Polarity in Action: Asymmetric Protein Localization in Bacteria

Abstract

Recent advances in microscopy and protein localization techniques have provided new insights into the remarkable complexity of the bacterial cell. Although bacteria lack discrete cellular compartments such as organelles, they possess an impressive scheme of subcellular organization at the level of protein localization. There are a growing number of examples of bacterial proteins for which specific intracellular localizations are essential for proper function and regulation. Dynamic polar localization of proteins critical for cell division, chromosome partitioning, and cell cycle control in Escherichia coli, Bacillus subtilis, and Caulobacter crescentus have recently been described (see Table 1). These exciting observations establish that bacterial polarity plays a critical cellular role and that prokaryotic organization is much more complex than previously believed.Clearly, many proteins and protein complexes are able to navigate the bacterial cell and ultimately recognize their appropriate destinations. The current challenge is to uncover the mechanisms, both active and passive, by which proteins are localized and then maintained at the proper intracellular location. The goal of this minireview is to explore a variety of examples of bacterial polarity, to expand upon the current models of polar localization, and to shed light on the spectrum of ways that bacteria may distinguish the polar cellular membrane from the lateral membrane. Several excellent reviews covering recent observations of dynamic polar protein localization have recently been published (7,37,38,41,76,82,83,92,93,102). Here we focus on other aspects of bacterial polarity, including the ultrastructural differences at the cell pole, the modes of polarity in actin-based motility and chemotaxis, and the implications of polarity in bacterial cellular function. MORPHOLOGICAL DIFFERENCES AT CELL ENDSThe diversity of bacterial shapes extends well beyond the basic sphere, rod, and spirochete forms. Many bacteria are decorated with pili, flagella, and/or stalks, which are often found exclusively at one or both cell poles. The presence of such polar structures reveals that at least some bacteria display a complicated organization scheme, since biogenesis of polar structures clearly demands an asymmetry of their components.In addition to these external polar structures, early ultrastructural studies revealed internal differences at the cell poles of some bacteria. One striking example is the polar organelle found at the flagellated pole of diverse gram-negative bacteria such as Aquaspirillum (65), Sphaerotilus (96), Rhodopseudomonas (95), Campylobacter (9, 75), and Helicobacter (63). In each case, the polar organelle is subpolarly located near the cytoplasmic membrane adjacent to the flagella (Fig. 1), suggesting a relationship between the polar flagella and the polar organelle. Further supporting this model, Sphaerotilus natans swarm cells have a polar organelle, whereas nonmotile cells do not (34). The polar organelle has not been identified in all polarl...

A polymerization-depolymerization model that accurately generates the self-sustained oscillatory system involved in bacterial division site placement

“…This observation implies that cell poles differ biochemically from other regions of the E. coli cell envelope. Consistent with this idea, a number of proteins are localized specifically to cell poles in E. coli and other organisms (19)(20)(21)(22). If the localization of MinD and͞or other polar proteins is initiated by interaction with specific nucleation sites, as predicated in the present model, the ''site'' could be either a protein or a function of local membrane phospholipid composition or organization.…”

Polar location and functional domains of the Agrobacterium tumefaciens DNA transfer protein VirD4

“…As the mutation is expected to affect nucleotide binding, these results suggest that the second step, the targeting of the oligomer to the cell pole, may be an energy-dependent process. Two bacterial proteins, Listeria monocytogenes IscA and Shigella flexneri ActA, localize to a single pole and use different mechanisms for their unipolar localization (Lybarger and Maddock, 2001). The polar location of VirD4 raises interesting questions on the location of the T-DNA transport apparatus.…”

“…Proteins essential for critical biological processes, e.g. cell division, chromosome partitioning and cell cycle control in bacteria, have been localized to the cell poles (Lybarger and Maddock, 2001). Substrate transfer by the type IV transport mechanism is another process that probably uses the cell pole.…”

Universal architecture of bacterial chemoreceptor arrays

“…S1A]. MCPs cluster together with other chemotaxis proteins including CheA and CheW in large arrays at the cell pole (5)(6)(7)(8)(9).…”