Functional differentiation in bryozoan colonies: a proteomic analysis

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.

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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

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.

    Article  Google 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.

    CAS  Article  PubMed  Google 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.

    Article  PubMed  Google 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.

    Article  Google 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.

    CAS  Article  PubMed  Google 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.

    Article  Google 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.

    Google 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/

  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.

    Article  Google 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.

    CAS  Article  PubMed  Google 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.

    Article  Google Scholar 

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Correspondence to V. A. Kutyumov.

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Original Russian Text © V.A. Kutyumov, A.L. Maltseva, O.N. Kotenko, A.N. Ostrovsky, 2016, published in Tsitologiya, 2016, Vol. 58, No. 1, pp. 60–66.

The article was translated by the authors.

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Kutyumov, V.A., Maltseva, A.L., Kotenko, O.N. et al. Functional differentiation in bryozoan colonies: a proteomic analysis. Cell Tiss. Biol. 10, 152–159 (2016). https://doi.org/10.1134/S1990519X16020073

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Keywords

  • Bryozoa
  • functional differentiation
  • modular organisms
  • proteomic analysis
  • 2D-DIGE