Skin and bones: the bacterial cytoskeleton, cell wall, and cell morphogenesis
Matthew T. Cabeen and Christine Jacobs-Wagner
Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT 06520
THE JOURNAL OF CELL BIOLOGY
The bacterial world is full of varying cell shapes and sizes, and individual speciesperpetuate a deﬁned morphology generation after generation. We review recent ﬁndings and ideas about how bacteria use the cytoskeleton and other strategies to regulate cell growth in time and space to produce different shapes and sizes.
infections (Chan et al., 1994). These morphological responses and the faithful maintenance and propagation of cell morphology indicate that sophisticated controlsystems must exist to regulate cell morphogenesis.
The cell morphogenesis triumvirate: cell wall, turgor pressure, and cytoskeleton
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Bacteria are exceedingly tiny compared with most eukaryotic organisms, yet, far from being amorphous bags of biomolecules, they display a breathtaking array of cell morphologies from spheres, rods, and helicesto tapered, branched, and flat shapes. Both shape and size are important for cell function, particularly with respect to diffusion and nutrient uptake. A sphere may seem a simple shape to achieve, but its surface area to volume ratio rapidly shrinks with increased size. Meanwhile, a rod can maintain a viable ratio with greater volumes. Other bacteria develop one or more long, thin appendages thateffectively increase the exposed surface area without substantially increasing volume. The shape of a bacterium is not dictated by diffusion considerations alone. For example, cyanobacteria are able to survive on exposed sandstone surfaces by forming long cell filaments that can insert and lodge in multiple pores (Kurtz and Netoff, 2001). With a variety of strategies available to a cell, it seemslikely that the morphology of each species is uniquely tailored for fitness and survival (Young, 2006). Remarkably, these defined bacterial cell morphologies are maintained and propagated from one generation to the next, underscoring the importance of cell shape and size. Bacteria can also make morphological transitions in response to changes in environmental conditions. For example, Escherichiacoli increases its length and diameter slightly when its growth rate is increased (Woldringh et al., 1980); the rod-shaped plant symbiont Sinorhizobium meliloti differentiates into Y-shaped nitrogenfixing cells in plant cells (VandenBosch et al., 1989); uropathogenic E. coli cells lengthen into long filaments as part of an immune evasion response (Justice et al., 2006); and the spiral-shapedpathogen Helicobacter pylori adopts a spherical (coccoid) shape both in extended culture (Benaissa et al., 1996) and in stomach
Correspondence to Christine Jacobs-Wagner: email@example.com Abbreviations used in this paper: PBP, penicillin-binding protein; PG, peptidoglycan.
Bacteria, like other organisms with walled cells such as plants and fungi, must temporally and spatially controlcell wall synthesis to regulate cell morphogenesis. An essential component of the bacterial cell wall is the peptidoglycan (PG), a meshwork of glycan strands cross-linked by peptide bridges that is synthesized and modified by enzymes collectively named penicillinbinding proteins (PBPs) because of their penicillin-binding property. Gram-negative bacteria mainly have one single layer of PG, whereasGram-positive bacteria have multiple layers that are linked to each other via short peptides (Höltje, 1998). Either way, the mono- or multilayered PG forms one single, giant molecule that surrounds the cytoplasmic membrane and protects it from the turgor pressure exerted by the cytoplasm. The wall restrains the turgor pressure to avoid swelling and lysis, and the turgor pressure, in turn, is...