The Bacterial Nucleoid Revisited

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The Bacterial Nucleoid Revisited MICROBIOLOGICAL REVIEWS, June 1994, p. 211-232 Vol. 58, No. 2 0146-0749/94/$04.O0+0 Copyright © 1994, American Society for Microbiology The Bacterial Nucleoid Revisited CARL ROBINOW'* AND EDUARD KELLENBERGER2,3* Department of Microbiology and Immunology, Health Sciences Centre, University of Westem Ontario, London, Canada N6A SC],' and Institut de Gene'tique et de Biologie Microbiennes, Universite de Lausanne, CH-1005 Lausanne,2 and Biozentrum der Universitat Basel, CH-4056 Basel,3 Switzerland REFLECTIONS ON THE HISTORY OF BACTERIAL CARYOLOGY.............................................................211 GROSS ANATOMY OF THE NUCLEOID: RECALL AND REVISION............................................................212 The Road from "Nuclear Material" to "Nucleoid" and Back Again ..............................................................212 HCl-Giemsa Must Be Taken with a Grain of Salt............................................................................. 213 Acid Hydrolysis of Osmium-Fixed Bacteria Endows Nucleoids with an Affinity for Purple Components of Standard Giemsa Stain Which They Normally Lack.........................................................214 The Nucleoid in Bouin-Thionin Preparations ............................................................................. 215 The Nucleoids in Cyanobacteria Remembered............................................................................. 216 ELECTRON MICROSCOPY OF BACTERIAL DNA-PLASMS IN SITU..........................................................216 Early Results of the Electron Microscopy of Bacteria and the Evolution of RK Fixation ..........................216 Conciliation of Nucleoid Morphology as Seen in the Light Microscope with That of Nucleoids in Thin Sections ............................................................................. 221 CHANGING VIEWS OF THE NUCLEOID............................................................................. 222 Shortcomings of RK Fixation, and How They Were Overcome by Autoradiography...................................222 New View of the Nucleoid Provided by CFS Treatment............................................................................. 223 FUNCTION-STRUCTURE RELATIONSHIPS ............................................................................. 224 Tracing Sites of DNA and mRNA in Sections of CFS-Treated Bacteria........................................................224 DNA ............................................................................. 224 RNA ............................................................................. 224 The Shape of Nucleoids Reflects the Level of Their Metabolic Activities......................................................224 Ill-Defined Interlinked "Nucleoids"............................................................................ 225 Looking for a Resting DNA-Plasm............................................................................ 225 GIANT BACTERIA............................................................................ 225 A SIDEWAYS GLANCE AT THE CHROMOSOMES OF DINOFLAGELLATES ...........................................226 CURRENT CONCERNS............................................................................. 228 ACKNOWLEDGMENTS ............................................................................ 229 REFERENCES ....................................................................................... 229 REFLECTIONS ON THE HISTORY OF BACTERIAL at, bacteria. Efficient ways of looking for bacteria had been CARYOLOGY brilliantly demonstrated by Koch (68) with his photographs of Bacillus anthracis and other bacteria stained with synthetic Unbending after a deep bow in the direction of Leeuwen- dyes that had recently become available. Refined to the level of hoek and Pasteur, we may reasonably assert that modern the Gram procedure and of special methods for certain bacteriology had its beginnings in the last quarter of the hard-to-stain organisms, these diagnostic morphological nineteenth century. The gross anatomy of bacterial cells is tech- readily described in a few short paragraphs, and their compo- niques of the laboratory are still in daily use worldwide. By and nent parts are well within the resolving power of microscopes large they reduce bacteria to a kind of Morse code of solidly equipped with the highly corrected objective lenses and com- colored dots and dashes (cocci and rods) lacking internal pensating eyepieces that became generally available in the differentiation. 1880s. In this essay we are trying to explain why, despite all this, Such images did little to arouse cytological curiosity, and in it is only very recently that the nature of the bacterial nucleoid the busy laboratories of applied bacteriology the study of has been clearly revealed and why even now there are uncer- bacterial cell structure was indeed rarely pursued. Two other tainties about some of its features. Bacteriologists working in factors contributed to the then prevailing lack of interest in the newly created laboratories of hospitals and Public Health bacterial cytology: the seemingly glass-like featureless translu- Authorities were first and foremost concerned with diagnosis. cency of living unstained bacteria from young cultures, and the They were microscopists who looked, one might say, for, not failure of well-tried old, natural histological stains such as carmine and hematoxylin and a host of new synthetic ones to reveal significant intelligible structures within the kind of * Corresponding authors. Mailing address for C. Robinow: Depart- bacteria most often encountered in medical laboratories. ment of Microbiology and Immunology, Health Sciences Centre, Microbiologists who had kept aloof from the "Hetzjagd der University of Western Ontario, London, Ontario, Canada N6A SCi. Bakterienstreberei" "the hot chase after noto- Phone: (519) 661-3427. Fax: (519) 661-3499. (approximately Mailing address for E. Kellenberger: Institut de Genetique et de riety in the field of bacteriology") grimly noted by deBary (18) Biologie Microbiennes, Universite de Lausanne, Rue Cesar-Roux 19, continued to ask questions about the anatomy of the bacterial CH-1005 Lausanne, Switzerland. Phone: 41 (21) 3206075. Fax: 41 (21) cell and were thus led to look for something corresponding to 3206078. a nucleus. They seem to have been an industrious lot, to judge 211 212 ROBINOW AND KELLENBERGER MICROBIOL. REV. 1 FIG. 1. Nucleoids in cells from a growing culture of a Bacillus species isolated from greenhouse soil, fixed with osmium tetroxide vapor and stained with HCl-Giemsa. The nucleoids of the three bacilli below, above, and to the right of the asterisk were preserved while going through the typical Piekarski round in which two nucleoids divide to make a set of four. Bar, 5 p,m. by the more than 400 papers on eubacterial and cyanobacterial the bacteria were cultured under conditions which made them cytology reviewed by Delaporte (21) in the introduction to the grow with short generation times. It was in samples of cells record of her own far-ranging observations. The bacterial cell, from such cultures that Piekarski found regular numbers of it could no longer be doubted, has its own kind of "corps neatly spaced Feulgen-positive bodies (also seen by Stille [117] chromatique," probably as necessary for the performance of in cells from young cultures of B. subtilis) of a narrow range of vital functions and for reproduction as are the nuclei of the sizes, whose orderly behavior suggested that they represented cells of higher organisms. However, the occurrence of bacterial some kind of basic entity whose reproduction was correlated "materiel nucleaire" in a protean array of configurations, with that of the bacteria containing them and which the author including axial filaments, networks, and random scatters of appropriately, if somewhat boldly, named "nucleoids." irregular granules, suggested to the reviewer, not unreason- At the same time it was shown by Piekarski that the sites of ably, that the forms assumed by bacterial chromatin had no the distinctly but only faintly positive Feulgen reaction could, obvious functional significance. Large, promising species, oc- after the acid hydrolysis which forms step I of the Feulgen casionally brought in from the wild, tended to disappoint their procedure, be brightly and selectively colored with some of the discoverers because they often could not be propagated in the components of the complex Giemsa stain (this protocol will be laboratory. Established ubiquitous species such as B. mycoides referred to in this review as HCl-Giemsa). Lastly, the results of and B. megaterium were not neglected but tended to be this work were presented in unambiguous photomicrographs. examined at late stages of their growth cycle, when coordina- Nucleoids were soon demonstrated in several other kinds of tion of the reproduction of chromatinic elements with that of bacteria by Neumann (81), who had obtained good results-with the organism containing them, obvious in cells from fast- straight Giemsa stain. Further confirmation of Piekarski's and growing young cultures, is often no longer apparent. It is easy Neumann's work was to see why, up to the end of the 1930s, bacterial cytology had provided by Robinow (90-93, 95), who failed to attract the attention of caryologists, who saw more favored the cells of young Bacillus cultures and relied chiefly rewarding and challenging materials for the exercise of their on HCI-Giemsa (Fig. 1). Tulasne
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