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Marine Biotechnology

, Volume 17, Issue 5, pp 523–532 | Cite as

Integration of Transcriptomic and Proteomic Approaches Provides a Core Set of Genes for Understanding of Scallop Attachment

  • Yan Miao
  • Lingling Zhang
  • Yan Sun
  • Wenqian Jiao
  • Yangping Li
  • Jin Sun
  • Yangfan Wang
  • Shi Wang
  • Zhenmin BaoEmail author
  • Weizhi LiuEmail author
Original Article

Abstract

Attachment is an essential physiological process in life histories of many marine organisms. Using a combination of transcriptomic and proteomic approach, scallop byssal proteins (Sbps) and their associated regulatory network genes were investigated for the first time. We built the first scallop foot transcriptome library, and 75 foot-specific genes were identified. Through integration of transcriptomic-proteomic approach, seven unique Sbps were identified. Of them, three showed significant amino acid sequence homology to known proteins. In contrast, the rest did not show significant protein matches, indicating they are possibly novel proteins. Our transcriptomic and proteomic analyses also suggest that post-translational modification may be one of the significant features for Sbps as well. Taken together, our study provides the first multidimensional collection of a core set of genes that may be potentially involved in scallop byssal attachment.

Keywords

Scallop Adhesion Byssus Transcriptome Proteomics 

Notes

Acknowledgments

This work was supported by National High Technology Research and Development Program of China (2012AA092204), National Natural Science Foundation of China (31472258) and Natural Science Foundation for Distinguished Young Scholars of Shandong Province (JQ201308).

Supplementary material

10126_2015_9635_MOESM1_ESM.doc (35 kb)
Table S1 All Mfp-relevant genes in GenBank; (DOC 35 kb)
10126_2015_9635_MOESM2_ESM.doc (2.1 mb)
Figure S1 Amino acids sequence alignment for the putative Sbp components with their homologs. (DOC 2141 kb)
10126_2015_9635_MOESM3_ESM.xlsx (18 kb)
ESM 1 The significant enriched terms were highlighted in different sheets for biological process, molecular function and cellular component, respectively. (XLSX 17 kb)

References

  1. Alejandrino A, Puslednik L, Serb JM (2011) Convergent and parallel evolution in life habit of the scallops (Bivalvia: Pectinidae). BMC Evol Biol 11:164PubMedCentralCrossRefPubMedGoogle Scholar
  2. Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351–1362CrossRefPubMedGoogle Scholar
  3. Cha HJ, Hwang DS, Lim S (2008) Development of bioadhesives from marine mussels. Biotechnol J 3:631–638CrossRefPubMedGoogle Scholar
  4. Gantayet A, Ohana L, Sone ED (2013) Byssal proteins of the freshwater zebra mussel, Dreissena polymorpha. Biofouling 29:77–85CrossRefPubMedGoogle Scholar
  5. Gantayet A, Rees DJ, Sone ED (2014) Novel proteins identified in the insoluble byssal matrix of the freshwater zebra mussel. Mar Biotechnol (NY) 16:144–155CrossRefGoogle Scholar
  6. Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A (2008) High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36:3420–3435PubMedCentralCrossRefPubMedGoogle Scholar
  7. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652PubMedCentralCrossRefPubMedGoogle Scholar
  8. Gruffydd LD (1978) The byssus and byssus glands in Chlamys islandica and other scallops (lamellibranchia). Zool Script 7:277–285CrossRefGoogle Scholar
  9. Hagenau A, Scheidt HA, Serpell L, Huster D, Scheibel T (2009) Structural analysis of proteinaceous components in Byssal threads of the mussel Mytilus galloprovincialis. Macromol Biosci 9:162–168CrossRefPubMedGoogle Scholar
  10. Harrington MJ, Waite JH (2007) Holdfast heroics: comparing the molecular and mechanical properties of Mytilus californianus byssal threads. J Exp Biol 210:4307–4318CrossRefPubMedGoogle Scholar
  11. Hennebert E, Wattiez R, Waite JH, Flammang P (2012) Characterization of the protein fraction of the temporary adhesive secreted by the tube feet of the sea star Asterias rubens. Biofouling 28:289–303CrossRefPubMedGoogle Scholar
  12. Hennebert E, Wattiez R, Demeuldre M, Ladurner P, Hwang DS, Waite JH, Flammang P (2014) Sea star tenacity mediated by a protein that fragments, then aggregates. Proc Natl Acad Sci U S A 111:6317–6322PubMedCentralCrossRefPubMedGoogle Scholar
  13. Holm ER (2012) Barnacles and biofouling. Integr Comp Biol 52:348–355CrossRefPubMedGoogle Scholar
  14. Holten-Andersen N, Waite JH (2008) Mussel-designed protective coatings for compliant substrates. J Dent Res 87:701–709PubMedCentralCrossRefPubMedGoogle Scholar
  15. Hwang DS, Zeng H, Masic A, Harrington MJ, Israelachvili JN, Waite JH (2010) Protein- and metal-dependent interactions of a prominent protein in mussel adhesive plaques. J Biol Chem 285:25850–25858PubMedCentralCrossRefPubMedGoogle Scholar
  16. Inoue K, Takeuchi Y, Miki D, Odo S (1995) Mussel adhesive plaque protein gene is a novel member of epidermal growth factor-like gene family. J Biol Chem 270:6698–6701CrossRefPubMedGoogle Scholar
  17. Kamino K (2001) Novel barnacle underwater adhesive protein is a charged amino acid-rich protein constituted by a Cys-rich repetitive sequence. Biochem J 356:503–507PubMedCentralCrossRefPubMedGoogle Scholar
  18. Kamino K (2008) Underwater adhesive of marine organisms as the vital link between biological science and material science. Mar Biotechnol (NY) 10:111–121CrossRefGoogle Scholar
  19. Kamino K, Nakano M, Kanai S (2012) Significance of the conformation of building blocks in curing of barnacle underwater adhesive. FEBS J 279:1750–1760CrossRefPubMedGoogle Scholar
  20. Lee H, Scherer NF, Messersmith PB (2006) Single-molecule mechanics of mussel adhesion. Proc Natl Acad Sci U S A 103:12999–13003PubMedCentralCrossRefPubMedGoogle Scholar
  21. Lee BP, Messersmith PB, Israelachvili JN, Waite JH (2011) Mussel-inspired adhesives and coatings. Annu Rev Mater Res 41:99–132PubMedCentralCrossRefPubMedGoogle Scholar
  22. Lin Q, Gourdon D, Sun C, Holten-Andersen N, Anderson TH, Waite JH, Israelachvili JN (2007) Adhesion mechanisms of the mussel foot proteins mfp-1 and mfp-3. Proc Natl Acad Sci U S A 104:3782–3786PubMedCentralCrossRefPubMedGoogle Scholar
  23. Mehdizadeh M, Yang J (2013) Design strategies and applications of tissue bioadhesives. Macromol Biosci 13:271–288PubMedCentralCrossRefPubMedGoogle Scholar
  24. Meyer E, Aglyamova GV, Wang S, Buchanan-Carter J, Abrego D, Colbourne JK, Willis BL, Matz MV (2009) Sequencing and de novo analysis of a coral larval transcriptome using 454 GSFlx. BMC Genomics 10:219PubMedCentralCrossRefPubMedGoogle Scholar
  25. Mori Y, Urushida Y, Nakano M, Uchiyama S, Kamino K (2007) Calcite-specific coupling protein in barnacle underwater cement. FEBS J 274:6436–6446CrossRefPubMedGoogle Scholar
  26. Qin XX, Coyne KJ, Waite JH (1997) Tough tendons. Mussel byssus has collagen with silk-like domains. J Biol Chem 272:32623–32627CrossRefPubMedGoogle Scholar
  27. Rebl A, Korytar T, Kobis JM, Verleih M, Krasnov A, Jaros J, Kuhn C, Kollner B, Goldammer T (2014) Transcriptome profiling reveals insight into distinct immune responses to Aeromonas salmonicida in gill of two rainbow trout strains. Mar Biotechnol (NY) 16:333–348CrossRefGoogle Scholar
  28. Shao H, Bachus KN, Stewart RJ (2009) A water-borne adhesive modeled after the sandcastle glue of P. californica. Macromol Biosci 9:464–471PubMedCentralCrossRefPubMedGoogle Scholar
  29. Shi M, Lin Y, Xu G, Xie L, Hu X, Bao Z, Zhang R (2013) Characterization of the Zhikong scallop (Chlamys farreri) mantle transcriptome and identification of biomineralization-related genes. Mar Biotechnol (NY) 15:706–715CrossRefGoogle Scholar
  30. Silverman HG, Roberto FF (2007) Understanding marine mussel adhesion. Mar Biotechnol (NY) 9:661–681CrossRefGoogle Scholar
  31. Stewart RJ (2011) Protein-based underwater adhesives and the prospects for their biotechnological production. Appl Microbiol Biotechnol 89:27–33PubMedCentralCrossRefPubMedGoogle Scholar
  32. Sun J, Zhang H, Wang H, Heras H, Dreon MS, Ituarte S, Ravasi T, Qian PY, Qiu JW (2012) First proteome of the egg perivitelline fluid of a freshwater gastropod with aerial oviposition. J Proteome Res 11:4240–4248CrossRefPubMedGoogle Scholar
  33. Sun J, Chen Q, Lun JC, Xu J, Qiu JW (2013) PcarnBase: development of a transcriptomic database for the brain coral Platygyra carnosus. Mar Biotechnol (NY) 15:244–251CrossRefGoogle Scholar
  34. Waite JH (2008) Mussel power. Nat Mater 7:8–9CrossRefPubMedGoogle Scholar
  35. Waite JH, Broomell CC (2012) Changing environments and structure–property relationships in marine biomaterials. J Exp Biol 215:873–883PubMedCentralCrossRefPubMedGoogle Scholar
  36. Werner GD, Gemmell P, Grosser S, Hamer R, Shimeld SM (2013) Analysis of a deep transcriptome from the mantle tissue of Patella vulgata Linnaeus (Mollusca: Gastropoda: Patellidae) reveals candidate biomineralising genes. Mar Biotechnol (NY) 15:230–243CrossRefGoogle Scholar
  37. Xiaoli Hu ZB, Jingjie H, Shao M, Zhang L, Bi K, Zhan A, Huang X (2006) Cloning and characterization of tryptophan 2,3-dioxygenase gene of Zhikong scallop Chlamys farreri (Jones and Preston 1904). Aquacult Res 37:1187–1194CrossRefGoogle Scholar
  38. Zhang L, Li L, Zhu Y, Zhang G, Guo X (2014) Transcriptome analysis reveals a rich gene set related to innate immunity in the Eastern oyster (Crassostrea virginica). Mar Biotechnol (NY) 16:17–33CrossRefGoogle Scholar
  39. Zhao H, Waite JH (2005) Coating proteins: structure and cross-linking in fp-1 from the green shell mussel Perna canaliculus. Biochemistry 44:15915–15923PubMedCentralCrossRefPubMedGoogle Scholar
  40. Zhao H, Waite JH (2006) Linking adhesive and structural proteins in the attachment plaque of Mytilus californianus. J Biol Chem 281:26150–26158CrossRefPubMedGoogle Scholar
  41. Zhao H, Robertson NB, Jewhurst SA, Waite JH (2006) Probing the adhesive footprints of Mytilus californianus byssus. J Biol Chem 281:11090–11096CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Yan Miao
    • 1
  • Lingling Zhang
    • 1
  • Yan Sun
    • 1
  • Wenqian Jiao
    • 1
  • Yangping Li
    • 1
  • Jin Sun
    • 2
  • Yangfan Wang
    • 1
  • Shi Wang
    • 1
  • Zhenmin Bao
    • 1
    Email author
  • Weizhi Liu
    • 1
    Email author
  1. 1.Ministry of Education Key Laboratory of Marine Genetics and Breeding, College of Marine Life SciencesOcean University of ChinaQingdaoChina
  2. 2.Department of BiologyHong Kong Baptist University Hong KongChina

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