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How Do Bacteria Localize Proteins to the Cell Pole?

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How Do Bacteria Localize Proteins to the Cell Pole? ß 2014. Published by The Company of Biologists Ltd | Journal of Cell Science (2014) 127, 11–19 doi:10.1242/jcs.138628 COMMENTARY How do bacteria localize proteins to the cell pole? Ge´raldine Laloux1 and Christine Jacobs-Wagner2,3,4,* ABSTRACT Within the bacterial cytoplasm, the cell poles – the rounded ends of rod-shaped cells that are generated by each division event It is now well appreciated that bacterial cells are highly organized, – constitute a domain where a subset of proteins specifically which is far from the initial concept that they are merely bags of localizes. Proteins that localize at the poles (referred to as ‘polar randomly distributed macromolecules and chemicals. Central to proteins’ hereafter) are numerous and vary widely in function. their spatial organization is the precise positioning of certain Localization of polar proteins, which is the focus of this proteins in subcellular domains of the cell. In particular, the cell Commentary, is essential for a large number of important poles – the ends of rod-shaped cells – constitute important cellular processes in bacteria, including cell cycle regulation, platforms for cellular regulation that underlie processes as cell differentiation, virulence, chemotaxis, motility and adhesion essential as cell cycle progression, cellular differentiation, (Bowman et al., 2011; Kirkpatrick and Viollier, 2011). Our goal virulence, chemotaxis and growth of appendages. Thus, here is not to provide a survey of the large number of polar understanding how the polar localization of specific proteins is proteins described so far, many of which have been reviewed achieved and regulated is a crucial question in bacterial cell biology. elsewhere (Ebersbach and Jacobs-Wagner, 2007; Dworkin, 2009; Often, polarly localized proteins are recruited to the poles through Kirkpatrick and Viollier, 2011; Davis and Waldor, 2013). Instead, their interaction with other proteins or protein complexes that were our objective is to review and illustrate the general principles already located there, in a so-called diffusion-and-capture used by bacterial cells to localize proteins at the poles. mechanism. Bacteria are also starting to reveal their secrets on The patterns displayed by proteins inside bacterial cells can be complex. Indeed, some proteins are known to change location how the initial pole ‘recognition’ can occur and how this event can be over time, such as during the course of the cell cycle; others regulated to generate dynamic, reproducible patterns in time (for reproducibly accumulate at only one of the two cell poles. The example, during the cell cycle) and space (for example, at a specific dynamics and asymmetry of polar localization underlie central cell pole). Here, we review the major mechanisms that have been cellular processes in bacteria, yet the mechanisms that control described in the literature, with an emphasis on the self-organizing polar localization in space and time are only starting to be principles. We also present regulation strategies adopted by bacterial uncovered. In this Commentary, we first summarize several polar cells to obtain complex spatiotemporal patterns of protein localization. localization mechanisms that have been selected during bacterial evolution. Then, we examine possible strategies that control these KEY WORDS: Bacterial cell cycle, Polar localization, Spatial mechanisms to produce specific spatiotemporal patterns of organization protein localization. Introduction How proteins localize at the cell poles: themes and variations Evidence for the elaborate spatial organization of bacterial cells Diffusion and capture through protein–protein interaction started to accumulate more than two decades ago, challenging the Most of the polar proteins identified so far are simply recruited to antiquated idea that bacteria were simple vessels of randomly the cell poles through an interaction with a protein or protein distributed macromolecules, far removed from organized, complex already present at the pole (Fig. 1A). In this scenario, compartmentalized eukaryotic cells. This misconception protein A diffuses in the cytoplasmic space until it encounters a naturally originated from the observation that the cytoplasm of polar protein B for which it has a binding affinity. Because of the these tiny cells generally lacks intracellular membrane-enclosed transient nature of protein–protein interactions, protein A is organelles in which biomolecules – hence cellular functions – can continuously exchanged between the diffusing pool in the cell be sorted. It is now well appreciated that cellular components of body and the localized pool at the pole. The concentration of various kinds (proteins, lipids, DNA, RNAs, ribosomes and protein B at the poles and the rates of association and dissociation metabolites) can display subcellular arrangements in bacterial between the interacting partners A and B will determine the cells. This spatial organization is critical for various aspects of extent of the polar accumulation of protein A at steady state. Note bacterial physiology and adaptation to diverse environments that ‘diffusion and capture’ is a general mechanism that also (Matsumoto et al., 2006; Shapiro et al., 2009; Rudner and Losick, explains the subcellular localization of many non-polar proteins. 2010; Campos and Jacobs-Wagner, 2013). Remarkably, some proteins can serve as polar landmarks or hubs for multiple proteins, which can themselves recruit other proteins, and so forth. These hub proteins tend to play important roles in different pathways or cell cycle events. For example, 1de Duve Institute, Universite´ Catholique de Louvain, B-1200 Brussels, Belgium. 2Department of Molecular, Cellular and Developmental Biology, Yale University, DivIVA is involved in several cellular programs in Bacillus New Haven, CT 06520, USA. 3Howard Hughes Medical Institute, Yale University, subtilis through the recruitment of multiple proteins: the New Haven, CT 06519, USA. 4Department of Microbial Pathogenesis, Yale School competence regulator ComN (dos Santos et al., 2012), the of Medicine, New Haven CT 06511, USA. division inhibitor Maf in competent cells (Briley et al., 2011) and *Author for correspondence ([email protected]) the determinants of division site placement MinCD via MinJ Journal of Cell Science 11 COMMENTARY Journal of Cell Science (2014) 127, 11–19 doi:10.1242/jcs.138628 A Diffusion and capture B Negative curvature R = 2/ RC RC = 1/ C Diffusing protein Polar protein R = 2/ C C Nucleoid occlusion D Affinity for polar features of the cell envelope Sidewall Pole Key E E Lipopolysaccharide OM OM Phospholipid P P Anionic phospholipid enriched at the poles (e.g. cardiolipin) CM CM Peptidoglycan Nucleoid Oligomer of a (chromosomal DNA self-assembling or Peptidoglycan turnover C C and proteins) aggregating protein Protein with affinity for cardiolipin Fig. 1. Localization of polar proteins through the recognition of polar features. (A) A protein (e.g. ParA1 in V. cholerae) diffusing in the cytoplasm (as indicated by single arrows) is trapped at the poles transiently (double arrows) through an affinity for a polar protein (e.g. HubP in V. cholerae) that is already localized at the cell poles. (B) Higher-order protein assemblies are favored in membrane regions of stronger curvature. Left: representation of a rod-shaped cell showing the radius of curvature (R) and the stronger negative curvature (C, curved arrows) at the cell poles (blue areas) compared with the sides of the cylinder (gray area), as described previously (Huang and Ramamurthi, 2010). Middle and right: formation of a higher-order protein assembly occurring preferentially in membrane regions of stronger negative curvature (e.g. DivIVA in B. subtilis). Arrows indicate the free diffusion of oligomers. (C) Formation of large protein assemblies such as higher-order structures (e.g. PopZ in C. crescentus) or protein aggregates (e.g. misfolded proteins in E. coli) is energetically favored outside the nucleoid region. (D) Differences in composition of the cytoplasmic membrane and peptidoglycan between cell poles and the rest of the cell envelope can serve as cues for localization of polar proteins. The particular case of a protein (e.g. ProP in E. coli) that preferentially binds anionic phospholipids enriched at the poles, such as cardiolipin, is depicted. E, extracellular space; OM, outer membrane; P, periplasmic space; CM, cytoplasmic membrane; C, cytoplasm. Note that the schematics in all figures are not to scale and do not reflect the structure of the illustrated proteins. (Bramkamp et al., 2008; Patrick and Kearns, 2008; chromosome. Because both ParB–parS complexes also carry a Eswaramoorthy et al., 2011). Moreover, DivIVA attaches the division inhibitor, their PopZ-dependent tight fastening at both chromosomal origin at the pole in the developing spore through an poles after complete segregation is essential for the correct interaction with the DNA-binding protein RacA (Ben-Yehuda et positioning of the division site near the midcell, where the al., 2003; Wu and Errington, 2003). In Caulobacter crescentus, inhibitor concentration is the lowest (Thanbichler and Shapiro, PopZ, which shares no sequence or structural similarity with 2006; Ebersbach et al., 2008). In Vibrio cholerae, HubP provides a DivIVA, also anchors the chromosomal origin at the pole through link between chromosome segregation, chemotaxis and flagellum an interaction with the chromosome partition complex, and synthesis by localizing
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