Molecular genetic and physical analysis of gas vesicles in buoyant enterobacteria.

Yosuke Tashiro,Rita E Monson,Joshua P Ramsay,George P C Salmond

doi:10.1111/1462-2920.13203

Yosuke Tashiro, Rita E Monson + Show 2 more

Open Access

https://doi.org/10.1111/1462-2920.13203

Copy DOI

Abstract

SummaryDifferent modes of bacterial taxis play important roles in environmental adaptation, survival, colonization and dissemination of disease. One mode of taxis is flotation due to the production of gas vesicles. Gas vesicles are proteinaceous intracellular organelles, permeable only to gas, that enable flotation in aquatic niches. Gene clusters for gas vesicle biosynthesis are partially conserved in various archaea, cyanobacteria, and some proteobacteria, such as the enterobacterium, S erratia sp. ATCC 39006 (S39006). Here we present the first systematic analysis of the genes required to produce gas vesicles in S39006, identifying how this differs from the archaeon H alobacterium salinarum. We define 11 proteins essential for gas vesicle production. Mutation of gvpN or gvpV produced small bicone gas vesicles, suggesting that the cognate proteins are involved in the morphogenetic assembly pathway from bicones to mature cylindrical forms. Using volumetric compression, gas vesicles were shown to comprise 17% of S39006 cells, whereas in E scherichia coli heterologously expressing the gas vesicle cluster in a deregulated environment, gas vesicles can occupy around half of cellular volume. Gas vesicle production in S39006 and E . coli was exploited to calculate the instantaneous turgor pressure within cultured bacterial cells; the first time this has been performed in either strain.

Highlights

Bacteria can use multiple modes of taxis, including swimming, twitching, swarming and flotation
This study presents a complete analysis of a single gas vesicle gene cluster and further demonstrates how gas vesicles can be exploited in E. coli, generating cells that are composed of ∼50% gas vesicles
sp. ATCC 39006 (S39006) has three genes, encoding isoforms of the primary gas vesicle structural protein, GvpA; this is consistent with six proteobacteria that possess a gas vesicle gene cluster

Summary

Introduction

Bacteria can use multiple modes of taxis, including swimming, twitching, swarming and flotation. Flotation is enabled through the regulated production of intracellular buoyancy chambers: gas vesicles. Gas vesicle-driven buoyancy facilitates the movement of photosynthetic cyanobacteria into water column positions, allowing exposure to wavelengths of light that can support phototrophy (Pfeifer, 2012). The primary gas vesicle structural protein, GvpA, assembles into tandem arrays that form ribs of the cylindrical vesicle (Englert and Pfeifer, 1993; Walsby, 1994). A second protein, GvpC, forms an exterior mesh on the gas vesicle surface, providing further structural support and influencing gas vesicle shape (Hayes et al, 1988; 1992; Walsby and Hayes, 1988; Englert and Pfeifer, 1993; Walsby, 1994; Offner et al, 2000). The precise biochemical roles of many other proteins found in gas vesicle gene clusters are unknown, their stoichiometry is thought to be important (Shukla and DasSarma, 2004; Chu et al, 2011; Pfeifer, 2012)

Results

Discussion

Conclusion