Rtude au microscope electronique de plasmas
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1 VOL. 29, 1965 STRUCTURE AND REPLICATION OF BACTERIAL NUCLEOIDS 293 deoxyribonucleic acid in Escherichia coli. Biochim. Biophys. Acta 34: MESELSON, M., AND F. W. STAHL The replication of DNA in Escherichia coli. Proc. Natl. Acad. Sci. U.S. 44: NAGATA, T The sequential replication of E. coli DNA. Cold Spring Harbor Symp. Quant. Biol. 28: PIEKARSKI, G Cytologische Untersuchungen an Paratyphus- und Colibakterien. Arch. Mikrobiol. 8: PIEKARSKI, G Haben Bakterien einen Zellkern? (Zur Definition des Zellkerns). Naturwissenschzften 37: POWELL, E Growth rate and generation time of bacteria, with special reference to continuous culture. J. Gen. Microbiol. 15: PREUSSER, H.-J Elektronenmikroskopische Untersuchungen uber die Cytologie von Proteus vulgaris. Arch. Mikrobiol. 29: PREUSSER, H.-J Form und Grbsse des Kernaquivalents von Escherichia coli in Abhangigkeit von den Kulturbedingungen. Arch. Mikrobiol. 33: Ris, H Ultrastructure and molecular organization of genetic systems. Can. J. Genet. Cytol. 3: ROBINOW, C. F The chromatin bodies of bacteria. Bacteriol. Rev. 20: ROBINOW, C. F Outline of the visible organization of bacteria, p In J. Brachet and A. E. Mirsky [ed.], The cell, vol. 4 pt. 1. Academic Press, Inc., New York. 35. RoBINOW, C. F Morphology of the bacterial nucleus. Brit. Med. Bull. 18: RYTER, A Etude au microscope 6lectronique des transformations nucleaires de E. coli K12S et K12S (X 26) apres irradiation aux rayons ultra-violets et au rayons X. J. Biophys. Biochem. Cytol. 8: RYTER, A., AND F. JACOB Etude au microscope electronique des relations entre mesosomes et noyaux chez Bac. subtilis. Compt. Rend. 257: DISCUSSION 38. RYTER, A., AND E. KELLENBERGER Rtude au microscope electronique de plasmas contenant de l'acide desoxyribonucleique. Z. Naturforsch. 13b: SCHAECHTER, M., M. W. BENTZON, AND 0. MAAL0E Synthesis of deoxyribonucleic acid during the division cycle of bacteria. Nature 183: SCHAECHTER, M., 0. MAAL0E, AND N. 0. KJELDGAARD Dependency on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. J. Gen. Microbiol. 19: SCHREIL, W Vergleichende Elektronenmikroskopie reiner DNS und der DNS des Bakteriennucleoids. Experientia 17: SCHREIL, W. H Studies on the fixation of artificial and bacterial DNA plasms for the electron microscopy of thin sections. J. Cell Biol. 22: SPEARING, J. K Cytological studies on the myxophyceae. Arch. Protistenk. 89: STANIER, R. Y La place des bact~ries dans le monde vivant. Ann. Inst. Pasteur 101: STANIER, R. Y., AND C. B. VAN NIEL The concept of a bacterium. Arch. Mikrobiol. 42: VAN ITERSON, W Membranes, particular organelles, and peripheral bodies in bacteria. Proc. Europ. Reg. Conf. Electron Microscopy, Delft 2: WHITFIELD, J. F., AND R. G. E. MURRAY The effects of the ionic environment on the chromatin structures of bacteria. Can. J. Microbiol. 2: a. YOUNG, I. E., AND P. C. FITZ-JAMES Pattern of synthesis of droxyribonucleic acid in Bacillus cereus growing synchronously out of spores. Nature 183: ZOBEL, C. R., AND M. BEER Electron stains. I. Chemical studies on the interaction of DNA with uranyl salts. J. Biophys. Biochem. Cytol. 10: PHILIP C. FITZ-JAMES Department of Bacteriology and Department of Biochemistry, University of Western Ontario, London, Canada In this discussion I shall continue from where Dr. Fuhs concluded and consider further the membrane or mesosomal attachment to the nuclear body. To begin with, I should like to disagree with Dr. Fuhs' closing comment, in that my work and that of other electron microscopists has suggested that mesosomes do play an active role in cell division. When membranous organelles or mesosomes were first observed by several workers in sections of Ryter-Kellenberger fixed bacilli, their arrangement immediately suggested not only a possible role in separating the consistently replicating deoxyribonucleic acid (DNA) but also an implication in transverse septum formation. This latter implication was present in the earlier work of
2 294 DISCUSSION BACTERIOL. REV. Chapman and Hillier (2), before the methods of preparation permitted a proper visualization of membrane structures. M-esosomes as genome separators. The possible function of the mesosomes as separators or anchor points of dividing nuclear bodies was briefly considered at a 1961 Gordon Conference. However, some proof of such a role has had to await the analysis of good serial sections. Recently, such sections of Bacillus subtilis were obtained by Ryter and Jacob (15), who outlined a model showing the possible function of the mesosome in maintaining the replicating DNA in two separate masses in the dividing cell. Likewise, arrangements of mesosomes apparently maintaining the separation of chromatin by attachment both to the forming and to the completed transverse septa have been established from serial sections of dividing cells of B. cereus and B. megaterium strains (Fitz-James, unpublished data). Continued membrane attachment of DNA can be found in thin sections after expulsion of the mesosome by osmotic shocking (14) and even in the protoplast state, as Dr. Fuhs has suggested today and Dr. Landman demonstrated at an earlier session of this Annual Meeting. While discussing the finding of such structural DNA-membrane associations, I should here make reference to the work of Jacob, Brenner, and Cuzin (11), who presented a model system showing how the replication of DNA could be triggered at a point of membrane contact and suggesting also that DNA replication could be coordinated by septation at the site of membrane attachment. Since the mesosomes can either be attached by their surface to, or even heavily embedded in, the nuclear DNA fibrils, and are also connected in a dividing Bacillus cell to a future growing or completed septal position, they are ideally located to perform a coordinating role both for DNA synthesis and septation. Let us consider then a few of the situations wherein mesosomes undergo, or can be made to assume, rearrangements or alterations and see how these alterations influence the possible role of the mesosome as organizer of nuclear division and of septation. Mesosomes and penicillin. The action of penicillin on cells of B. megaterium growing in peptone-sucrose medium and already adjusted to such medium was found to destroy the normal mesosomal structure within 60 min (Fitz-James and Hancock, in preparation). The initial lesion, however, does not involve the mesosomes at all, but rather the growing transverse septum. Indeed, the relationship of normal membrane to transverse septum is lost, and is replaced (as early as 5 min after penicillin addition) by a ring vacuole filled with fibrous material. However, the mesosomes, even when closely approximated to these penicillin-induced lesions, are still structurally intact (Fig. 1). It is not until 40 to 60 min of drug exposure, at which time the cell wall is obviously failing to contain the protoplast, that mesosomes, as intact structures, are disarranged and their contents lost to the wall-membrane interspace. A similar mesosomal loss occurs on osmotic shocking and lysozyme digestion (6). Even then, however, some membrane attachments to the DNA are still found (Fig. 2). With the mesosomal loss, a more scattered array of chromatin is found in thin sections. After 2 hr in this system, some 50 % of the cells exist as free protoplasts. In spite of the structural alterations, no change in rate of formation or total cell content of ribonucleic acid (RNA), DNA, or lipid phosphorus was encountered. Mesosomes and spore formation. A second system worth considering in regard to membranechromatin associations is that of spore formation. Here, mesosomes appear to be active both in a DNA-attached role and in one in which DNA or nuclear fibrils are not involved. Thus, with serial sections, mesosomes can invariably be found anchoring the ends and middle parts of the axial filament of chromatin (a stage peculiar to early spore formation) to the adjacent plasma membrane. These otherwise fleeting formations are FIG. 1. Thin section of Bacillus megaterium after 20 min of aeration in dimethoxyphenyl penicillin (1 mg/ml) in sucrose-peptone medium. The displacement of the membrane from the transverse septum by accumulated fibrous material (arrow) has not altered the internal structure of the mesosome (M) or its association with chromatin. X 77,000. FIG. 2. Bacillus megaterium after 2 hr of exposure to dimethoxyphenyl penicillin. The rods have become bulbous; the wall is giving away, the accumulation of fibrous material is marked (arrow). In the right cell the mesosome has unfolded into a wall-membrane vacuole; in the left cell a chromatinmesosome link persists (C-M). X 53,000. FIG. 3. Section of a Bacillus cereus mutant unable to proceed beyond the "axial filament" stage of sporulation. Serial sections show all mesosomes extended from chromatin to peripheral membrane. X 56,000. FIG. 4. Mesosome attachment of the nonspore piece of chromatin at the cell end away from the spore in Bacillus cereus var. medusa. Penicillin has been used to block cortex formation of the spore, but in these nongrowing cells has no other apparent effects. X 53,000.
3 VOL. 29, 1965 DISCUSSION 295 # K A- FIGS. 1-4
4 296 DISCUSSION more easily studied in sections of asporogenous mutants (7) blocked beyond the axial filament stage (Fig. 3). Subsequently, during the separation of part of the chromatin into the forespore, a mesosome appears to guide, or at least to accompany, the DNA fibrils into the future spore (5). In contrast, perisporal mesosomes can be readily demonstrated during formation of forespore, cortex, and coat (6), which have no obvious link to DNA. Now what about the DNA moiety not taken into the spore? It, again, is often seen to be well anchored by a mesosome organelle to the opposite end of the cell (Fig. 4), where, for the subsequent hours of sporulation, it remains normal in appearance until caught up in the decay of terminal lysis. Mesosomes and synchronization. Finally, a study of the synchronization of cells should offer some valuable leads to the possible significance of membrane-dna associations. The natural synchrony achieved when resting spores are rapidly germinated has been the subject of a thin-section analysis (Fitz-James, unpublished data). During the first 15 min of germination, mesosomes are not prominent. Thus, in spite of the obvious inclusion of such organelles in the forming spore, their de novo development may be a characteristic of germination, a matter for further study. After 30 min of germination, at which time DNA replication is well under way (4), the mesosome is prominent, usually peripheral, and often chromatin-associated. After 40 to 60 min, when separation of the duplicating chromatin is occuring, mesosomes embedded in the nucleoid are a more frequent finding, as are also direct links of nuclear fibrils to the peripheral membrane or to stubby peripheral mesosomes. By 90 min, the mesosomes again become more prominent at the cell periphery and, while maintaining an apical attachment to the chromatin, are found, by 120 min, at the sites of the first transverse septum in the now-escaping cell. Synchronization via temperature shifts. Artificial methods of producing synchronous division are also proving useful in the analysis of mesosomal structure. The procedure of Hunter-Szybalska et al. (10, see also 13), as modified from the original observation of Hotchkiss (9), has been applied here to B. megaterium. After chilling ac- BACTERIOL. REV. tively growing cells at 15 C for 30 min, one can expect a synchronous burst of division some 40 min after aeration at 34 C. Superficially, it would appear that the synchrony depends on the recovery of a disarranged mesosome to a normal, transverse septal prominent stage (Fitz-James, in preparation). The rapid chilling has a marked effect on the mesosome structure, depending on the stage of division when chilling is applied. Those mesosomes associated with developing transverse septa in dividing cells are displaced to the periphery, their contents spreading in the wall-membrane space. Their connection to nuclear fibrils is not prominent (Fig. 5). In shorter cells which have completed division, chilling appears to cause the mesosome to become well embedded in DNA fibrils and to show marked vacuolization (Fig. 6). In chilled cells, this mesosomal alteration can be associated with a condensed nuclear body when examined in stained smears (10). Just before warming the culture after 30 min of chilling, the disarrangement of the mesosome is still extreme. However, 10 min after warming and aeration at 34 C, a remarkable recovery of the mesosome structure is encountered, regardless of the original chilled state of the organelle (Fig. 7). This recovery phase was found to be accompanied by a rapid rise in DNA and lipid phosphorus, but a less-marked increase in RNA. After 30 min at 34 C, the mesosomes are oganized in the now longer cells at the sites of future divisions, which, by 40 min, are beginning in nearly all cells (Fig. 8) and are complete by 50 min. However, prolonged aeration at 15 C will also permit slow recovery of the mesosomes so that, after 90 min at this temperature, a remarkably large mesosome is now encountered in a short undivided cell relatively rich in lipid phosphorus and low in DNA. In their studies of RNA, DNA, and protein of chilled cells, Falcone and Szybalski (3) were unable to relate any particular chemical event with the highest induction of synchrony. A study of total lipid phosphorus, presumably a major component of membrane systems, has, in these studies, lent some chemical support to the structural changes encountered. Since penicillin has little early effect on the structure of the mesosome and since there is FIG Thin sections of Bacillus megaterium cells aerated in peptone-water and undergoing temperature shifts to achieve synchronous division. (Fig. 5) Mesosome displacement seen after rapid chilling of still dividing cells from 34 to 15 C and aeration for 10 min. X 64,000. (Fig. 6) Internal disorganization of mesosomes of completely divided cells after chilling and aeration at 16 C for 10 min. X 63,700. (Fig. 7) All cells from the same culture as that shown in Fig. 6 contained an extensive and wellorganized mesosome, as shown here, after rapid warming to 34 C and aeration for 10 min. X 53,000. (Fig. 8) After 40 min of aeration at 34 C (after 30 min at 15 C), all cells begin division and possess mesosomes in their characteristic location at the transverse septa. Parts of mesosomes surrounded by chromatin have been sectioned. X 53,000.
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6 298 DISCUSSION BACTERIOL. REV. marked disarray of the forming wall, one might conclude that these organelles do not function in the penicillin-sensitive mechanism of wall formation. Yet mesosomes are prominent at the site of septation in the first division of the germinated spore. Again, their structural recovery and participation in transverse septum formation coincides with the division of Bacillus cells induced to synchrony by temperature shifts. It will be interesting to see if future work reveals that the temperature shift synchrony in other mesosomebearing organisms produces such an alteration in mesosomal organization. Such a result would then implicate these organelles, not only as regulators of balanced growth but also as active participants in the susceptibility to transforming DNA, as observed in synchronized pneumococci (9). The structural evidence reviewed in this discussion suggests only that mesosomes may function as regulatory organelles responsible for the orderly formation of division septa. Throughout division, continuously replicating chromatin in a balanced cell can be continuously separated through its attachment, via the mesosome, to the continuously expanding membrane-wall exoskeleton. Proof of contractile and migratory abilities on the part of the mesosome would make regulatory models of mesosome function even more attractive, but such a proof is not available from studies of fixed material. In reply to Dr. Fuhs' argument that no special apparatus or structure can be demonstrated at the mesosome-chromatin junction in current thin sections, one need only to be reminded of the remarkable revelation of membrane-attached macromolecules by phosphotungstate-negative staining by Abrams (1) and hope that such a method might, in the future, satisfy Dr. Fuhs' doubts. LITERATURE CITED 1. ABRAM, D Fine structures of bacterial cell membranes. Bacteriol. Proc., p CHAPMAN, G. B., AND J. HILLIER Electron microscopy of ultra-thin sections of bacteria. I. Cellular division in Bacillus cereus. J. Bacteriol. 66: FALCONE, G., AND W. SZYBALSKI Biochemical studies on the induction of synchronized cell division. Exptl. Cell Res. 11: FITZ-JAMES, P. C The phosphorus fractions of Bacillus cereus and Bacillus megaterium. II. A correlation of the chemical with the cytological changes occurring during spore germination. Can. J. Microbiol. 1: FITz-JAMEs, P Participation of the cytoplasmic membrane in the growth and spore formation of bacilli. J. Biophys. Biochem. Cytol. 8: FITZ-JAMES, P Fate of the mesosomes of Bacillus megaterium during protoplasting. J. Bacteriol. 87: FITz-JAMEs, P Spore formation in wild and mutant strains of B. cereus and some effects of inhibitors. In International CNRS symposium on mechanisms of regulation in microorganisms, Marseilles, July Editions du CNRS, Paris. 8. FUHS, G. W Symposium on the fine structure and replication of bacteria and their parts. I. Fine structure and replication of bacterial nucleoids. Bacteriol. Rev. 29: HOTCHKISS, R. D Cyclical behavior in pneumococcal growth and transformability occasioned by environmental changes. Proc. Natl. Acad. Sci. U.S. 40: HUNTER-SZYBALSKA, M. E., W. SZYBALSKI, AND E. D. DELAMATER Temperature synchronization of nuclear and cellular division in Bacillus megaterium. J. Bacteriol. 71: JACOB, F., S. BRENNER, AND F. CUZIN On the regulation of DNA replication in bacteria. Cold Spring Harbor Symp. Quant. Biol. 28: LANDMAN, 0. E., A. RYTER, AND R. E. KNOTT On the chemical and physical basis of stability of L forms. Bacteriol. Proc., p MAAL0E, Synchronous growth, p In I. C. Gunsalus and R. Y. Stanier [ed.], The bacteria, vol. 4. Academic Press, Inc., New York. 14. RYTER, A Discussion in regulation of spore formation. In International CNRS symposium on mechanisms of regulation of cellular activities in microorganisms, Marseilles, July Gordon and Breach, New York. 15. RYTER, A., AND F. JACOB Etude au microscope electronique des relations entre mesosomes et noyaux chez Bacillus subtilis. Compt. Rend. 257:
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