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Marine Biology

, Volume 143, Issue 1, pp 17–21 | Cite as

Polyploidy and polyteny in the gigantic eubacterium Epulopiscium fishelsoni

  • V. Bresler
  • L. FishelsonEmail author
Article

Abstract

Content and distribution of basic proteins, histones, acidic proteins and DNA, as well as the interaction of basic proteins with DNA, were studied microfluorometrically within nucleoid bodies of the gigantic eubacterium Epulopiscium fishelsoni living in the guts of the algivorous surgeonfish Acanthurus nigrofuscus. The fine structure of the bacterial nucleoid was studied using transmission electron microscopy (TEM). The mean content of basic proteins, histones and acidic proteins per nucleoid was directly proportional both to cell volume and DNA amount, proving that these proteins are integral components of bacterial chromatin. The maximal DNA quantity of ~1012 base pairs nucleoid−1 was found in the largest specimens of 354,000 µm3 volume (150-fold more then in human lymphocyte). Binding of proteins to DNA was strongest in cup-like nucleoids at the end of the bacterial life cycle, and weakest in enlarged and elongated nucleoids in mid-cycle. Contact fluorescent microscopy and TEM revealed a non-homogenous distribution of these proteins within the nucleoids, as well as the presence of giant polytene chromosome(s). We assume that the unusual genetic and morphological peculiarities, particularly increased polyploidy and polyteny, as revealed in E. fishelsoni, are the results of specific adaptations to the chemical conditions in the host's gut.

Keywords

Basic Protein Polytene Chromosome Deinococcus Radiodurans Methanococcus Bacterial Nucleoid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

Thanks are due to Prof. A.J. Bendich and Prof. K. Drlica (USA) for their constructive comments on a draft of the manuscript. Our gratitude goes to the Nature Protection Administration of Israel for permitting the collection of fish and to N. Paz for editing the manuscript. The constructive remarks of the reviewers are acknowledged. The experimental work in this study complied with the current laws in Israel.

References

  1. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD (1994) Molecular biology of the cell, 3rd edn. Garland, New YorkGoogle Scholar
  2. Angert ER, Clements KD, Pace NR (1993) The largest bacterium. Nature 382:239–241Google Scholar
  3. Angert ER, Brooks AE, Pace NR (1996) Phylogenetic analysis of Metabacterium polyspora: clues to the evolutionary origin of daughter cell production in Epulopiscium species, the largest bacterium. J Bacteriol 178:1451–1456PubMedGoogle Scholar
  4. Azam TA, Hiraga S, Ishihama A (2000) Two types of localization of the DNA-binding proteins within Escherichia coli nucleoid. Genes Cells 5:613–626CrossRefPubMedGoogle Scholar
  5. Bendich AJ, Drlica K (2000) Prokaryotic and eukaryotic chromosomes: what's the difference. BioEssays 22:481–486CrossRefPubMedGoogle Scholar
  6. Bhaud Y, Guillelault D, Lennon J, Defacque H, Soyer-Gobillard MO, Moreau H (2000) Morphology and behavior of dinoflagellates chromosomes during the cell cycle and mitosis. J Cell Sci 113:1231–1239PubMedGoogle Scholar
  7. Bresler V, Montgomery WL, Fishelson L, Pollak PL (1998) Gigantism in bacterium, Epulopiscium fishelsoni, correlates with complex patterns in arrangement, quantity, and segregations of DNA. J Bacteriol 180:5601–5611PubMedGoogle Scholar
  8. Campbell B, Nakagawa LK, Kobayashi MN, Hokama Y (1987) Gambierdiscus toxicus in gut content of the surgeonfish Ctenochaetus strigosus (herbivore) in relation to toxicity. Toxicon 25:1125–1127PubMedGoogle Scholar
  9. Clark G (1987) Staining procedures, 4th edn. Williams and Wilkins, BaltimoreGoogle Scholar
  10. Clements KD, Sutton DC, Choat JH (1989) Occurrence and characteristics of unusual protistan symbionts from surgeonfishes (Acanthuridae) of the Great Barrier Reef, Australia. Mar Biol 102:403–412Google Scholar
  11. Curtis SK, Cowden RR (1985) Microfluorimetric estimates of protein associated with murine hepatocyte and thymocyte nuclei, residual structures and nuclear matrix derivates. Histochemistry 82:331–339PubMedGoogle Scholar
  12. Fishelson L (1999) Polymorphism in gigantobacterial symbionts in the gut of surgeonfish (Acanthuridae, Teleostei). Mar Biol 133:345–351CrossRefGoogle Scholar
  13. Fishelson L, Montgomery WL, Myrberg AA (1985) Unique symbiosis in the gut of tropical herbivorous surgeonfish (Acanthuridae: Teleostei) from the Red Sea. Science 239:49–51Google Scholar
  14. Geyer G (1973) Ultrahistochemistry. Fischer , JenaGoogle Scholar
  15. Harborne JE (1993) Introduction to ecological biochemistry, 4th edn. Academic, LondonGoogle Scholar
  16. Hiraga S (2000) Dynamic localization of bacterial and plasmid chromosomes. Annu Rev Genet 34:21–59CrossRefPubMedGoogle Scholar
  17. Holmes VF, Cozzarelli NR (2000) Closing the ring: links between SMC proteins and chromosome partitioning, condensation and supercoiling. Proc Natl Acad Sci USA 97:1322CrossRefPubMedGoogle Scholar
  18. Jensen RB, Shapiro L (2000) Proteins in the move: dynamic protein localization in prokaryotes. Trends Cell Biol 10:483–488CrossRefPubMedGoogle Scholar
  19. Lewis PJ (2001) Bacterial chromosome segregation. Microbiology 147:519–526PubMedGoogle Scholar
  20. Montgomery WL, Pollak PE (1988) Epulopiscium fishelsoni n.g., n.sp., a protist of uncertain taxonomic affinities from the gut of an herbivorous reef fish. J Protozool 35:565–569Google Scholar
  21. Otto SP, Whitton J (2000) Polyploidy incidence and evolution. Annu Rev Genet 34:401–437CrossRefPubMedGoogle Scholar
  22. Ruch F (1973) Quantitative determination of DNA and protein in single cells. In: Thaer AA, Sernetz M (eds) Fluorescence techniques in cell biology. Springer, Berlin, pp 89–93Google Scholar
  23. Saier MH Jr, Paulsen IT, Sliwinski MK, Rao SS, Skurray RA, Nikaido H (1998) Evolutionary origins of multidrug and drug-specific efflux pumps in bacteria. FASEB J 12:265–274PubMedGoogle Scholar
  24. Sandman K, Pereira SI, Reeve JN (1998) Diversity of prokaryotic chromosomal proteins and the origin of the nucleosome. Cell Mol Life Sci 54:1350–1364PubMedGoogle Scholar
  25. Schulz NN, Jorgensen BB (2001) Big bacteria. Annu Rev Microbiol 55:105–137PubMedGoogle Scholar
  26. Sharpe ME, Errington J (1999) Upheaval in the bacterial nucleoid: an active chromosome segregation mechanism. Trends Genet 15:70–74CrossRefPubMedGoogle Scholar
  27. Sharpe ME, Hauser PM, Sharpe RG, Errington J (1999) Bacillus subtilis cell cycle as studied by fluorescence microscopy: constancy of cell length at initiation of DNA replication and evidence for active nucleoid partitioning. J Bacteriol 180:547–555Google Scholar
  28. Zybina EV, Zybina TG (1996) Polytene chromosomes in mammalian cells. Int Rev Cytol 165:53–119Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Institute for Nature Conservation Research, Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael
  2. 2.Department of Zoology, George S. Wise Faculty of Life SciencesTel Aviv UniversityTel AvivIsrael

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