google Scholar 

  • Zhu F, Shen ZY, Xu XF, Tao HP, Dong SN, Tang XD, Xu L (2010) Phylogenetic analysis of complete rRNA gene sequence of Nosema philosamiae isolated from the Lepidopteran Philosamia cynthia ricini. J Eukaryot Microbiol 57:294–296

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the earmarked fund for the Modern Agro-industry Technology Research System. We are grateful to all who provided the means for us to access free software, which we have used and cited in this article. We thanked all partners and lab members for their kind help and criticism.

Author information

Authors and Affiliations

  1. Jiangsu University of Science and Technology, Zhenjiang, 212018, China

    Darui Chen, Zhongyuan Shen, Jiange Hou, Jiao Zhang, Xiaofang Xu, Xudong Tang & Li Xu

  2. Sericultural Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu Province, 212018, China

    Zhongyuan Shen, Feng Zhu, Rui Guan, Xudong Tang & Li Xu

  3. The Key Laboratory of Genetic Improvement of Silkworm and Mulberry of Agricultural Ministry, Zhenjiang, 212018, China

    Zhongyuan Shen

Authors
  1. Darui Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhongyuan Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Feng Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rui Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jiange Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xiaofang Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xudong Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Li Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhongyuan Shen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chen, D., Shen, Z., Zhu, F. et al. Phylogenetic characterization of a microsporidium (Nosema sp. MPr) isolated from the Pieris rapae . Parasitol Res 111, 263–269 (2012). https://doi.org/10.1007/s00436-012-2829-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-012-2829-6

Keywords

Search

Navigation