Advertisement

Cell and Tissue Biology

, Volume 10, Issue 2, pp 152–159 | Cite as

Functional differentiation in bryozoan colonies: a proteomic analysis

  • V. A. KutyumovEmail author
  • A. L. Maltseva
  • O. N. Kotenko
  • A. N. Ostrovsky
Article

Abstract

Bryozoans are typical modular organisms. They consist of repetitive structural units, the zooids. Bryozoan colonies grow by zooidal budding, with the distribution pattern of the budding loci underlying the diversity of colony forms. Budding is usually restricted to the colony periphery, where a “growing edge” or local terminal growth zones are formed. Non-budding parts of the colony can be functionally subdivided, too. In many species colonies consist of regular, often repetitive zones of feeding and non-feeding modules, associated with a periodical degeneration and regeneration of the polypide retractile tentacle crown with a gut and the accompanying musculature. The mechanisms of functional differentiation in bryozoan colonies are unknown. Presumably, budding and/or polypide recycling are induced or inhibited by certain determinants of functional specialization in different colony parts. An effective tool of their identification is the comparison of proteomes in functionally different zones. Here we report the results of proteomic analysis of three bryozoan species from the White Sea with a different colony form: Flustrellidra hispida, Terminoflustra membranaceotruncata and Securiflustra securifrons. Using differential two-dimensional electrophoresis (2D-DIGE), we compared proteomes of the growing edge, the zone with polypides and the zone without polypides. We assessed the general level of differences between the zones and revealed proteins whose relative abundance changed gradually along the proximal-distal colony axis. These proteins might be involved in the determination of the functional differentiation of the colony.

Keywords

Bryozoa functional differentiation modular organisms proteomic analysis 2D-DIGE 

Abbreviations

LC-MS/MS

liquid chromatography-tandem quadrupole time-of-flight mass spectrometry

PAAG

polyacrylamide gel

CHAPS

3-[(3-cholamidopropyl)dimethy-lammonio]-1-propane sulfonate

ACN

acetonitrile

DTT

dithiothreitol

DIGE

differential electrophoresis

IEF

iso-electric focusing

IPG

immobilized ðÍ gradient

SDS

sodium dodecyl sulfate

Tris

Tris(hydroxymethyl)aminomethane

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Beklemishev, V.N., Osnovy sravnitel’noi anatomii bespozvonochnykh (Basics of Comparative Anatomy of Invertebrates), vol. 1: Promorfologiya (Promorphology), Moscow: Nauka, 1964.Google Scholar
  2. Boardman, R.S., Cheetham, A.H., Blake, D.B., Utgaard, J., Karklins, O.L., Cook, P.L., Sandberg, P.A., Lutaud, G., and Wood, T.S., Treatise on Invertebrate Paleontology, Vol. 1: Bryozoa (Part G, revised), Lawrence: Geological Society of America, University of Kansas, Boulder, 1983, pp. 1–625.Google Scholar
  3. Cheetham, A.H., Sanner, J., Taylor, P.D., and Ostrovsky, A.N., Morphological differentiation of avicularia and the proliferation of species in mid-Cretaceous Wilbertopora Cheetham, 1954 (Bryozoa: Cheilostomata), J. Paleontol., 2006, vol. 80, pp. 49–71.CrossRefGoogle Scholar
  4. Diz, A.P., Truebano, M., and Skibinski, D.O., The consequences of sample pooling in proteomics: an empirical study, Electrophoresis, 2009, vol. 30, pp. 2967–2975.CrossRefPubMedGoogle Scholar
  5. Dyrynda, P.E., A preliminary study of patterns of polypide generation-degeneration in marine cheilostome Bryozoa, in Recent and Fossil Bryozoa, Fredensborg: Olsen and Olsen, 1981, pp. 73–81.Google Scholar
  6. Hageman, S.J., Complexity generated by iteration of hierarchical modules in Bryozoa, Integr. Comp. Biol., 2003, vol. 43, pp. 87–98.CrossRefPubMedGoogle Scholar
  7. Hageman, S.J., Bock, P.E., Bone, Y., and McGowran, B., Bryozoan growth habits: classification and analysis, J. Paleontol., 1998, vol. 72, pp. 418–436.CrossRefGoogle Scholar
  8. Hyman, L.H., The Invertebrates: Smaller Coelomate Groups, Vol. V: Chaetognatha, Hemi-chordata, Pogonophora, Phoronida, Ectoprocta, Brachipoda, Sipunculida, the Coelomate Bilateria, New York: McGraw-Hill, 1959.Google Scholar
  9. Klyuge, G.A., Opredeliteli po faune SSSR (Identification Keys of the Fauna of USSR), vol. 76: Mshanki severnykh morey SSSR (Bryozoans of the North Seas of USSR), Moscow: Izd. Akad. Nauk SSSR, 1962.Google Scholar
  10. Lidgard, S., Budding process and geometry in encrusting cheilostome bryozoans, in Bryozoa: Ordovician to Recent, Fredensborg: Olsen and Olsen, 1985, pp. 175–182.Google Scholar
  11. Lidgard, S., Ontogeny in animal colonies: a persistent trend in the bryozoan fossil record, Science, 1986, vol. 232, pp. 230–232.CrossRefPubMedGoogle Scholar
  12. Lidgard, S. and Jackson, J.B., Growth in encrusting cheilostome bryozoans. I. Evolutionary trends, Paleobiology, 1989, vol. 15, pp. 255–282.Google Scholar
  13. Lidgard, S., Carter, M.C., Dick, M.H., Gordon, D.P., and Ostrovsky, A.N., Division of labor and recurrent evolution of polymorphisms in a group of colonial animals, Evol. Ecol., 2012, vol. 26, pp. 233–257.CrossRefGoogle Scholar
  14. Marfenin, N.N., The concept of modular organization in development, Zh. Obscch. Biol., 1999, vol. 60, 1, pp. 6–17.Google Scholar
  15. Marfenin, N.N., Fundamental patterns of modular organization in biology, Vestn. Tver. Univ. Ser. Biol. Ecol., 2008, vol. 9, pp. 147–161.Google Scholar
  16. McKinney, F.K. and Jackson, J.B., Bryozoan Evolution, Boston: Unwin Hyman, 1989.Google Scholar
  17. Nikulina, E.A., The evolution of colony morphogenesis in bryozoans of the order Cheilostomata, Paleontol. J., 2002, vol. 36, pp. 353–428.Google Scholar
  18. Ostrovsky, A.N., Evolution of Sexual Reproduction in Marine Invertebrates: Example of Gymnolaemate Bryozoans, Dordrecht: Springer, 2013.CrossRefGoogle Scholar
  19. R Core Team, R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria, 2015. ISBN 3-900051-07-0, URL http://www.R-project.org/Google Scholar
  20. Reed, C.G., Bryozoa, in Reproduction of Marine Invertebrates, Vol. 6: Echinoderms and Lophophorates. Pacific Grove: Boxwood Press, 1991, pp. 85–245.Google Scholar
  21. Ryland, J.S., Bryozoans, London: Hutchinson University Library, 1970.Google Scholar
  22. Ryland, J.S., Physiology and ecology of marine bryozoans, Adv. Mar. Biol., 1976, vol. 14, pp. 285–443.CrossRefGoogle Scholar
  23. Silén, L., Polymorphism, in Biology of Bryozoans, New York: Academic Press, 1977, pp. 184–232.Google Scholar
  24. Stach, L.W., Observations on Carbasea indivisa Busk (Bryozoa), Proc. Zool. Soc. London, 1938, vol. 108, pp. 389–399.Google Scholar
  25. Thiyagarajan, V., Wong, T., and Qian, P.Y., 2D gel-based proteome and phosphoproteome analysis during larval metamorphosis in two major marine biofouling invertebrates, J. Proteome Res., 2009, vol. 8, pp. 2708–2719.CrossRefPubMedGoogle Scholar
  26. Wang, H., Zhang, H., Wong, Y.H., Voolstra, C., Ravasi, T.B., Bajic, V., and Qian, P.Y., Rapid transcriptome and proteome profiling of a non-model marine invertebrate, Bugula neritina, Proteomics, 2010, vol. 10, pp. 2971–2981.Google Scholar
  27. Wong, Y.H., Arellano, S.M., Zhang, H., Ravasi, T., and Qian, P.Y., Research dependency on de novo protein synthesis and proteomic changes during metamorphosis of the marine bryozoan Bugula neritina, Proteome Sci., 2010, vol. 8, pp. 1–14.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • V. A. Kutyumov
    • 1
    Email author
  • A. L. Maltseva
    • 1
  • O. N. Kotenko
    • 1
  • A. N. Ostrovsky
    • 1
    • 2
  1. 1.Department of Invertebrate ZoologySt. Petersburg State UniversitySt. PetersburgRussia
  2. 2.Department of PalaeontologyUniversity of ViennaViennaAustria

Personalised recommendations