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Alternatives to binary fission in bacteria

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.

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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.

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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.

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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.

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

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