Bacterial Chromosome

Eduard Kellenberger, University of Lausanne, Lausanne, Switzerland Jing-Yan Li, Kuming Institute of Zoology, Chinese Academy of Sciences, China
Under conditions favouring most active growth, bacteria replicate their DNA and divide with generation times as short as 20–25 minutes; similary rapid rates are practically unknown in other taxa. In contrast to the typical eukaryotic cell, DNA transcription, translation and replication occur simultaneously and at nearby locations. The highly dynamic processes lead to a reticulation of DNA and RNA, permitting optimization of mRNA interaction (number of contacts) with ribosomes. Increased order in the chromatin seems to occur only with very much slower overall growth.

Secondary article
Article Contents
. Introduction . Functions, Size and Nature of the Bacterial Chromosome and its Packing into the Cell . New Views of the Bacterial Chromatin Using Cryofixation and Freeze-substitution . The Bacterial Chromatin is Supercoiled . Histones, Histone-like Proteins and Nucleosomes

During the 1950s, a deoxyribonucleic acid (DNA)-specific cytological staining (of the Feulgen type) of chemicallyfixed bacteria revealed in the light microscope, one, two or even four strongly stained ‘patches’ per cell. In cells of higher organisms, this staining was known to be confined to the nucleus and defined the chromatin and the chromosomes (Gr. khroma colour). This shared staining pattern gave rise to the terms ‘bacterial chromosomes’, ‘nucleoids’ or ‘nuclear equivalents’, all meaning these same, coloured patches. After removing the ribonucleic acid (RNA) by digestion with ribonuclease to leave only DNA for staining, these results were further confirmed. More recently, the staining with DNA-specific fluorescent dyes, such as 4’,6-diamidino-2-phenylindole (DAPI), substantiates these earlier results and provides an easier approach. With such dyes, it is now even possible to stain the DNA of live cells without disturbing their growth (Figure 1). Owing to the limited resolution ($ 0.2 mm), it is impossible to define exactly the shape of nucleoids in light micrographs, particularly because the size and shape of these patches is extremely variable and dependent on the preparation methods and growth media used. At about the same time, toward the middle of the twentieth century, bacterial mutants (variants) were discovered, which ‘breed true’, i.e. in which the overwhelming majority of the descendants of an individual mutant cell carry the altered character. In the decade following Watson and Crick’s double helix proposal (1953) of a linear genetic code, the widespread acceptance of the DNA molecule as the support for the cell’s genetic information displaced the earlier belief that proteins fulfilled this role and led to a great increase in research on DNA, so that knowledge of bacterial genetics progressed rapidly. Microbial taxonomy has been revolutionized through the use of new techniques of DNA and RNA sequence analysis. By comparing, for example, the detailed base sequence of 16S ribosomal RNAs, Woese proposed that

there were two branches of the former bacteria: the Bacteria and the Archaea, of which the latter seem to share more with Eukarya than the former (as discussed later in this entry). As very few ultrastructural

Figure 1 In vivo, fluorescently stained, Escherichia coli. DAPI is added to a culture of exponentially growing cells in an amount determined experimentally for each strain and medium; being low enough not to inhibit growth. Viewed under near blue ultraviolet fluorescence and phase contrast. The latter is necessary for visualizing the bacterial ‘body’.

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the packing density was defined by Woldringh and Nanninga as the local concentration of DNA (mg mL 2 1). Further. This conclusion was confirmed independently. illustrating previous biochemical findings that transcription and translation occur simultaneously in bacteria. which are not occupied by the histone-like. crosslinking proteins? Or is it a more ‘mobile’ randomly distributed structure. Miller found an essential difference: within the bacteria. by genetic methods. He found large circles with a 1300-mm circumference. Is the packing of the chromosome the result of a folding into a defined three-dimensional structural pattern that is determined by specific interactions with ‘condensing principles’.g. one purpose of bound proteins might be precisely the prevention of spontaneous aggregation (condensation) of DNA. are some ten times more condensed. they are responsible for the cell turgor pressure. highly specific condensing mechanisms. The latter can be simulated in vitro. The other space-saving organization characteristic of DNA is that of compaction by supercoiling. basic proteins. the twigs of mRNA were studded with ribosomes. coli cell with two nucleoids). When similar calculations were made for eukaryotic DNA in the interphase (in which DNA undergoes replication) nucleus of a liver cell. resembling intracellular conditions. such as specific. the 50-mm long bacteriophage T2 DNA condenses into individual particles that. Size and Nature of the Bacterial Chromosome and its Packing into the Cell Taking great care to minimize shearing. 20–40 mg mL 2 1 was also obtained. coli cell and spread it onto a photographic plate to record autoradiographic images. by addition of polyethylene glycol (PEG). with an increasing length of the ‘twigs’ towards one end. microscopic) studies have yet been made on the nucleoids of archaea. He also demonstrated the process of replication of such circles. on nearby sites. They form associations with lower dissociation constants than with the monovalent potassium ions.els. putrescine and spermidine are important as neutralizing partners of the negatively charged phosphate groups of DNA.e.3 mm. Ca2 1 . i. When comparing nuclear DNA of eukaryotes with that isolated from bacteria. more than 10 times smaller than the length of the ‘artificially’ unravelled DNA. In experimental conditions in vitro. the ‘condensates’ had a size comparable to that of mature phage.5 Â 10 2 14 g mass of DNA of chromosome and 1. in eukaryotes. obviously inhibits replication and transcription. Intracellular. generally more abundant extracellularly. ‘Christmas trees’. coli cell of 2–3-mm length and some 0. For the first it is too frequently forgotten that intracellular concentrations of small molecular weight solutes in growing bacteria are generally 2–3 times higher than those of the medium. at 200–300 mg mL 2 1. however. e. and Escherichia coli in particular. we concentrate mainly on the results of the more thoroughly studied bacteria. as in eukaryotic metaphase chromosomes. The foregoing findings strongly suggest that achieving the low packing densities encountered in vivo in growing bacterial cells (20 mg mL 2 1). i.8-mm diameter is often erroneously considered as a remarkable feat requiring a high degree of condensation and compaction. and in the DNA pool of replicating and transcribing ‘vegetative phage’. are visible even by light microscopy. requires no particular. To accommodate the 1300-mm long chromosome into an E. Cairns (1963) isolated the radioactive isotopically labelled DNA of an E. a set of essential observations were made by Miller (1973) using electron microscopy: DNA was isolated from metabolizing cells in such a way that the synthesized messenger RNA (mRNA) transcript remained attached to the DNA and formed tree-like patterns. which. reflecting simply those specific metabolic functions actively undergoing transcription-translation as well as those involved in the replication of the chromosome for a given cell environment and growth phase? Highly relevant are recent physical chemistry experiments involving ‘spontaneous’ condensation of DNA as a consequence of increased ion concentrations and of ‘crowding’ effects. With similar experiments. We have to conclude that the condensation of the bacterial chromosomes is comparable to that of the eukaryotic interphase nucleus and thus does not require any procedure of an exceptional nature. In contrast. positively charged Mg2 1 . with fluorescent staining. condensed chromosomes taking up posi2 tions on the equatorial plane of the (three-dimensional) spindle apparatus. Functions.4 Â 10 2 12 mL volume of an E. Nature Publishing Group / www. the mRNA has to become detached from the DNA and to move out of the nucleus into the cytoplasm before translation can begin. but using electron microscopy. . and DNA in bacterial viruses can even reach 800 to 1000 mg mL 2 1! These chromosomes are associated with nonreplicating. the radius of the particles is estimated to be about 0. is replaced intracellularly by K 1 . ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd. and Cl 2 by negatively charged amino acids (like glutamic acid) and other small molecular organic substances.e.e. This is discussed below. neatly demonstrating that the genetic apparatus of a bacterium consists of a single linear molecule of DNA in the form of a (closed) circle. probably reflecting relative levels in the conditions in which bacteria evolved. Estimates of some 20 mg mL 2 1 were found for the DNA of actively growing bacteria (1. ignoring differentially stained eu-and heterochromatin. when strong enough. Taking into account the light microscope’s limited resolution. To quantify these parameters.Bacterial Chromosome (i. Metaphase chromosomes. Na 1 .

Water-containing biological material can be frozen so rapidly that its water is transformed into the vitreous state. 40 times that of the light microscope. For DNA. it can be subjected to thin slicing or microtomy. developed for the study of eukaryotic cells and tissues. The nonuniform distribution of ribosomes can be distinguished.8-mm bacteria. 0.. while still solid. the frozen material at low temperature can also be freeze-substituted by organic solvents. The fibrillar material was directly identified. ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd. noncrystalline. 1991). the ‘DNA-containing plasm’. such as acetone or methanol. i. A fundamental change came with the introduction of cryotechniques. taken from the middle part of the cell. the DNA-dependent Figure 2 Serial. For the rather globular content of the ribosome-free spaces of CFS-prepared bacteria. The method is thus ideal for several layers of 0. According to Miller’s experiments.5 mm. which replaces the fibrillar one visible within the nucleoids obtained with the previously employed Ryter–Kellenberger (R-K)-technique.e. The same cytological techniques of fixation and embedding applied to bacteria yielded disappointing results: the bacterial DNA was in the form of randomly shaped aggregates within an otherwise empty zone. Cryofixation is not simply a temperature reversible immobilization. Such frozen and still hydrated material can be cryosectioned. indirect identification had to be made by immunocytochemistry. longitudinal sections of Escherichia coli. 1991). the ice is dissolved slowly into the solvent. Improved fixation prevented the aggregation of the DNA during dehydration in ethanol so that the chromatin. coli and Bacillus subtilis processed by CFS reveal additional features: the ribosomes are clearly visible and are not distributed equally throughout. water-miscible solvents. Techniques for staining cryosections with heavy metals are not yet available and image contrast is therefore too low to reveal fine detail. as shown by immunostaining (Bohrmann et al. which can in turn be substituted by the liquid resin. Bar. Nature Publishing Group / www. producing a gel that resists subsequent aggregation in organic.Bacterial Chromosome New Views of the Bacterial Chromatin Using Cryofixation and Freezesubstitution Electron microscopy of thin sections. but has been demonstrated to create physical crosslinks. at that time named the ‘nuclear vacuole’. Fortunately. the slices yielded are not as thin as those obtained from current embedding in plastic resins. by appearance as containing DNA. What was troubling to those involved in such studies was the strong variation of shape of the ‘nucleoid’. i. should have been able to provide the fine details of the bacterial chromosome that were lacking. if not all.els. which depended on the cytoplasmic fixatives used: with osmium tetroxide fixation it is rather strongly confined. achieved revolutionary progress that laid a basis for modern cell biology. even when they are at room temperature. The ice is thus progressively replaced by the solvent. When this is subsequently rendered 3 . a new immunostain was discovered which showed convincingly that most. The bacterial chromatin is in the ribosome-free spaces. At temperatures around 2 808C. This procedure of cryofixation and freeze-substitution (CFS) is limited to rather thin layers of material because the maximum depth of vitreous ice is only some 10–20-mm thick. ribosome-free spaces contained double-stranded DNA (Bohrmann et al. however. Thin-section techniques. In early studies these expectations were only partially fulfilled. Many ribosome-free spaces of variable size are apparent (Figure 2) that contain fine globular material. whereas after aldehyde fixation it comprises a group of many. Five of a series of 11 thin sections. The absence of a membrane around this vacuole was later confirmed for bacterial nucleoids in whatever form they were observed. much smaller ‘vacuoles’. which is amorphous. with a resolution estimated not to be below some 5 nm. Sections of E. appeared in the form of fine fibrils whose thickness was compatible with that expected of DNA. prepared by cryofixation and freeze-substitution (CFS) for the electron microscope. are shown.e. referred to previously.

By reconstructing a cell from these serial sections. From Bohrmann et al. frequently showing a ribosome-free central core. Canada. such as is needed for replication and transcription. with excrescences reaching far into the cytoplasm. there is an increased amount in the central region. They found negative supercoiling. (c) A light microscope phase contrast micrograph is shown. In this restrained form. Its physical structure and generation are still not understood. When a circular DNA molecule is supercoiled. depending upon whether it is under torsion or not. To a somewhat lesser degree. this form of the nucleoid. or by amino acid starvation of an amino acid-requiring strain.. so as to inhibit their DNA strands from opening. The very flexible stem and the twigs of Miller’s Christmas trees are distributed all over the cell within the ribosome-free spaces in such a manner that a maximum number of ribosomes can become involved in protein synthesis. this is possible only to a very limited degree with the plectonemic form. centrally located. They demonstrate how the apparent size of the ‘nucleoid’ is determined by optical parameters. The package of superimposed transcripted sections was then photographed by a low-resolution (pinhole) camera and printed (Figure 3).e. This experiment demonstrates that the ribosome-free spaces are not entirely randomly distributed within the cell. this is also true for the varying intensities of the fluorescent staining. applied to a thread. (1991) with permission. This typical spherical nucleoid is observed whatever the method of preparation/microscopy technique used. the nucleoid no longer appeared to be confined to a central location. phase contrast images vary exactly as do those of (b1) to (b4). The amount of this substance detected as being 4 bound is directly related to the degree of supercoiling. The low-resolution picture of the reconstituted cell looks exactly like some of the phase contrast light micrographs taken from a culture of the same strain. The problem with these new CSF findings was that. We will see further (below) that the DNA of thermophilic bacteria is. by autoradiography. a cell of E. Figure 3 Serial sections. The ribosome-free spaces of 11 serial sections were transferred to slightly coloured transparent foil and carefully cut out. It is still not known in which of the two ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd. will be relaxed when the thread is put into the form of a left-handed solenoid (Figure 4). or with the observation of whole cells by electron microscopy. on hard-grade paper.Bacterial Chromosome RNA polymerase must be associated with the metabolically active DNA. the chromatin is at rest. in light microscopy. of which five are shown in Figure 2. in cell sections. Pettijohn and Pfenniger (1980) have systematically applied this technique to cells of E. then the circle is reduced (collapsed) into an elongated plectonemic supercoil (Figure 4). corresponding to what is observed in the light microscope with live. 1975). cut longitudinally. Nature Publishing Group / www. coli. A sharp photographic image of this reconstructed cell is given in (a). to be outside the bulk of the nucleoid (Ryter and Chang. Indeed. According to a proposal of C.g. this would obviously counter the destabilizing effect of the high temperatures of their environment. positively supercoiled. coli is sectioned into about 15 consecutive serial sections. This is what we do when we fold our garden hose and is what happens when the DNA is wound around the protein cores of the eukaryotic chromatin forming nucleosomes. a torsional stress that facilitates opening of the double strands. Robinow. These central areas – the ‘bulk’ – are considered to represent those parts of the chromatin. Knowing that a good thin section is at the most 50-nm thick means also that. differ from each other only by the exposure time. shows differential binding of psoralen. the problem might be resolved. by treatment with sublethal doses of chloramphenicol. larger ribosome-free spaces had frequently been observed in near-equatorial sections. not subject to twisting forces. as was the case with osmium tetroxide fixation. which are not (at a given moment) involved in gene expression. According to the concentration of the surrounding refracting material. these prints. Even by more ‘old-fashioned’ ¨ methods (osmium tetroxide fixation). entire . after staining or by phase contrast. i. The Bacterial Chromatin is Supercoiled Double-stranded DNA. When the protein synthesis is inhibited. Left-hand torsion. in contrast. was described as ‘coralline’. e. or. with the ribosome-free spaces carefully cut out. the chromatin assembles into a near sphere. the site of RNA synthesis was found.els. superimposed to form a package that is a reconstruction of the whole cell. this was confirmed by immunolabelling (Durrenberger et al. University of Western Ontario. 1988). are schematically redrawn on coloured foils and. The out-of-focus pictures (b1) to (b4) are obtained with a pinhole camera. While the solenoid allows for a substantial shortening (‘compacting’) of a DNA thread.

only two groups achieved something approaching her work in quality. Probably stimulated by the pictures of Kavenoff. Topoisomerases I and II are of particular importance and were discovered first. Under these conditions it is strongly charged and neighbouring fibres repulse each other.23 for these and 0. Most of these loops were randomly bent and only few appeared in the form of plectonemic supercoils. frequently in combination with other histone-like proteins. A fibrous appearance. solenoidal compaction has been observed only with nucleosomes. Considerable efforts were developed to apply Laemmli’s biochemical and immunochemical procedures also on the Kavenoff-type of prokaryotic nucleoids. possibly in the form of loops. As yet. 1977). which showed some hundred loops emerging laterally from a sort of scaffold. ‘naked’ DNA shows neither the compacted form (b) nor (c). but only 3 in (a). Ruth Kavenoff once succeeded in producing very elegant electron micrographs of isolated bacterial nucleoids (reported in most general reviews on bacterial chromatin). can be readily accounted for as chemically induced relaxation of the supercoil. the intact scaffold remained behind. By normalizing the dimensions of the figure such that two windings of (c) correspond to those of a eukaryotic nucleosome. By immunolabelling. Nature Publishing Group / www. The compaction ratio of the length of the stretched DNA molecule to that of the supercoiled.25 and 0. In the absence of a sufficient amount of adequate basic proteins as partners.26 for (b) and (a) respectively. compacted form is about 9 in (b) and (c).Bacterial Chromosome Figure 4 Proposed compaction forms of DNA. low ionic concentrations are preferred for the electron microscopic studies of DNA. The whole arrangement showed a surprising resemblance to the model of the eukaryotic chromosome proposed by Laemmli: after dissolution of chromatin. obtained after chemical fixation. although much less convincing. having lost most of the supercoil of the loops and without succeeding in adding any biochemical and immunological identifications. whereas topoisomerase II (known as gyrase in bacteria) is able to break both. where the DNA is wound around a solid core of histones. an attractive model of the bacterial nucleoid is based on these findings and by analogy with the model of Laemmli: the loops are formed by a crosslinking by gyrase 5 ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd. Speculatively. forms the bacterial chromatin is supercoiled. In (c) it is in a solenoidal form. they demonstrated that the supercoiling of each individual segment is independently lost through the radiation-induced single-strand nicks produced in each segment (Lyderson and Pettijohn. Unfortunately. For technical reasons. Topoisomerase I is able to introduce torsion by opening only one strand of DNA. The same length of DNA is shown in the form of the loose (a) and compacted (b) plectonemic supercoiling. None was solenoidally coiled. the bending (curvature) is then 0. Topoisomerase II was demonstrated to be situated on the scaffold and to be involved in the attachment of the chromatin . topoisomerase I was localized to the same area as that of RNA polymerase. Both forms would lead to a rather microglobular appearance on high resolution electron micrographs if preserved as such. The loose plectonemic form and its derivatives have been and still are extensively studied by electron microscopy and sedimentation rates. The enzymes responsible for supercoiling are the topoisomerases. so as to produce the loose structure.els. Pettijohn and coworkers demonstrated the existence of independent chromosomal segments or domains. By irradiating the bacterial chromosome in vivo with gamma rays.

by immunocytochemistry. and therefore must be an HP-chromatin. a structural role for the histonelike proteins could only be inferred indirectly. 1992). on the nucleoid projections and not in the. Journal of Molecular Biology 6: 208–213. Portemer C. These distinctive differences between bacteria and archaea should stimulate the careful investigation of archaea with modern methods. mainly their relatively small size. By using permeabilized cells. Johansen J and Kellenberger E (1991) Coralline shape of the bacterial nucleoid after cryofixation. to our great surprise. This fragility is obviously the reason why they have never yet been isolated. 1997). is the strongest observation in favour of this putative model. Journal of Bacteriology 170: 4757–4768. Molecular Microbiology 26: 767–777. By immunocytochemistry. they exert functions that are metabolically very active. (2) the chromatin is resistant to aggregation during dehydration involved in the preparation for thin sections. The reverse gyrase of thermophilic bacteria generated interest in recent years (Bouthier de la Tour et al. Journal of Bacteriology 180: 274–281. i. in the native cell.. however. In overproducing conditions the cells lose viability. with a view to obtaining clearer ideas about our unicellular forebears. it is worth mentioning that. in particular of proteins. 1998). which. there is a tendency to assume that they have similar functions to those of the eukaryotic histones. For the stated reasons. a phenomenon which is in agreement with a beaded structure but there is no proof for it. exactly as demonstrated for the eukaryotic chromosome. they also modify the migration rate of small circular DNA during electrophoresis. in the H-NS excess situation. if they exist at all in bacteria. in vivo. that the relative amounts of these histone-like bacterial proteins are much too low to be able to organize all the chromatin of a cell into nucleosomes. Journal of Bacteriology 173: 3149–3158. must be highly fragile. as have the various helicases. Although the hypothesis of the loops has not yet been demonstrated. Bjornsti MA.. coli. Histones. ¨ some authors could introduce large amounts of HU into the cell and found. it is interesting to note that some repeat sequences in E. is correlated with other features that are distinct from those of the bacteria (Li et al. the ‘histone fold’.. that the bulk of chromatin also contained HU. Implicitly. this fold was not found in histone-like proteins of bacteria described . Bouthier de la Tour C. and the synthesis of macromolecules. Histone-like Proteins and Nucleosomes The name ‘histone-like’ was chosen because of the chemical properties shared with the eukaryotic histones. Uetz T. ´ Espeli O and Boccard F (1997) In vivo cleavage of Escherichia coli BIME2 repeats by DNA gyrase: genetic characterization of the target and identification of the cut site. in DNA-binding proteins of most of the archaea that have so far been carefully investigated. Cairns J (1963) The bacterial chromosome and its manner of replication as seen by autoradiography. but was present. coli (BIME-2) have strong ´ correlations with the binding and activity of gyrases (Espeli and Boccard. Although a negative result. quite distinct from the role of the histones of the eukaryotic nucleosomes in quiescence.. i. supposedly inert. H-NS. 1999): (1) nucleosomes are relatively stable and can be isolated. Durrenberger M. as a similar structure to that of the eukaryotes. Of interest is the additional observation that. The authors’ interpretation of these observations is that H-NS plays a decisive role in the confinement of the chromosome into the spherical shape. a chromatin rich in associated proteins. It is well known. is inhibited. chloramphenicol-induced nucleoid (mentioned above). leading to the same conclusions as discussed above for HU when present in excess. and thus not published. As far as is known from the still limited number of investigations. namely to cause the solenoidal coiling of DNA by forming its central solid core. something resembling the eukaryotic nucleosomes had been assembled in vitro with a large excess of the protein HU. Villiger W. together forming a scaffold. In the electron microscope. DNA-binding properties and their acid solubility. The other major histone-like protein of E. In a strain overproducing H-NS. For us this 6 observation confirmed that. by restraint of supercoiling to a comparable degree. basicity. was also found mostly on the border between the bulk of the nucleoid and the cytoplasm.Bacterial Chromosome and other proteins. When in vivo the histone-like proteins are bound to DNA.els. gyrase was not found to be enriched in the centre of the globular.e. spherical nucleoids appear. it was chiefly present in the bulk of the nucleoid (for references see Spurio et al. protein HU was found to be localized in the area of RNA synthesis. Hobot JA and Kellenberger E ¨ (1988) Intracellular localization of the histone-like protein HU in Escherichia coli. whereas the well-known DNA-binding property of HU is again validated. The presence of ‘real’ histones. References Bohrmann B. bulk (Durrenberger et al. the bulk of the DNA is not saturated with HU to form nucleosomes. as defined by the presence of this typical fold. Why then does direct inhibition of protein synthesis also lead to the same or similar form of nucleoid? Recent structural studies of eukaryotic histones by Xrays and nuclear magnetic resonance imaging led to the discovery and definition of a typical substructure. ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd. accounting for their alternative designation as compactosomes. 1988). by fluorescence microscopy. It is generally agreed that nucleosomes. Kaltoum H and Duguet M (1998) Reverse gyrase from the hyperthermophilic bacterium Thermotoga maritima: properties and gene structure. In common with the latter. Nature Publishing Group / www.e.

158–166.] Robinow CF and Kellenberger E (1994) The bacterial nucleoid 7 . Falconi A et al. Journal of Molecular Biology 98: 797–810. Microbiology 145: 1–2. Washington. [Best comprehensive book. London: Academic Press. (1992) Lethal over¨ production of the Escherichia coli nucleoid protein H-NS: ultramicroscopic and molecular autopsy. Further Reading Drlica K and Riley M (1990) The Bacterial Chromosome. [Comprehensive and short. Spurio R.] Gualerzi CO and Pon CL (1986) Bacterial Chromatin.Bacterial Chromosome Li J-Y. unfortunately some years old. Arnold-Schulz-Gahmen B and Kellenberger E (1999) Histones and histone-like DNA-binding proteins: correlations between structural differences. DC: ASM Press. Nanninga N (1998) Morphogenesis of Escherichia coli. Pettijohn DE (1996) The nucleoid. Lyderson K and Pettijohn DE (1977) Interactions stabilising DNA tertiary structure in the Escherichia coli chromosome investigated with ionising radiation. Berlin: Springer. Microbiological Reviews 58: 211–232. vol. Ryter A and Chang A (1975) Localization of transcribing genes in the bacterial cell by means of high resolution autoradiography. Nanninga N (1985) Molecular Cytology of Escherichia coli. Durrenberger M. recent references. Washington.] ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd. Pettijohn DE and Pfenniger O (1980) Supercoils in prokaryotic DNA restrained in vivo. Scientific American 228: 27–34. Nature Publishing Group / www. Chromosoma 62: 199–215. Microbiology and Molecular Biology Reviews 62: 110–129. pp. [Recommended for the more technical aspects. Proceedings of the National Academy of Sciences of the USA 77: 1331–1335. DC: ASM Press. properties and functions. In: Neidhardt FC (ed. Molecular and General Genetics 231: 201–211. 1. Miller OL (1973) The visualisation of genes in action.) Escherichia coli and Salmonella.els.

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