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Distribution, formation and regulation of gas vesicles

Key Points

  • Many bacteria and archaea synthesize intracellular gas-filled proteinaceous structures known as gas vesicles to act as flotation devices in aqueous environments.

  • Gas vesicles provide buoyancy to cells and might help cells survive under stress conditions. Large amounts of gas vesicles reduce the size of the cytoplasm and thereby increase the cell surface-to-volume ratio. Gas vesicles add hollow spaces to the cells, and these spaces are filled, by diffusion, with gases that are dissolved in the surrounding medium; no storage of gas occurs. Gas vesicles of cyanobacteria are permeable to oxygen, nitrogen, hydrogen, carbon dioxide, carbon monoxide, methane and even perfluorocyclobutane.

  • The archaeal gas vesicle wall is formed solely of protein, and the small hydrophobic protein gas vesicle protein A (GvpA) is the main constituent. Another structural protein is GvpC, which stabilizes the wall by attaching to the outside. In the halophilic archaeon Halobacterium salinarum, 12 additional Gvp proteins are required for gas vesicle formation, two of which, GvpD and GvpE, are involved in the regulation of gvp gene expression. GvpE increases transcription by 60–100-fold, whereas GvpD acts as a sink for GvpE. High salt concentrations, high cell densities or growth at low temperatures increase the formation of archaeal gas vesicles, whereas low salt concentrations, anoxic conditions or high light intensities decrease the production of these vesicles.

  • Bacterial gvp gene clusters share many of the essential gvp genes with haloarchaea, but also contain genes with no haloarchaeal homologues. The formation of bacterial gas vesicles is influenced by cell density and light intensities.

  • The formation of the gas vesicle wall is not yet fully understood. Initial information on the structure of GvpA came from solid-NMR studies and suggests a coil–α-helix–β-strand–β-strand–α-helix–coil peptide backbone. The GvpA monomer contains an antiparallel β-sheet (formed by the two β-strands), which might be extended by antiparallel associations with the β-sheets in adjacent monomers.

Abstract

A range of bacteria and archaea produce intracellular gas-filled proteinaceous structures that function as flotation devices in order to maintain a suitable depth in the aqueous environment. The wall of these gas vesicles is freely permeable to gas molecules and is composed of a small hydrophobic protein, GvpA, which forms a single-layer wall. In addition, several minor structural, accessory or regulatory proteins are required for gas vesicle formation. In different organisms, 8–14 genes encoding gas vesicle proteins have been identified, and their expression has been shown to be regulated by environmental factors. In this Review, I describe the basic properties of gas vesicles, the genes that encode them and how their production is regulated. I also discuss the function of these vesicles and the initial attempts to exploit them for biotechnological purposes.

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Figure 1: Gas vesicles: the basics.
Figure 2: Regulation of haloarchaeal gene clusters encoding gas vesicle proteins.
Figure 3: Gas vesicle protein-encoding gene clusters.
Figure 4: The sequence and structure of gas vesicle protein A.

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Acknowledgements

Research in the F.P. laboratory is supported by grants from the German Research Foundation (DFG). The author thanks A. Walsby for helpful comments on the manuscript, and A. Kletzin for discussions, help with the comparison of gvp gene clusters and critical reading of the manuscript.

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Glossary

Halophilic

Pertaining to microorganisms: salt-loving, living at 2–5 M sodium chloride at neutral pH.

Biconical

Pertaining to a three-dimensional geometric structure: formed by merging two conical ends.

Anoxygenic photosynthetic

Pertaining to microorganisms: unable to form oxygen owing to the lack of photosystem II.

Heterotrophic

Pertaining to microorganisms: using organic carbon sources.

Pellicle

A thin layer of microorganisms at the air–liquid surface.

Anoxic

Without oxygen.

Haloalkaliphilic

Pertaining to microorganisms: high-salt and high-pH loving, living at 2–5 M salt and pH 9–11.

Hypersaline

With a salt concentration surpassing that of the ocean water (>4% weight per volume).

Brackish

With a salt concentration between that of fresh water and ocean water.

Sporulation

The process of endospore formation in microorganisms.

Mini-chromosome

A piece of circular DNA that occurs in addition to the main chromosome and contains essential genes (such as tRNA genes) which are required to survive.

Insertion element

A transposable DNA sequence (0.5–2 kb) that is able to replicate and insert into another position in the chromosome.

Quorum sensing

A chemical communication system that uses small signal molecules to measure cell densities and coordinate the regulation of gene expression in certain bacteria and archaea.

Mycelium

The thread-like cells of Streptomyces spp.; these cells resemble the vegetative hyphae of fungi.

Antigen presentation system

A system of proteins that are engineered to display antigens to the immune system of mice or other animals.

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Pfeifer, F. Distribution, formation and regulation of gas vesicles. Nat Rev Microbiol 10, 705–715 (2012). https://doi.org/10.1038/nrmicro2834

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