Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Alternatives to binary fission in bacteria

Nature Reviews Microbiology volume 3, pages 214–224 (2005)Cite this article

Abstract

Whereas most prokaryotes rely on binary fission for propagation, many species use alternative mechanisms, which include multiple offspring formation and budding, to reproduce. In some bacterial species, these eccentric reproductive strategies are essential for propagation, whereas in others the programmes are used conditionally. Although there are tantalizing images and morphological descriptions of these atypical developmental processes, none of these reproductive structures are characterized at the molecular genetic level. Now, with newly available analytical techniques, model systems to study these alternative reproductive programmes are being developed.

Key Points

  • Although binary fission is conceptually simple, complex genetic mechanisms enhance the fidelity of cell division. Based on comparisons of model organisms, there is remarkable flexibility in the evolution of genes that govern this essential process in the Bacteria.

  • Alternative reproductive modes are found in diverse lineages in the Bacteria. These include modified programmes based on endospore formation, multiple fission of an enlarged or filamentous cell and budding. This review discusses selected lineages that could serve as new models for studying the mechanisms that mediate these unusual reproductive strategies. A phylogenetic perspective is emphasized because model systems can serve as a foundation on which to build hypotheses to study these alternative systems of reproduction and development.

  • Some low-GC Gram-positive bacteria, such as Metabacterium polyspora, the segmented filamentous bacteria and Epulopiscium spp. have apparently converted a programme of endospore formation into a mode of propagation in which multiple intracellular offspring are produced.

  • The pleurocapsalean cyanobacteria, such as Stanieria, Myxosarcina, Pleurocapsa and Dermocarpella, use multiple fission of an enlarged cell to produce baeocyte offspring.

  • To enhance dispersal of offspring, members of the Actinobacteria produce spores on aerial structures. In the case of streptomycetes, terminal cells of the aerial mycelium divide synchronously to produce the uninucleoid cells which become spores. Other Actinobacteria, such as Actinoplanes and Pilimelia, produce complex sporangia in the absence of aerial mycelium formation.

  • The life cycle of the predatory δ-proteobacterium Bdellovibrio has distinct stages of growth, multiple fission and differentiation to motile attack-phase cells.

  • A morphologically diverse group of prosthecate α-proteobacteria, including Hyphomonas, Pedomicrobium and Ancalomicrobium, reproduce by budding mechanisms.

  • Some Planctomycetes also reproduce by budding; currently nothing is known about cell division or reproduction in this bacterial lineage.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Life cycles of Bacillus subtilis.
Figure 2: Evolutionary relationships of model organisms and bacteria that show unusual reproductive strategies.
Figure 3: Formation of multiple dormant offspring in Metabacterium polyspora.
Figure 4: Intracellular offspring of the segmented filamentous bacteria.
Figure 5: Viviparity in Epulopiscium.
Figure 6: Streptomyces coelicolor life cycle.

Similar content being viewed by others

References

  1. Lutkenhaus, J. Unexpected twist to the Z ring. Dev. Cell 2, 519–521 (2002).

    Article  CAS  PubMed  Google Scholar 

  2. Donachie, W. D. Co-ordinate regulation of the Escherichia coli cell cycle or the cloud of unknowing. Mol. Microbiol. 40, 779–785 (2001).

    Article  CAS  PubMed  Google Scholar 

  3. Harry, E. J. Bacterial cell division: regulating Z-ring formation. Mol. Microbiol. 40, 795–803 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Margolin, W. Spatial regulation of cytokinesis in bacteria. Curr. Opin. Microbiol. 4, 647–652 (2001).

    Article  CAS  PubMed  Google Scholar 

  5. Jensen, R. B., Wang, S. C. & Shapiro, L. Dynamic localization of proteins and DNA during a bacterial cell cycle. Nature Rev. Mol. Cell Biol. 3, 167–176 (2002).

    Article  CAS  Google Scholar 

  6. Errington, J., Daniel, R. A. & Scheffers, D. J. Cytokinesis in bacteria. Microbiol. Mol. Biol. Rev. 67, 52–65 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Sherratt, D. J. Bacterial chromosome dynamics. Science 301, 780–785 (2003).

    Article  CAS  PubMed  Google Scholar 

  8. Ryan, K. R. & Shapiro, L. Temporal and spatial regulation in prokaryotic cell cycle progression and development. Annu. Rev. Biochem. 72, 367–394 (2003).

    Article  CAS  PubMed  Google Scholar 

  9. Skerker, J. M. & Laub, M. T. Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nature Rev. Microbiol. 2, 325–337 (2004).

    Article  CAS  Google Scholar 

  10. Stephens, C. Prokaryotic development: a new player on the cell cycle circuit. Curr. Biol. 14, R505–R507 (2004).

    Article  CAS  PubMed  Google Scholar 

  11. Wu, L. J. Structure and segregation of the bacterial nucleoid. Curr. Opin. Genet. Dev. 14, 126–132 (2004).

    Article  CAS  PubMed  Google Scholar 

  12. Viollier, P. H. et al. Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc. Natl Acad. Sci. USA 101, 9257–9262 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Wu, L. J. & Errington, J. Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117, 915–925 (2004).

    Article  CAS  PubMed  Google Scholar 

  14. Gerdes, K., Moller-Jensen, J., Ebersbach, G., Kruse, T. & Nordstrom, K. Bacterial mitotic machineries. Cell 116, 359–366 (2004).

    Article  CAS  PubMed  Google Scholar 

  15. Lowe, J. & Amos, L. A. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391, 203–206 (1998).

    Article  CAS  PubMed  Google Scholar 

  16. Wang, X. & Lutkenhaus, J. The FtsZ protein of Bacillus subtilis is localized at the division site and has GTPase activity that is dependent upon FtsZ concentration. Mol. Microbiol. 9, 435–442 (1993).

    Article  CAS  PubMed  Google Scholar 

  17. Iyer, L. M., Makarova, K. S., Koonin, E. V. & Aravind, L. Comparative genomics of the FtsK–HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res. 32, 5260–5279 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Romberg, L. & Levin, P. A. Assembly dynamics of the bacterial cell division protein FtsZ: poised at the edge of stability. Annu. Rev. Microbiol. 57, 125–154 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Margolin, W. Catching some Zs: a new protein for spatial regulation of bacterial cytokinesis. Cell 117, 850–851 (2004).

    Article  CAS  PubMed  Google Scholar 

  20. Crowley, D. J. & Courcelle, J. Answering the call: coping with DNA damage at the most inopportune time. J. Biomed. Biotechnol. 2, 66–74 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Kawai, Y., Moriya, S. & Ogasawara, N. Identification of a protein, YneA, responsible for cell division suppression during the SOS response in Bacillus subtilis. Mol. Microbiol. 47, 1113–1122 (2003).

    Article  CAS  PubMed  Google Scholar 

  22. Raskin, D. M. & de Boer, P. A. MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J. Bacteriol. 181, 6419–6424 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Marston, A. L., Thomaides, H. B., Edwards, D. H., Sharpe, M. E. & Errington, J. Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Dev. 12, 3419–3430 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Nierman, W. C. et al. Complete genome sequence of Caulobacter crescentus. Proc. Natl Acad. Sci. USA 98, 4136–4141 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Rothfield, L., Justice, S. & Garcia-Lara, J. Bacterial cell division. Annu. Rev. Genet. 33, 423–448 (1999).

    Article  CAS  PubMed  Google Scholar 

  26. Margolin, W. Themes and variations in prokaryotic cell division. FEMS Microbiol. Rev. 24, 531–548 (2000).

    Article  CAS  PubMed  Google Scholar 

  27. Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y. & Hattori, M. The KEGG resource for deciphering the genome. Nucleic Acids Res. 32, D277–D280 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Andrews, P. D., Harper, I. S. & Swedlow, J. R. To 5D and beyond: quantitative fluorescence microscopy in the postgenomic era. Traffic 3, 29–36 (2002).

    Article  PubMed  Google Scholar 

  29. Ostrowski, S. G., Van Bell, C. T., Winograd, N. & Ewing, A. G. Mass spectrometric imaging of highly curved membranes during Tetrahymena mating. Science 305, 71–73 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Gisselson, L. A., Graneli, E. & Pallon, J. Variation in cellular nutrient status within a population of Dinophysis norvegica (Dinophyceae) growing in situ: single-cell elemental analysis by use of nuclear microprobe. Limnol. Oceanogr. 46, 1237–1242 (2001).

    Article  Google Scholar 

  31. Grossman, A. D. Integration of developmental signals and the initiation of sporulation in B. subtilis. Cell 65, 5–8 (1991).

    Article  CAS  PubMed  Google Scholar 

  32. Eichenberger, P. et al. The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis. PLoS Biol. 2, E328 (2004).

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  33. Stragier, P. in Bacillus subtilis and Its Closest Relatives (eds Sonenshein, A. L., Hoch, J. A. & Losick, R.) 519–526 (ASM Press, Washington DC, 2002).

    Book  Google Scholar 

  34. Errington, J. Regulation of endospore formation in Bacillus subtilis. Nature Rev. Microbiol. 1, 117–126 (2003).

    Article  CAS  Google Scholar 

  35. Hilbert, D. W. & Piggot, P. J. Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiol. Mol. Biol. Rev. 68, 234–262 (2004). This current review outlines recent advances in our understanding of endospore formation and provides an exceptional historical insight into the field.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Stragier, P. & Losick, R. Molecular genetics of sporulation in Bacillus subtilis. Annu. Rev. Genet. 30, 297–241 (1996).

    Article  CAS  PubMed  Google Scholar 

  37. Bath, J., Wu, L. J., Errington, J. & Wang, J. C. Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell–prespore division septum. Science 290, 995–997 (2000).

    Article  CAS  PubMed  Google Scholar 

  38. Levin, P. A. & Losick, R. Transcription factor Spo0A switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis. Genes Dev. 10, 478–488 (1996).

    Article  CAS  PubMed  Google Scholar 

  39. Ryter, A. Etude morphologique de la sporulation de Bacillus subtilis. Ann. Inst. Pasteur (Paris) 108, 40–60 (1965).

    CAS  Google Scholar 

  40. Ben-Yehuda, S., Rudner, D. Z. & Losick, R. RacA, A bacterial protein that anchors chromosomes to the poles. Science 299, 532–536 (2003).

    Article  CAS  PubMed  Google Scholar 

  41. Nicholson, W. L., Munakata, N., Horneck, G., Melosh, H. J. & Setlow, P. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64, 548–572 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Chatton, É. & Pérard, C. Schizophytes du caecum du cobaye. II Metabacterium polyspora n. g., n. s. C. R. Hebd. Soc. Biol. (Paris) 74, 1232–1234 (1913).

    Google Scholar 

  43. Robinow, C. F. Kurzer hinweis auf Metabacterium polyspora. Z. Tropenmed. Parasitol. 8, 225–227 (1957).

    CAS  PubMed  Google Scholar 

  44. Kunstyr, I., Schiel, R., Kaup, F. J., Uhr, G. & Kirchhoff, H. Giant gram-negative noncultivable endospore-forming bacteria in rodent intestines. Naturwissenschaften 75, 525–527 (1988).

    Article  CAS  PubMed  Google Scholar 

  45. Angert, E. R. & Losick, R. M. Propagation by sporulation in the guinea pig symbiont Metabacterium polyspora. Proc. Natl Acad. Sci. USA 95, 10218–10223 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Duda, V. I., Labedinsky, A. V., Mushegjan, M. S. & Mitjushina, L. L. A new anaerobic bacterium, forming up to five endospores per cell - Anaerobacter polyendosporus gen. et spec. nov. Arch. Microbiol. 148, 121–127 (1987).

    Article  CAS  Google Scholar 

  47. Siunov, A. V. et al. Phylogenetic status of Anaerobacter polyendosporus, an anaerobic, polysporogenic bacterium. Int. J. Syst. Bacteriol. 49, 1119–1124 (1999).

    Article  CAS  PubMed  Google Scholar 

  48. Klaasen, H. L. et al. Intestinal, segmented, filamentous bacteria in a wide range of vertebrate species. Lab. Anim. 27, 141–150 (1993).

    Article  CAS  PubMed  Google Scholar 

  49. Davis, C. P. & Savage, D. C. Habitat, succession, attachment, and morphology of segmented, filamentous microbes indigenous to the murine gastrointestinal tract. Infect. Immun. 10, 948–956 (1974).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Erlandsen, S. L. & Chase, D. G. Morphological alterations in the microvillous border of villous epithelial cells produced by intestinal microorganisms. Am. J. Clin. Nutr. 27, 1277–1286 (1974).

    Article  CAS  PubMed  Google Scholar 

  51. Klaasen, H. L., Koopman, J. P., Poelma, F. G. & Beynen, A. C. Intestinal, segmented, filamentous bacteria. FEMS Microbiol. Rev. 8, 165–180 (1992).

    Article  CAS  PubMed  Google Scholar 

  52. Chase, D. G. & Erlandsen, S. L. Evidence for a complex life cycle and endospore formation in the attached, filamentous, segmented bacterium from murine ileum. J. Bacteriol. 127, 572–583 (1976).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Ferguson, D. J. & Birch-Andersen, A. Electron microscopy of a filamentous, segmented bacterium attached to the small intestine of mice from a laboratory animal colony in Denmark. Acta Pathol. Microbiol. Scand. 87, 247–252 (1979). This is a compelling account of the murine SFB life cycle.

    CAS  Google Scholar 

  54. Umesaki, Y., Okada, Y., Imaoka, A., Setoyama, H. & Matsumoto, S. Interactions between epithelial cells and bacteria, normal and pathogenic. Science 276, 964–965 (1997).

    Article  CAS  PubMed  Google Scholar 

  55. Klaasen, H. L. et al. Apathogenic, intestinal, segmented, filamentous bacteria stimulate the mucosal immune system of mice. Infect. Immun. 61, 303–306 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Fishelson, L., Montgomery, W. L. & Myrberg, A. A. A unique symbiosis in the gut of a tropical herbivorous surgeonfish (Acanthuridae: Teleostei) from the Red Sea. Science 229, 49–51 (1985).

    Article  Google Scholar 

  57. Clements, K. D., Sutton, D. C. & Choat, J. H. Occurrence and characteristics of unusual protistan symbionts from surgeonfishes Ancanthuridae of the Great Barrier Reef Australia. Marine Biol. 102, 403–412 (1989).

    Article  Google Scholar 

  58. Montgomery, W. L. & Pollak, P. E. Epulopiscium fishelsoni n. g., n. s., a protist of uncertain taxonomic affinities from the gut of an herbivorous reef fish. J. Protozool. 35, 565–569 (1988).

    Article  Google Scholar 

  59. Angert, E. R., Clements, K. D. & Pace, N. R. The largest bacterium. Nature 362, 239–241 (1993).

    Article  CAS  PubMed  Google Scholar 

  60. Angert, E. R., Brooks, A. E. & Pace, N. R. Phylogenetic analysis of Metabacterium polyspora: clues to the evolutionary origin of daughter cell production in Epulopiscium species, the largest bacteria. J. Bacteriol. 178, 1451–1456 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Angert, E. R. & Clements, K. D. Initiation of intracellular offspring in Epulopiscium. Mol. Microbiol. 51, 827–835 (2004). With reference 45, demonstrates the power of fluorescence microscopy in describing developmental processes in bacteria that cannot be cultured in the laboratory.

    Article  CAS  PubMed  Google Scholar 

  62. Kunst, F. et al. The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390, 249–256 (1997).

    Article  CAS  PubMed  Google Scholar 

  63. Onyenwoke, R. U., Brill, J. A., Farahi, K. & Wiegel, J. Sporulation genes in members of the low G+C Gram-type-positive phylogenetic branch (Firmicutes). Arch. Microbiol. 182, 182–192 (2004).

    Article  CAS  PubMed  Google Scholar 

  64. Waterbury, J. B. & Stanier, R. Y. Patterns of growth and development in pleurocapsalean cyanobacteria. Microbiol. Rev. 42, 2–44 (1978). This outstanding, lucid monograph describes the developmental patterns of 32 strains of cyanobacteria based on stunning electron micrographs and time-lapse, light microscopy of growing cells.

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Mazouni, K., Domain, F., Cassier-Chauvat, C. & Chauvat, F. Molecular analysis of the key cytokinetic components of cyanobacteria: FtsZ, ZipN and MinCDE. Mol. Microbiol. 52, 1145–1158 (2004).

    Article  CAS  PubMed  Google Scholar 

  66. The Development of Drosophila melanogaster (eds. Bate, M. & Arias, A. M.) (Cold Spring Harbor Laboratory Press, New York, 1993).

  67. Chater, K. F. & Hopwood, D. A. in Microbial Differentiation (eds Ashworth, J. M. & Smith, J. E.) 143–160 (Cambridge University Press, Cambridge, 1973).

    Google Scholar 

  68. Chater, K. F. Genetics of differentiation in Streptomyces. Annu. Rev. Microbiol. 47, 685–713 (1993).

    Article  CAS  PubMed  Google Scholar 

  69. Chater, K. F. & Horinouchi, S. Signalling early developmental events in two highly diverged Streptomyces species. Mol. Microbiol. 48, 9–15 (2003).

    Article  CAS  PubMed  Google Scholar 

  70. Flardh, K. Growth polarity and cell division in Streptomyces. Curr. Opin. Microbiol. 6, 564–571 (2003). A cell biological view of recent advances in understanding hyphal growth and spore development in Streptomyces.

    Article  CAS  PubMed  Google Scholar 

  71. Gehring, A. M., Nodwell, J. R., Beverley, S. M. & Losick, R. Genomewide insertional mutagenesis in Streptomyces coelicolor reveals additional genes involved in morphological differentiation. Proc. Natl Acad. Sci. USA 97, 9642–9647 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Ikeda, H. et al. Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nature Biotechnol. 21, 526–531 (2003).

    Article  Google Scholar 

  73. Bentley, S. D. et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141–147 (2002).

    Article  PubMed  Google Scholar 

  74. McCormick, J. R., Su, E. P., Driks, A. & Losick, R. Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol. Microbiol. 14, 243–254 (1994).

    Article  CAS  PubMed  Google Scholar 

  75. Lechevalier, M. P. in Bergey's Manual of Systematic Bacteriology (eds Williams, S. T., Sharpe, M. E. & Holt, J. G.) 2405–2417 (Williams and Wilkins, Baltimore, 1989).

    Google Scholar 

  76. Vobis, G. in Bergey's Manual of Systematic Bacteriology (eds Williams, S. T., Sharpe, M. E. & Holt, J. G.) 2418–2450 (Williams and Wilkins, Baltimore, 1989).

    Google Scholar 

  77. Vobis, G. in The Prokaryotes (eds Balows, A., Truper, H. G., Dworkin, M., Harder, W. & Schleifer, K. H.) 1029–1060 (Springer, New York, 1992).

    Google Scholar 

  78. Parenti, F. & Coronelli, C. Members of the genus Actinoplanes and their antibiotics. Annu. Rev. Microbiol. 33, 389–411 (1979).

    Article  CAS  PubMed  Google Scholar 

  79. Lazzarini, A., Cavaletti, L., Toppo, G. & Marinelli, F. Rare genera of actinomycetes as potential producers of new antibiotics. Antonie Van Leeuwenhoek 78, 399–405 (2000).

    Article  CAS  PubMed  Google Scholar 

  80. Lechevalier, H. & Holbert, P. E. Electron microscopic observation of the sporangial structure of a strain of Actinoplanes. J. Bacteriol. 89, 217–222 (1965).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Lechevalier, H. A., Lechevalier, M. P. & Holbert, P. E. Electron microscopic observation of the sporangial structure of strains of Actinoplanaceae. J. Bacteriol. 92, 1228–1235 (1966). Together with reference 80, this paper provides a detailed ultrastructure-based description of sporangial development in Micromonosporaceae with comparisons to streptomycete spore development.

    CAS  PubMed  PubMed Central  Google Scholar 

  82. Stolp, H. & Starr, M. P. Bdellovibrio bacteriovorus gen. et sp. n., a predatory, ectoparasitic, and bacteriolytic microorganism. Antonie Van Leeuwenhoek 29, 217–248 (1963).

    Article  CAS  PubMed  Google Scholar 

  83. Starr, M. P. & Baigent, N. L. Parasitic interaction of Bdellovibrio bacteriovorus with other bacteria. J. Bacteriol. 91, 2006–2017 (1966).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Diedrich, D. L., Denny, C. F., Hashimoto, T. & Conti, S. F. Facultatively parasitic strain of Bdellovibrio bacteriovorus. J. Bacteriol. 101, 989–996 (1970).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Burnham, J. C., Hashimoto, T. & Conti, S. F. Ultrastructure and cell division of a facultatively parasitic strain of Bdellovibrio bacteriovorus. J. Bacteriol. 101, 997–1004 (1970).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Rendulic, S. et al. A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 303, 689–692 (2004).

    Article  CAS  PubMed  Google Scholar 

  87. Cotter, T. W. & Thomashow, M. F. A conjugation procedure for Bdellovibrio bacteriovorus and its use to identify DNA sequences that enhance the plaque-forming ability of a spontaneous host-independent mutant. J. Bacteriol. 174, 6011–6017 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Ajithkumar, V. P. et al. A novel filamentous Bacillus sp., strain NAF001, forming endospores and budding cells. Microbiol. 147, 1415–1423 (2001).

    Article  CAS  Google Scholar 

  89. Waterbury, J. & Stanier, R. Two unicellular cyanobacteria which reproduce by budding. Arch. Microbiol. 115, 249–257 (1977).

    Article  CAS  Google Scholar 

  90. Staley, J. T. & Fuerst, J. A. in Bergey's Manual of Systematic Bacteriology (eds Staley, J. T., Bryant, M. P., Pfennig, N. & Holt, J. G.) 1890–1993 (Williams and Wilkins, Baltimore 1989).

    Google Scholar 

  91. McDonald, I. R. et al. A review of bacterial methyl halide degradation: biochemistry, genetics and molecular ecology. Environ. Microbiol. 4, 193–203 (2002).

    Article  CAS  PubMed  Google Scholar 

  92. Moore, R. L. The biology of Hyphomicrobium and other prosthecate, budding bacteria. Ann. Rev. Microbiol. 35, 567–594 (1981).

    Article  CAS  Google Scholar 

  93. Ausmees, N. & Jacobs-Wagner, C. Spatial and temporal control of differentiation and cell cycle progression in Caulobacter crescentus. Annu. Rev. Microbiol. 57, 225–247 (2003).

    Article  CAS  PubMed  Google Scholar 

  94. Quardokus, E. M. & Brun, Y. V. Cell cycle timing and developmental checkpoints in Caulobacter crescentus. Curr. Opin. Microbiol. 6, 541–549 (2003).

    Article  CAS  PubMed  Google Scholar 

  95. Ausmees, N., Kuhn, J. R. & Jacobs-Wagner, C. The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115, 705–713 (2003).

    Article  CAS  PubMed  Google Scholar 

  96. Nelson, W. J. Adaptation of core mechanisms to generate cell polarity. Nature 422, 766–774 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Moore, R. L. & Hirsch, P. Nuclear apparatus of Hyphomicrobium. J. Bacteriol. 116, 1447–1455 (1973).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Zerfas, P. M., Kessel, M., Quintero, E. J. & Weiner, R. M. Fine-structure evidence for cell membrane partitioning of the nucleoid and cytoplasm during bud formation in Hyphomonas species. J. Bacteriol. 179, 148–156 (1997). Remarkable electron micrographs showing the transit of vesicles through the Hyphomonas prostheca to the developing bud.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Brun, Y. V. & Janakiraman, R. in Prokaryotic Development (eds Brun, Y. V. & Shimkets, L. J.) 297–317 (American Society for Microbiology Press, Washington DC, 2000).

    Book  Google Scholar 

  100. Bernal, A., Ear, U. & Kyrpides, N. Genomes onLine database (GOLD): a monitor of genome projects world-wide. Nucleic Acids Res. 29, 126–127 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

I thank P. Levin and several anonymous reviewers for their helpful comments. I apologise to colleagues whose work, or favourite organism, has not been cited in this review owing to space constraints. Research in my laboratory is supported by the National Science Foundation.

Author information

Authors and Affiliations

  1. Department of Microbiology, Cornell University, 260A Wing Hall, Ithaca, 14853-5701, New York, USA

    Esther R. Angert

Authors
  1. Esther R. Angert
    View author publications

    You can also search for this author in PubMed Google Scholar

Ethics declarations

Competing interests

The author declares no competing financial interests.

Related links

Related links

DATABASES

Entrez

Bacillus subtilis

Bdellovibrio bacteriovorus

Caulobacter crescentus

Escherichia coli

Streptomyces coelicolor

Synechocystis sp. PCC 6803

SwissProt

DivIVA

EzrA

FtsZ

MinC

MinD

SMC

YneA

FURTHER INFORMATION

Esther Angert's laboratory

Glossary

NUCLEOID

The highly organized chromosomal DNA of a bacterial cell.

CYTOSKELETON

Internal network of proteins that gives a eukaryotic cell its shape, facilitates its movement and provides a means of internal spatial organization.

ENDOSPORE

A specialized dormant cell, that forms within some Gram-positive bacteria, and which is highly resistant to agents (such as heat, solvents and ultraviolet radiation) that would normally harm a vegetative cell.

COPROPHAGOUS

Feeding on faeces.

HOLDFAST

A tapered protrusion of the segmented filamentous bacterial cell that firmly secures it to an epithelial cell that lines the host intestinal tract.

OLIGOTROPHIC

A low nutrient environment.

PROSTHECA

A cellular extension, also known as a stalk or hypha, which contains cytoplasm and is bound by the cell envelope of the organism.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Angert, E. Alternatives to binary fission in bacteria. Nat Rev Microbiol 3, 214–224 (2005). https://doi.org/10.1038/nrmicro1096

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro1096

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing