Bacterial and Archaeal Inclusions

Abstract

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 μm. (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 μm. 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. Science319: 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 BChld 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 BChld. (f) Scheme showing the organisation of the syn‐anti monomer stacks of BChld 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–α–β–β–α–coil structure (right). The antiparallel β‐regions (blue arrows) are thought to form the hydrophobic inner surface of the protein membrane, whereas the α‐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., and is based on studies done in Ralstonia eutropha (see also references cited in Wältermann et al., ).

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. .

Figure 8.

Model proposed for TAG and WE granule formation in prokaryotes. This figure was reproduced from Wältermann et al., 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 μm; (b)=40 nm. Reproduced with permission from Seufferheld et al. . © The American Society for Biochemistry and Molecular Biology.

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References

Alvarez HM, Mayer F, Fabritius D et al. (1996) Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Archives of Microbiology 165: 377–386.

Ballicora MA, Iglesias AA and Preiss J (2003) ADP‐glucose pyrophosphorylase; a regulatory enzyme for bacterial glycogen synthesis. Microbial and Molecular Biological Reviews 67: 213–225.

Bazylinski DA and Frankel RB (2004) Magnetosome formation in prokaryotes. Nature Reviews Microbiology 2: 217–230.

Bryant DA and Frigaard N‐U (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends in Microbiology 14: 488–496.

Bryant DA, Garcia Costas AM, Maresca JA et al. (2007) “Candidatus Chloracidobacterium thermophilum”: an aerobic phototrophic acidobacterium. Science 317: 523–526.

Chandra G, Chater KF and Bornemann S (2011) Unexpected and widespread connections between bacterial glycogen and trehalose metabolism. Microbiology 157: 1565–1572.

Chu LJ, Chen MC, Setter J et al. (2011) New structural proteins of Halobacterium salinarum gas vesicle revealed by comparative proteomics analysis. Journal of Proteome Research 10: 1170–1178.

Cort JR, Selan UM, Schulte A et al. (2008) Allochromatium vinosum DsrC: solution‐state NMR structure, redox properties and interaction with DsrEFH, a protein essential for purple sulfur bacterial sulfur oxidation. Journal of Molecular Biology 362: 692–707.

DasSarma S and Arora P (1997) Genetic analysis of gas vesicle gene cluster in haloarchaea. FEMS Microbiology Letters 153: 1–10.

Docampo R (2006) Acidocalcisomes and polyphosphate granules. In: Shively JM (ed.) Microbiology Monographs Vol.1: Inclusions in Prokaryotes, pp. 53–70. Berlin, Heidelberg: Springer‐Verlag.

Docampo R and Moreno SN (2011) Acidocalcisomes. Cell Calcium 50: 113–115.

Elbein AD, Pastuszak I, Tackett AJ et al. (2010) Last step in the conversion of trehalose to glycogen: a mycobacterial enzyme that transfers maltose from maltose 1‐phosphate to glycogen. Journal of Biological Chemistry 285: 9803–9812.

Frankel RB, Williams TJ and Bazylinski DA (2007) Magneto‐aerotaxis. In: Schüler D (ed.) Microbiological Monographs Vol.3: Magnetoreception and Magnetosomes in Bacteria, pp. 1–24. Berlin, Germany: Springer‐Verlag.

Frigaard N‐U, Li H, Milks KJ et al. (2004) Nine mutants of Chlorobium tepidum each unable to synthesize a different chlorosome protein still assemble functional chlorosomes. Journal of Bacteriology 186: 646–653.

Ganapathy S, Oostergetel GT, Wawrzyniak PK et al. (2009) Alternating syn‐anti bacteriochlorophylls form concentric helical nanotubes in chlorosomes. Proceedings of the National Academy of Sciences USA 106: 8525–8530.

Heinhorst S, Cannon GC and Shively JM (2006) Carboxysomes and carboxysome‐like inclusions. In: Shively JM (ed.) Microbiological Monographs Vol. 2: Complex Intracellular Structures in Prokaryotes, pp. 141–165. Berlin, Heidelberg: Springer‐Verlag.

Kerfeld CA, Heinhorst S and Cannon GC (2010) Bacterial microcompartments. Annual Review of Microbiology 64: 391–408.

Komeili A (2007) Cell biology of magnetosome formation. In: Schüler D (ed.) Microbiological Monographs Vol. 3: Magnetoreception and Magnetosomes in Bacteria, pp. 163–174. Berlin, Heidelberg: Springer‐Verlag.

Li H and Bryant DA (2009) Envelope proteins of the CsmB/CsmF and CsmC/CsmD motif families help determine the size, shape and composition of chlorosomes in Chlorobaculum tepidum. Journal of Bacteriology 191: 7109–7120.

Oostergetel GT, Reus M, Gomez Maqueo Chew A et al. (2007) Long‐range organization of bacteriochlorophyll in chlorosomes of Chlorobium tepidum investigated by cryo‐electron microscopy. FEBS Letters 581: 5435–5439.

Peña KL, Castel SE, de Araujo C et al. (2010) Structural basis of the oxidative activation of the carboxysomal γ‐carbonic anhydrase, CcmM. Proceedings of the National Academy of Sciences USA 107: 2455–2460.

Pötter M and Steinbüchel A (2005) Poly(3‐hydroxybutyrate) granule‐associated proteins: impacts on PHB synthesis and degradation. Biomacromolecules 6: 552–560.

Prange A, Chauvistré R, Modrow H et al. (2002) Quantitative speciation of sulfur in bacterial sulfur globules: X‐ray absorption spectroscopy reveals at least three different species of sulfur. Microbiology 148: 267–276.

Prange A, Engelhardt H, Trüper HG et al. (2004) The role of the sulfur globule proteins of Allochromatium vinosum: mutagenesis of the sulfur globule protein genes and expression studies by real‐time RT‐PCR. Archives of Microbiology 182: 165–174.

Preiss J (2009) Glycogen Biosynthesis. In: Schaechter M (ed.) The Encyclopedia of Microbiology, 3rd edn, pp. 145–158. Oxford: Elsevier.

Psencík J, Ikonen TP, Laurinmäki P et al. (2004) Lamellar organization of pigments in chlorosomes, the light harvesting complexes of green photosynthetic bacteria. Biophysical Journal 87: 1165–1172.

Sallam A, Steinle A and Steinbüchel A (2009) Cyanophycin: biosynthesis and applications. In: Rehm BHA (ed.) Microbial Production of Biopolymers and Polymer Precursors: Applications and Perspectives, 1st edn, pp. 79–99. Norfolk, Caister: Academic Press.

Seufferheld M, Vieira MC, Ruiz FA et al. (2003) Identification of organelles in bacteria similar to acidocalcisomes of unicellular eukaryotes. Journal of Biological Chemistry 278: 29971–29978.

Shively JM (ed.) (2006a) MicrobiologyMonographs Vol.1: Inclusions in Prokaryotes, 349pp. Berlin, Heidelberg: Springer‐Verlag.

Shively JM (ed.) (2006b) Microbiology Monographs Vol. 2: Complex Intracellular Structures in Prokaryotes, 379pp. Berlin, Heidelberg: Springer‐Verlag.

Shukla HD and DasSarma S (2004) Complexity of gas vesicle biogenesis in Halobacterium sp. Strain NRC‐1: identification of five new proteins. Journal of Bacteriology 186: 3182–3186.

Sivertsen AC, Bayro MJ, Belenky M et al. (2010) Solid‐state NMR characterization of gas vesicle structure. Biophysical Journal 99: 1932–1939.

So A‐K, Espie GS, Williams EB et al. (2004) A novel evolutionary lineage of carbonic anhydrase (ε‐class) is a component of the carboxysome shell. Journal of Bacteriology 186: 623–630.

Steinbüchel A (2001) Perspectives for biotechnological production and utilization of biopolymers: metabolic engineering of polyhydroxyalkanoate biosynthesis pathways as a successful example. Macromolecular Bioscience 1: 1–24.

Strunk T, Hamacher K, Hoffgaard F, et al. (2011) Model of the gas vesicle protein GvpA and analysis of GvpA mutants in vivo. Molecular Microbiology May 4. doi: 10.1111/j.1365‐2958.2011.07669.x. [Epub ahead of print].

Stuart ES, Morshed F, Sremac M et al. (2004) Cassette‐based presentation of SIV epitopes with recombinant gas vesicles from halophilic archaea. Journal of Biotechnology 114: 225–237.

Tabita FR (1999) Microbial ribulose 1,5‐bisphosphate carboxylase /oxygenase: a different perspective. Photosynthesis Research 60: 1–28.

Tanaka S, Kerfeld CA, Sawaya MR et al. (2008) Atomic‐level models of the bacterial carboxysome shell. Science 319: 1083–1086.

Thomas‐Keprta KL, Bazylinski DA, Kirschvink JL et al. (2000) Elongated prismatic magnetite (Fe3O4) crystals in ALH84001 carbonate globules: potential martian magnetofossils. Geochimical and Cosmochimical Acta 64: 4049–4081.

Uchino K, Saito B, Gebauer B et al. (2007) Isolated poly(3‐hydroxybutyrate) (PHB) granules are complex bacterial organelles catalyzing formation of PHB from acetyl‐CoA and degradation of PHB to acetyl‐CoA. Journal of Bacteriology 189: 8250–8256.

Wältermann M, Hinz A, Robenek H et al. (2005) Mechanism of lipid‐body formation in prokaryotes: how bacteria fatten up. Molecular Microbiology 55: 750–763.

Welte C, Hafner S, Krätzer C et al. (2009) Interaction between Sox proteins of two physiologically distinct bacteria and a new protein involved in thiosulfate oxidation. FEBS Letters 583: 1281–1286.

Wen J, Tsukatani Y, Cui W et al. (2011) Structural and spectroscopic insights of the FMO antenna protein of the aerobic chlorophototroph Candidatus Chloracidobacterium thermophilum. Biochimica Biophysica Acta 1807: 157–164.

Further Reading

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.

Frigaard N‐U and Dahl C (2009) Sulfur metabolism in phototrophic sulfur bacteria. Advances in Microbial Physiology 54: 103–200.

Jendrossek D (2009) Polyhydroxyalkanoate granules are complex subcellular organelles (carbonosomes). Journal of Bacteriology 191: 3195–3202.

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.

Preiss J (2009) Chapter 4.7.4, glycogen: biosynthesis and regulation. In: Ussery D, Böck A and Curtiss R III et al. (eds) EcoSal – E. coli and Salmonella: Cellular and Molecular Biology. Washington, DC: ASM Press. http://www.ecosal.org

Rao NN, Gómez‐García MR and Kornberg A (2009) Inorganic polyphosphate: essential for growth and survival. Annual Review of Biochemistry 78: 605–647.

Röttig A, Wenning L and Steinbüchel A (2010) Fatty acid alkyl esters: perspectives for production of alternatives biofuels. Applied Microbiology and Biotechnology 85: 1713–1734.

Schüler D (ed.) (2007) Microbiological Monographs Vol. 3: Magnetoreception and Magnetosomes in Bacteria, pp. 319. Berlin, Heidelberg: Springer‐Verlag.

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.

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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]