Structure of the wall of Halobacterium halobium gas vesicles

doi:10.1016/0022-2836(76)90270-9

Journal of Molecular Biology

Volume 106, Issue 3, 25 September 1976, Pages 871-888

https://doi.org/10.1016/0022-2836(76)90270-9 Get rights and content

Abstract

The gas vesicles of Halobacterium halobium have been studied by recording X-ray diffraction patterns from both intact and collapsed vesicles. The wall is found to be remarkably thin; the average thickness is no more than 20 Å. Electron microscopy indicates that the wall consists of ribs, and the X-ray data confirm this. The thickness is therefore greater than 20 Å at some points and less at others. The X-ray data also indicate that the ribs on the two sides of the collapsed vesicle are intermeshed.

Our data indicate a large amount of β-sheet in the wall. The β-sheet consists of parallel (or anti-parallel) polypeptide chains which are regularly hydrogen-bonded to one another. This bonding locks the presumed subunit proteins into the wall, which is important for its function at the gas-liquid interface. The β-sheet is in two layers, one on top of the other. The two layers together can stiffen the wall and hence strengthen the vesicle against collapse.

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Gas vesicles are proteinous, lipid-free organelles commonly found in diverse prokaryotic species inhabiting aquatic environments, including both Archaea (halophiles, such as Halobacterium sp. NRC-1, and methanogens) and Bacteria (phototrophs and heterotrophs) (Blaurock and Wober, 1976; DasSarma and Arora, 1997; Krantz and Ballou, 1973; McMaster et al., 1996; Walsby, 1975). Ecological studies have shown that they aid in cell buoyancy processes, such as in the stratification of cyanobacterial and halobacterial species (which increases their ability to respire and photosynthesize), although their function in other microorganisms, such as methanogens and soil bacteria, is unclear (Bentley et al., 2002; Li and Cannon, 1998; Walsby, 1975; Zhilina and Zavarzin, 1979).
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Such a detailed description of the molecular and supramolecular organization is unique in the field of synthetic biomimetic assembly. This hierarchical peptide organization, completely new and not previously described for peptide self-assemblies, is very similar to the organization of the hydrophobic proteins forming the wall of the gas vesicles of Halobacterium halobium(36,37). Indeed, both the lanreotide nanotubes and the gas vesicles walls are bilayers formed by the lateral assembly of fibers formed by two protofilaments.
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A presentation vehicle was developed based on particulate gas vesicles produced by halophilic archaea. Gas vesicle epitope displays were prepared using standard coupling methods or recombinant DNA technology. When presented in the context of gas vesicle preparations, either the hapten, TNP, or a model six amino acid recombinant insert in the outer gas vesicle protein, GvpC was rendered immunogenic. Assays to quantify humoral responses indicated that each preparation elicited strong antibody responses in the absence of exogenous adjuvant. Thus, each preparation elicited a humoral response when injected into mice and this response was long lived and exhibited immunologic memory. Recombinant gas vesicle preparations therefore constitute a new, self-adjuvanting carrier/display vehicle for presentation of an array of peptidyl epitopes.
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This chapter reviews the functional inclusions in prokaryotic cells. Inclusions are visible expressions of cell metabolism. The inclusion is an integral part of the cell's metabolic machinery, it is important in adjusting the environment of the cell, thereby regulating certain metabolic events, or might represent a product of the cell's metabolism. Gas vesicles are rigid shells of protein that are found in a wide variety of prokaryotic organisms. The protein subunits of the gas vesicle have unique properties that enable their association to result in a structure that is impermeable to water. The genes encoding the structural components of the phycobilisome, gas vesicle, andthe genes for the enzymes involved in glycogen biosynthesis are cloned and sequenced. Site-directed mutagenesis provides valuable information relating to the molecular mechanisms of catalysis and allosteric regulation. The organization of the genes for a given inclusion is determined and is found to be clustered on the chromosome.
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^†: Present address: Department of Chemistry, California Institute of Technology, Pasadena, Calif. 91125, U.S.A.

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Journal of Molecular Biology

Structure of the wall of Halobacterium halobium gas vesicles

Abstract

J. Mol. Biol

J. Mol. Biol

J. Biol. Chem

J. Mol. Biol

Biophys. J

Biophys. J

Advan. Exp. Med. Biol