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Cell Biology of Prokaryotic Organelles Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press Cell Biology of Prokaryotic Organelles Dorothee Murat, Meghan Byrne, and Arash Komeili Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, California 94720-3102 Correspondence: [email protected] Mounting evidence in recent years has challenged the dogma that prokaryotes are simple and undefined cells devoid of an organized subcellular architecture. In fact, proteins once thought to be the purely eukaryotic inventions, including relatives of actin and tubulin control prokaryotic cell shape, DNA segregation, and cytokinesis. Similarly, compartmental- ization, commonly noted as a distinguishing feature of eukaryotic cells, is also prevalent in the prokaryotic world in the form of protein-bounded and lipid-bounded organelles. In this article we highlight some of these prokaryotic organelles and discuss the current knowledge on their ultrastructure and the molecular mechanisms of their biogenesis and maintenance. he emergence of eukaryotes in a world Skeptical readers might wonder if a pro- Tdominated by prokaryotes is one of the karyotic structure can really be defined as an defining moments in the evolution of modern organelle. Here we categorize any compartment day organisms. Although it is clear that the cen- bounded by a biological membrane with a dedi- tral metabolic and information processing ma- cated biochemical function as an organelle. This chineries of eukaryotes and prokaryotes share a simple and broad definition presents cells, be common ancestry, the origins of the complex they eukaryotes or prokaryotes, with a similar eukaryotic cell plan remain mysterious. Eukary- set of challengesthat need to be addressed to suc- otic cells are typified by the presence of intracel- cessfully build an intracellular compartment. lular organelles that compartmentalize essential First, an organism needs to mold a cellular mem- biochemical reactions whereas their prokaryotic brane into a desired shape and size. Next, the counterparts generally lack such sophisticated compartment must be populated with the pro- subspecialization of the cytoplasmic space. In per set of proteins that carry out the activity of most cases, this textbook categorization of eu- the organelle. Finally, the cell must ensure the karyotes and prokaryotes holds true. However, proper localization, maintenance and segrega- decades of research have shown that a number tion of these compartments across the cell cycle. of unique and diverse organelles can be found Eukaryotic cells perform these difficult mecha- in the prokaryotic world raising the possibility nistic steps using dedicated molecular pathways. that the ability to form organelles may have Thus, if connections exist between prokaryotic existed before the divergence of eukaryotes and eukaryotic organelles it seems likely that from prokaryotes (Shively 2006). relatives of these molecules may be involved in Editors: Lucy Shapiro and Richard M. Losick Additional Perspectives on Cell Biology of Bacteria available at www.cshperspectives.org Copyright # 2010 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a000422 Cite this article as Cold Spring Harb Perspect Biol 2010;2:a000422 1 Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press D. Murat, M. Byrne, and A. Komeili the biogenesis and maintenance of prokaryotic in a variety of applied settings have made them organelles as well. center of most studies on magnetosomes (Bazy- Prokaryotic organelles can be generally div- linski and Frankel 2004). ided into two major groups based on the com- From a cell biological perspective, however, position of the membrane layer surrounding it is the often-neglected magnetosome mem- them. First are the cellular structures bounded brane that may hold the key to understanding by a nonunit membrane such a protein shell or fundamental properties of prokaryotic organ- a lipid monolayer (Shively 2006). Well-known elles. Detailed electron microscopic (EM) work examples of these compartments include lipid and biochemical studies have shown that the bodies, polyhydroxy butyrate granules, carbox- magnetosome membrane has the cytological ysomes, and gas vacuoles. The second class con- and chemical properties of a lipid bilayer mem- sists of those organelles that are surrounded by a brane (Gorby et al. 1988; Gru¨nberg et al. 2004). lipid-bilayer membrane, an arrangement that is Additionally, numerous proteomic studies have reminiscent of the canonical organelles of the shown that this compartment contains a unique eukaryotic endomembrane system. Therefore, mix of soluble and transmembrane domain- this article is dedicated to a detailed exploration containing proteins, implying the existence of of three prokaryotic lipid-bilayer bounded or- a dedicated protein sorting pathway (Okuda ganelle systems: the magnetosomes of magneto- et al. 1996; Gru¨nberg et al. 2001; Gru¨nberg tactic bacteria, photosynthetic membranes, and et al. 2004; Tanaka et al. 2006). The magneto- the internal membrane structures of the Planc- some membrane loaded with its protein cohort tomycetes. In each case, we present the most is present before crystal formation and serves as recent findings on the ultrastructure of these the site of biomineralization further confirming organelles and highlight the molecular mecha- that it is an independent organelle (Komeili nisms that control their formation, dynamics, et al. 2004). The organization of magnetosomes and segregation. We also highlight some pro- into one or multiple chains also suggests that tein-bounded compartments to present the mechanisms must exist for the proper localiza- reader with a more complete view of prokaryotic tion and division of this structure within the compartmentalization. cell. This already detailed view of the magneto- some has been pushed to the next level with two recent imaging studies that describe the use of Magnetosomes: Bacterial Compasses cryo-electron tomography (CET) to obtain The magnetosomes of magnetotactic bacteria high resolution three-dimensional images of (MB) are one of the most fascinating prokary- MB (Komeili et al. 2006; Scheffel et al. 2006). otic compartments (Fig. 1). MB are a phyloge- In CET a series of two-dimensional images of netically diverse group of microorganisms with a specimen, taken by tilting the stage of an elec- the ability to use geomagnetic field lines as tron microscope at various angles relative to the guides in their search for their preferred redox electron beam, is translated into a three-dimen- conditions (Bazylinski and Frankel 2004; Kom- sional image using a specific algorithm. This eili 2007). This behavior is achieved through the technique provides such a detailed view of a use of a unique magnetic organelle termed the cell that disruptive fixing and staining treat- magnetosome. A magnetosome consists of a ments common in other EM techniques are lipid bilayer membrane that houses an approx- not needed. As a result one can prepare a sample imately 50-nanometer crystal of the magnetic by a simple rapid freezing method and sub- mineral magnetite (Fe3O4) or greigite (Fe3S4). sequently image a cell at high resolution in a Individual magnetosomes are arranged into one near-native state (Milne and Subramaniam or more chains within the cell where they act 2009). This combination of rapid preservation, passively to orient the bacterium within a mag- minimal disruption of cellular features, and netic field. The unusual properties of these mag- nanometer scale resolution revealed features of netic minerals and their potential to be exploited magnetosomes that had not been visualized in 2 Cite this article as Cold Spring Harb Perspect Biol 2010;2:a000422 Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press Cell Biology of Prokaryotic Organelles Figure 1. Magnetosomes can be easily visualized with various forms of electron microscopy. The electron-dense magnetite crystals are seen as a chain running through the cell in (A). Cryo-electron tomography was instrumen- tal in demonstrating that the magnetosome membrane is an invagination of the inner cell membrane (B) and cytoskeletal filaments surround the magnetosome chain (C). (A, Reprinted, with permission from Komeili et al. 2004 [# National Academy of Sciences]; B, reprinted with permission from Komeili et al. 2006 [# AAAS]; C, image courtesy of Zhuo Li and Grant Jensen.) more than 30 years of work on MB. Most strik- crystals implying that this organelle is an invag- ing was the finding that in Magnetospirillum ination of the inner membrane at all times magneticum AMB-1, individual magnetosomes (Komeili et al. 2006). Although such an organ- are not separated into vesicles and are instead in- ization might seem puzzling at first it does make vaginations of the inner cell membrane (Fig. 1B). sense in the context of magnetosome function This state was observed in empty magnetosomes and magnetite biomineralization. Because the as well as those that contained fully formed primary job of the magnetosome chain is to Cite this article as Cold Spring Harb Perspect Biol 2010;2:a000422 3 Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press D. Murat, M. Byrne, and A. Komeili orient the cell in external magnetic fields the or- magnetosome
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