Skip to main content
SpringerLink
Log in

Skin mucus C-type lectin genes from all 19 Anguilla species/subspecies

  • Original Article
  • Biology
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

Fish skin and its corresponding mucus are important defenses against infections from pathogenic organisms, and several types of defensive molecules, particularly lectins, are often found in mucus. Freshwater eels of the genus Anguilla are widely distributed throughout the world, and the genus currently contains 16 species plus 3 subspecies. In this work, genomic sequences of skin mucus C-type lectin-encoding genes from all 19 presently known species/subspecies of the genus Anguilla were determined. The nucleotide sequences were approximately 2 kbp long, and the genomic structure of five exons and four introns was common in all species. All of the encoded C-type lectins were considered functional because of the presence of calcium ion-binding and sugar-binding motifs as well as conserved cysteine residues. Phylogenetic analysis of the genus indicated that the C-type lectins in freshwater eels might be divided into two clusters, corresponding to their temperate and tropical growth habitats, suggesting that Anguilla species C-type lectin has evolved to adapt to microflora in each environment. This study is the first to comprehensively describe the immune-related genes in a complete fish genus.

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
Fig. 4

Similar content being viewed by others

References

  1. Ege V (1939) A revision of the genus Anguilla Shaw, a systematic, phylogenetic and geographical study. Dana Rep 16:1–256

    Google Scholar 

  2. Castle PHJ, Williamson GR (1974) The validity of the freshwater eel species Anguilla ancestralis Ege from Celebes. Copeia 1974:569–570

    Article  Google Scholar 

  3. Watanabe S, Aoyama J, Tsukamoto K (2009) A new species of freshwater eel Anguilla luzonensis (Teleostei: Anguillidae) from Luzon Island of the Philippines. Fish Sci 75:387–392

    Article  CAS  Google Scholar 

  4. Aoyama J (2009) Life history and evolution of migration in catadromous eels (genus Anguilla). Aqua BioSci Monogr 2:1–42

    Article  Google Scholar 

  5. Aoyama J, Watanabe S, Miller MJ, Mochioka N, Otake T, Yoshinaga T, Tsukamoto K (2014) Spawning sites of the Japanese eel in relation to oceanographic structure and the West Mariana Ridge. PLoS One. doi:10.1371/journal.pone.0088759

    Google Scholar 

  6. Schmidt J (1922) The breeding places of the eel. Philos Trans R Soc Lond B 211:179–208

    Article  Google Scholar 

  7. Tesch FW (1977) The eel. Chapman and Hall Ltd, London

    Book  Google Scholar 

  8. Tsukamoto K (1992) Discovery of the spawning area for Japanese eel. Nature 356:789–791

    Article  Google Scholar 

  9. Tsukamoto K (2006) Spawning of eels near a seamount: tiny transparent larvae of the Japanese eel collected in the open ocean reveal a strategic spawning site. Nature 493:929

    Article  Google Scholar 

  10. Tsukamoto K, Chow S, Otake T, Kurogi H, Mochioka N, Miller MJ, Aoyama J, Kimura S, Watanabe S, Yoshinaga T, Shinoda A, Kuroki M, Oya M, Watanabe T, Hata K, Ijiri S, Kazeto Y, Nomura K, Tanaka H (2011) Oceanic spawning ecology of freshwater eels in the western North Pacific. Nat Commun 2:179. doi:10.1038/ncomms1174

    Article  PubMed Central  PubMed  Google Scholar 

  11. Alexander JB, Ingram GA (1992) Noncellular nonspecific defense mechanisms of fish. Ann Rev Fish Dis 2:249–279

    Article  Google Scholar 

  12. Ingram GA (1980) Substances involved in the natural resistance of fish to infection—a review. J Fish Biol 16:23–60

    Article  CAS  Google Scholar 

  13. Suzuki Y, Tasumi S, Tsutsui S, Okamoto M, Suetake H (2003) Molecular diversity of skin mucus lectins in fish. Comp Biochem Physiol 136B:723–730

    Article  CAS  Google Scholar 

  14. Barondes SH (1988) Bifunctional properties of lectins; lectin redefined. Trends Biochem Sci 13:480–482

    Article  CAS  PubMed  Google Scholar 

  15. Sharon N, Lis H (1972) Lectins: cell-agglutinating and sugar-specific proteins. Science 177:949–959

    Article  CAS  PubMed  Google Scholar 

  16. Tasumi S, Ohira T, Kawazoe I, Suetake H, Suzuki Y, Aida K (2002) Primary structure and characteristics of a lectin from skin mucus of the Japanese eel Anguilla japonica. J Biol Chem 277:27305–27311

    Article  CAS  PubMed  Google Scholar 

  17. Tasumi S, Yang WJ, Usami T, Tsutsui S, Ohira T, Kawazoe I, Wilder MN, Aida K, Suzuki Y (2004) Characteristics and primary structure of a galectin in the skin mucus of the Japanese eel, Anguilla japonica. Dev Comp Immunol 28:325–335

    Article  CAS  PubMed  Google Scholar 

  18. Aoyama J, Nishida M, Tsukamoto K (2001) Molecular phylogeny and evolution of the freshwater eel, genus Anguilla. Mol Phylogenet Evol 20:450–459

    Article  CAS  PubMed  Google Scholar 

  19. Minegishi Y, Aoyama J, Inoue JG, Miya M, Nishida M, Tsukamoto K (2005) Molecular phylogeny and evolution of the freshwater eels genus Anguilla based on the whole mitochondrial genome sequences. Mol Phylogenet Evol 34:134–146

    Article  CAS  PubMed  Google Scholar 

  20. Tanaka C, Shirotori F, Sato M, Ishikawa M, Shinoda A, Aoyama J, Yoshinaga T (2014) Genetic identification method for two subspecies of the Indonesian short-finned eel, Anguilla bicolor, using an allelic discrimination technique. Zool Stud 53:57. doi:10.1186/s40555-014-0057-8

    Article  Google Scholar 

  21. Yoshinaga T, Aoyama J, Shinoda A, Watanabe S, Azanza RV, Tsukamoto K (2014) Occurrence and biological characteristics of glass eels of the Japanese eel Anguilla japonica at the Cagayan River of Luzon Island, Philippines in 2009. Zool Stud 53:13. doi:10.1186/1810-522X-53-13

    Article  Google Scholar 

  22. Tsutsui S, Iwamoto K, Nakamura O, Watanabe T (2007) Yeast-binding C-type lectin with opsonic activity from conger eel (Conger myriaster) skin mucus. Mol Immunol 44:691–702

    Article  CAS  PubMed  Google Scholar 

  23. Breathnach R, Chambon P (1981) Organization and expression of eukaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383

    Article  CAS  PubMed  Google Scholar 

  24. Seif I, Khoury G, Dhar R (1979) BKV splice sequences based on analysis of preferred donor and acceptor sites. Nucleic Acids Res 6:3387–3398

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Drickamer K (1988) Two distinct classes of carbohydrate-recognition domains in animal lectins. J Biol Chem 263:9557–9560

    CAS  PubMed  Google Scholar 

  26. Drickamer K (1993) Ca2+-dependent carbohydrate-recognition domain in animal lectins. Curr Opin Struct Biol 3:393–400

    Article  CAS  Google Scholar 

  27. Drickamer K (1993) Evolution of Ca2+-dependent animal lectins. Prog Nucl Acid Res Mol Biol 45:207–232

    Article  CAS  Google Scholar 

  28. Weis WI, Drickamer K, Hendrickson WA (1992) Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature 360:127–134

    Article  CAS  PubMed  Google Scholar 

  29. Tsukamoto K, Watanabe S, Kuroki M, Aoyama J, Miller MJ (2014) Freshwater habitat use by a moray eel species, Gymnothorax polyuranodon, in Fiji shown by otolith microchemistry. Environ Biol Fish 97:1377–1385

    Article  Google Scholar 

  30. Teng HY, Lin YS, Tzeng CS (2009) A new Anguilla species and reanalysis of the phylogeny of freshwater eels. Zool Stud 48:808–822

    Google Scholar 

  31. Lin YS, Poh YP, Tzeng CS (2001) A phylogeny of freshwater eels inferred from mitochondrial genomes. Mol Phylogenet Evol 20:252–261

    Article  CAS  PubMed  Google Scholar 

  32. Inoue JG, Miya M, Miller MJ, Sado T, Hanel R, Hatooka K, Aoyama J, Minegishi Y, Nishida M, Tsukamoto K (2010) Deep-ocean origin of the freshwater eels. Biol Lett 6:363–366

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Marine Biosciences, Kitasato University, 1-15-1 Kitasato, Sagamihara, Kanagawa, 252-0373, Japan

    Shigeyuki Tsutsui, Tatsuki Yoshinaga & Osamu Nakamura

  2. College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa, 252-0880, Japan

    Shun Watanabe & Katsumi Tsukamoto

  3. Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba, 277-8564, Japan

    Jun Aoyama

Authors
  1. Shigeyuki Tsutsui
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tatsuki Yoshinaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shun Watanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jun Aoyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Katsumi Tsukamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Osamu Nakamura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shigeyuki Tsutsui.

Additional information

Nucleotide sequence data will be available in the DDBJ/EMBL/GenBank databases under the accession numbers LC049084–LC049102.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tsutsui, S., Yoshinaga, T., Watanabe, S. et al. Skin mucus C-type lectin genes from all 19 Anguilla species/subspecies. Fish Sci 81, 1043–1051 (2015). https://doi.org/10.1007/s12562-015-0922-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-015-0922-3

Keywords

Search

Navigation