Bacterial and Archaeal Inclusions

Jessup M Shively, Clemson University, Clemson, South Carolina, USA
Gordon C Cannon, University of Southern Mississippi, Hattiesburg, Mississippi, USA
Sabine Heinhorst, University of Southern Mississippi, Hattiesburg, Mississippi, USA
Donald A Bryant, Montana State University, Bozeman, Montana, USA
Shiladitya DasSarma, University of Maryland, Baltimore, Maryland, USA
Dennis Bazylinski, University of Nevada, Las Vegas, Nevada, USA
Jack Preiss, Michigan State University, East Lansing, Michigan, USA
Alexander Steinbüchel, Institut für Molekulare Mikrobiologie und Biotechnologie, Münster, Germany
Roberto Docampo, University of Georgia, Athens, Georgia, USA
Christiane Dahl, Institut für Mikrobiologie & Biotechnologie, Bonn, Germany

Published online: December 2011

DOI: 10.1002/9780470015902.a0000302.pub3

Bacterial inclusions can be defined as discrete structures seen within the confines of prokaryotic cells, generally intracytoplasmic, but in some instances in the periplasmic region of the cell. Inclusions function as metabolic reserves, cell positioners, or as metabolic organelles. Some inclusions may contribute to more than one of these functions. Those that function as metabolic reserves are glycogen, polyhydroxyalkanoate, wax ester, triacylglycerol, cyanophycin, and polyphosphate granules, and sulfur globules. These reserves are commonly accumulated in response to a nutrient imbalance, for example, under conditions of excess carbon/energy. Magnetosomes and gas vesicles contribute to cell mobility thereby assisting the cells in attaining nutrient and/or redox needs. Carboxysomes, containing the enzyme ribulose bisphosphate carboxylase/oxygenase, and chlorosomes, sacs of self-aggregated bacterriochlorophyll are carbon-fixing and light-harvesting organelles, respectively.

Key Concepts:

  • The cytoplasmic region of prokaryotic cells can be much more complex than originally thought.
  • In addition to flagella, many prokaryotes have developed mechanisms whereby they are capable of positioning/orienting themselves in an aqueous environment.
  • Although not as complex as the well-known eukaryotic organelles, many prokaryotes possess simple organelles.
  • Many of the inclusions may have useful properties for applications in biotechnology

Keywords: granules; globules; vesicles; crystals; metabolic reserves; simple organelles; inclusions; mobility

Figure 1. Transmission electron micrographs of polyhedral inclusions of bacteria. (a) Thin section of Halothiobacillus neapolitanus. Carboxysomes indicated with arrows. Bar, 1 m. (b) Negative stain of carboxysomes purified from H. neapolitanus. Ribulose bisphosphate carboxylase/oxygenase particles clearly visible within the carboxysomes. Bar, 100 nm. (c) Thin section of Salmonella enterica. Polyhedral bodies indicated with arrows. Bar, 1 m. Micrographs courtesy of Henry C. Aldrich, University of Florida, Gainesville. (d) Model of a carboxysome shell that consists of the common microcompartment building blocks, pfam 00936 proteins (blue hexamers, CsoS1 or CcmK) and pfam 03319 proteins (yellow pentamers, CsoS4 or CcmL). Panel (d) was originally published in and Adapted from Tanaka et al., (2009) Atomic-level models of the bacterial carboxysome shell. Science 319: 5866, with permission from American Association for the Advancement of Science (AAAS).
Figure 2. Structure of chlorosomes from the green sulfur bacterium Chlorobaculum tepidum. (a) Thin-section electron micrograph showing chlorosomes, electron transparent ovoids, on the inner surface of the cytoplasmic membrane. (b) Electron micrograph showing negatively stained chlorosomes from wild type. (c) Cryo-electron micrograph showing the structure of BChl d molecules in chlorosomes of a bchQ bchR bchU mutant of C. tepdium. (d) Electron micrograph of a single, negatively stained chlorosome from the bchQ bchR bchU mutant of C. tepdium. (e) Cryo-electron micrograph showing an end view of a single chlorosome from the bchQ bchR bchU mutant of C. tepdium. The three vertical white arrows indicate the lamellar surfaces that are separated 2.1 nm and that are formed from the syn-anti monomer stacks of BChl d. (f) Scheme showing the organisation of the syn-anti monomer stacks of BChl d in the chlorosomes of the bchQ bchR bchU mutant of C. tepdium. (g) Scheme showing the overall organisation of BChls and Csm proteins in wild-type chlorosomes. Chlorophylls may be organised as nanotubes (left) or ‘undulating lamellae’ or folded sheets (right). Red arrows indicate energy transfer pathways and blue arrows indicate electron transfer pathways. For additional details, see text.
Figure 3. Idealised diagram of a cylindrical gas vesicle with end-caps, highlighting the striated structures (left). A de novo model of GvpA, the major gas vesicle protein, showing its coil–––––coil structure (right). The antiparallel -regions (blue arrows) are thought to form the hydrophobic inner surface of the protein membrane, whereas the -regions form the hydrophilic outer surface. The width of the striated structures, 4.5 nm, is indicated by lines and arrows. Figure courtesy of Ezzeldin HM, Kaluda JB, DasSarma S and Solares SD, University of Maryland, unpublished results.
Figure 4. (a) Electron micrograph of a negatively stained cell of marine, Magnetotactic spirillum showing chain of electron-dense magnetosomes along the long axis of the cell. (b) A transmission electron micrograph of a thin section of a Magnetotactic vibrio showing the magnetosome membrane (at arrows) as a thin electron-dense layer surrounding the magnetite crystals. Micrograph (b) courtesy of Terrence Beveridge and Dianne Moyles, University of Guelph, Ontario, Canada.
Figure 5. (a) Structural formula. (b) A transmission electron micrograph of a thin section of the Gram-negative bacterium Ralstonia eutropha showing PHB granules. Cells were grown in a mineral salts medium containing 1.5% sodium gluconate and had accumulated PHB to approximately 70% of the cell dry matter. Bar, 0.2 m. Micrograph courtesy of Markus Pötter and Rudolf Reichelt, Westfälische Wilhelms-Universität Münster.
Figure 6. Model proposed for PHB granule formation in bacteria. This figure was reproduced from Wältermann et al., 2005 and is based on studies done in Ralstonia eutropha (see also references cited in Wältermann et al., 2005).
Figure 7. (a) Long-chain-length fatty acids and glycerol or long-chain-length fatty alcohols. Structural formulas. (b) A transmission electron micrograph of a thin section of the Gram-positive bacterium Rhodococcus opacus strain PD630 showing TAG granules. Cells were grown in a mineral salts medium containing 1.5% (wt vol–1) sodium gluconate and had accumulated various TAGs to approximately 80% of the cell dry matter. Bar, 0.5 m. Figure reproduced from Alvarez et al. (1996).
Figure 8. Model proposed for TAG and WE granule formation in prokaryotes. This figure was reproduced from Wältermann et al., 2005 and is based on studies done in Acinetobacter baylyi and Rhodococcus opacus.
Figure 9. (a) Structural formula. (b) A transmission electron micrograph of a thin section of the Gram-negative bacterium Acinetobacter baylyi showing cyanophycin granules. Cells were grown in a mineral salts medium containing 75 mm arginine and 10 mm ammonium sulfate and had accumulated cyanophycin up to approximately 40% of the cell dry matter. Micrograph courtesy of Yasser Elbahloul and Rudolf Reichelt, Westfälische Wilhelms-Universität Münster.
Figure 10. Acidocalcisomes in Agrobacterium tumefaciens. (a) electron micrograph of intact bacteria. Arrow shows an electron-dense material in the periphery of an acidocalcisome. White arrowhead shows an electron-dense inclusion. (b) Staining of acidocalcisomes with antibodies against a vacuolar proton pyrophosphatase as detected by immunoelectron microscopy. Arrowheads show the gold particles labelling the membrane of an acidocalcisome (vg, volutin granule). Bars, (a)=0.1 m; (b)=40 nm. Reproduced with permission from Seufferheld et al. (2003). © The American Society for Biochemistry and Molecular Biology.
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 Further Reading
    book Frigaard N-U and Bryant DA (2006) "Chlorosomes: antenna organelles in green photosynthetic bacteria". In: Shively JM (ed.) Microbiological Monographs Vol. 2: Complex Intracellular Structures in Prokaryotes, pp. 79–114. Berlin, Heidelberg: Springer-Verlag.
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    Kalscheuer R and Steinbüchel A (2003) A novel bifunctional wax ester synthase/acyl-CoA: diacylglycerol acyltransferase mediates wax ester and triacylglycerol biosynthesis in Acinetobacter calcoaceticus ADP1. Journal of Biological Chemistry 278: 8075–8082.
    Peplinski K, Ehrenreich A, Döring C et al. (2010) Genome-wide transcriptome analyses of the “Knallgas” bacterium Ralstonia eutropha H16 with regard to polyhydroxyalkanoate metabolism. Microbiology (SGM) 156: 2136–2152.
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    book Schüler D (ed.) (2007) Microbiological Monographs Vol. 3: Magnetoreception and Magnetosomes in Bacteria, pp. 319. Berlin, Heidelberg: Springer-Verlag.
    book Shively JM, Cannon GC, Heinhorst S et al. (2009) "Intracellular structures of prokaryotes: inclusions, compartments and assemblages". In: Schaechter M (ed.) Encyclopedia of Microbiology, pp. 404–424. Oxford: Elsevier.
    Walsby AE (1994) Gas vesicles. Microbiological Reviews 58: 94–144.

Related Sub-Topics:

Cell Compartments and Cellular Organelles | Cell Motility | Cell Energetics | Composition and Structure of Microbial Cells | Bacteria | Energetics and Catabolism | Microbial Photosynthesis
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Article Title: Bacterial and Archaeal Inclusions
 
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Shively, Jessup M, Cannon, Gordon C, Heinhorst, Sabine, Bryant, Donald A, DasSarma, Shiladitya, Bazylinski, Dennis, Preiss, Jack, Steinbüchel, Alexander, Docampo, Roberto, and Dahl, Christiane(Dec 2011) Bacterial and Archaeal Inclusions. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000302.pub3]